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  • 1
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    3D intrusions transport active surface microbial assemblages to the dark ocean (2024)
    National Academy of Sciences
    Details
    Publication Date: 2024-06-05
    Description: Significance Particulate organic carbon (POC) formed by photosynthesis in the sunlit surface ocean fuels the ecosystems in the dark ocean below. We show that mesoscale fronts and eddies, which are ubiquitous physical features in subtropical oceans, generate three-dimensional intrusions connecting the surface to deep ocean. Intrusions are enriched in total POC due to enhancement of small, nonsinking photosynthetic plankton and free-living bacteria that resemble surface microbial communities. Flow-driven export of POC, estimated using an approximation of eddy physics, is the same order of magnitude as export by sinking POC, which was previously thought to dominate export. These observations reveal coupling of surface and deep ocean productivity and biodiversity and give insight into mechanisms by which the ocean transports carbon to depth. Abstract Subtropical oceans contribute significantly to global primary production, but the fate of the picophytoplankton that dominate in these low-nutrient regions is poorly understood. Working in the subtropical Mediterranean, we demonstrate that subduction of water at ocean fronts generates 3D intrusions with uncharacteristically high carbon, chlorophyll, and oxygen that extend below the sunlit photic zone into the dark ocean. These contain fresh picophytoplankton assemblages that resemble the photic-zone regions where the water originated. Intrusions propagate depth-dependent seasonal variations in microbial assemblages into the ocean interior. Strikingly, the intrusions included dominant biomass contributions from nonphotosynthetic bacteria and enrichment of enigmatic heterotrophic bacterial lineages. Thus, the intrusions not only deliver material that differs in composition and nutritional character from sinking detrital particles, but also drive shifts in bacterial community composition, organic matter processing, and interactions between surface and deep communities. Modeling efforts paired with global observations demonstrate that subduction can flux similar magnitudes of particulate organic carbon as sinking export, but is not accounted for in current export estimates and carbon cycle models. Intrusions formed by subduction are a particularly important mechanism for enhancing connectivity between surface and upper mesopelagic ecosystems in stratified subtropical ocean environments that are expanding due to the warming climate.
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  • 2
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    Modes of Pangean lake level cyclicity driven by astronomical climate pacing modulated by continental position and p CO2 (2022)
    National Academy of Sciences
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    Publication Date: 2024-05-22
    Description: Orbital cyclicity is a fundamental pacemaker of Earth’s climate system. The Newark–Hartford Basin (NHB) lake sediment record of eastern North America contains compelling geologic expressions of this cyclicity, reflecting variations of climatic conditions in tropical Pangea during the Late Triassic and earliest Jurassic (~233 to 199 Ma). Climate modeling enables a deeper mechanistic understanding of Earth system modulation during this unique greenhouse and supercontinent period. We link major features of the NHB record to the combined climatic effects of orbital forcing, paleogeographic changes, and atmospheric p CO 2 variations. An ensemble of transient, orbitally driven climate simulations is assessed for nine time slices, three atmospheric p CO 2 values, and two paleogeographic reconstructions. Climatic transitions from tropical humid to more seasonal and ultimately semiarid are associated with tectonic drift of the NHB from ~ 5 ° N to 20 ° N . The modeled orbital modulation of the precipitation–evaporation balance is most pronounced during the 220 to 200 Ma interval, whereas it is limited by weak seasonality and increasing aridity before and after this interval. Lower p CO 2 at around 205 Ma contributes to drier climates and could have led to the observed damping of sediment cyclicity. Eccentricity-modulated precession dominates the orbitally driven climate response in the NHB region. High obliquity further amplifies summer precipitation through the seasonal shifts in the tropical rainfall belt. Regions with other proxy records are also assessed, providing guidance toward an integrated picture of global astronomical climate forcing in the Late Triassic and ultimately of other periods in Earth history.
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  • 3
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    A Late Pleistocene coastal ecosystem in French Guiana was hyperdiverse relative to today (2024)
    National Academy of Sciences
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    Publication Date: 2024-05-13
    Description: Warmer temperatures and higher sea level than today characterized the Last Interglacial interval [Pleistocene, 128 to 116 thousand years ago (ka)]. This period is a remarkable deep-time analog for temperature and sea-level conditions as projected for 2100 AD, yet there has been no evidence of fossil assemblages in the equatorial Atlantic. Here, we report foraminifer, metazoan (mollusks, bony fish, bryozoans, decapods, and sharks among others), and plant communities of coastal tropical marine and mangrove affinities, dating precisely from a ca. 130 to 115 ka time interval near the Equator, at Kourou, in French Guiana. These communities include ca. 230 recent species, some being endangered today and/or first recorded as fossils. The hyperdiverse Kourou mollusk assemblage suggests stronger affinities between Guianese and Caribbean coastal waters by the Last Interglacial than today, questioning the structuring role of the Amazon Plume on tropical Western Atlantic communities at the time. Grassland-dominated pollen, phytoliths, and charcoals from younger deposits in the same sections attest to a marine retreat and dryer conditions during the onset of the last glacial (ca. 110 to 50 ka), with a savanna-dominated landscape and episodes of fire. Charcoals from the last millennia suggest human presence in a mosaic of modern-like continental habitats. Our results provide key information about the ecology and biogeography of pristine Pleistocene tropical coastal ecosystems, especially relevant regarding the—widely anthropogenic—ongoing global warming.
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  • 4
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    Dynamics of Aggregates and Sinking Carbon Fluxes in a Turbulent Ocean (2024)
    National Academy of Sciences
    Details
    Publication Date: 2024-04-26
    Description: The sinking of particulate matter from the upper ocean dominates the export and sequestration of organic carbon by the biological pump, a critical component of the Earth's carbon cycle. Controls on carbon export are thought to be driven by ecological processes that produce and repackage sinking biogenic particles. Here, we present observations during the demise of the Northeast Atlantic Ocean spring bloom illustrating the importance of storm-induced turbulence on the dynamics of sinking particles. A sequence of four large storms caused upper layer mean turbulence levels to vary by more than three orders of magnitude. Large particle (>0.1 to 10 mm) abundance and size changed accordingly: increasing via shear coagulation when turbulence was moderate and decreasing rapidly when turbulence was intense due to shear disaggregation. Particle export was also tied to storm forcing as large particles were mixed to depth during mixed layer deepening. After the mixed layer shoaled, these particles, now isolated from intense surface mixing, grew larger and subsequently sank. This sequence of events matched the timing of sinking particle flux observations. Particle export was influenced by increases in aggregate abundance and porosity, which appeared to be enhanced by the repeated creation and destruction of aggregates. Last, particle transit efficiency through the mesopelagic zone was reduced by presumably biotic processes that created small particles (〈0.5 mm) from larger ones. Our results demonstrate that ocean turbulence significantly impacts the nature and dynamics of sinking particles, strongly influencing particle export and the efficiency of the biological pump.
    Type: Article , NonPeerReviewed
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  • 5
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    Evidence of nitrate-based nighttime atmospheric nucleation driven by marine microorganisms in the South Pacific (2023)
    National Academy of Sciences
    Details
    Publication Date: 2024-02-23
    Description: Significance Oceans represent 70% of our planet’s surface, housing a large spectrum of microorganisms that interact with the above atmosphere. Ocean microorganisms were proposed in the late 80’s to be at the center of a climate feedback loop involving dimethyl sulfide (DMS) that would form aerosols and modify cloud properties (CLAW hypothesis). In the present paper, we report observational evidence from semicontrolled experiments in the South Pacific that nitrate ions, yet hitherto not considered, is a key species involved in aerosol nucleation in the pristine marine atmosphere and which precursors are coemitted with DMS. Our results further indicate that nitrate ion formation would be related to short-term microbial processes, sensitive to environmental stressors, therefore potentially “closing the loop”. Abstract Our understanding of ocean–cloud interactions and their effect on climate lacks insight into a key pathway: do biogenic marine emissions form new particles in the open ocean atmosphere? Using measurements collected in ship-borne air–sea interface tanks deployed in the Southwestern Pacific Ocean, we identified new particle formation (NPF) during nighttime that was related to plankton community composition. We show that nitrate ions are the only species for which abundance could support NPF rates in our semicontrolled experiments. Nitrate ions also prevailed in the natural pristine marine atmosphere and were elevated under higher sub-10 nm particle concentrations. We hypothesize that these nucleation events were fueled by complex, short-term biogeochemical cycling involving the microbial loop. These findings suggest a new perspective with a previously unidentified role of nitrate of marine biogeochemical origin in aerosol nucleation.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
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  • 6
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    Denitrification in foraminifera has an ancient origin and is complemented by associated bacteria (2022)
    National Academy of Sciences
    Details
    Publication Date: 2024-02-07
    Description: Significance A substantial component of the global nitrogen cycle is the production of biologically inaccessible dinitrogen attributed to anaerobic denitrification by prokaryotes. Recent evidence identified a eukaryote, foraminifera, as new key players in this “loss” of bioavailable nitrogen. The evolution of denitrification in eukaryotes is a rare event, and the genetic mechanisms of the denitrification pathway in foraminifera are just starting to be elucidated. We present large-scale sequencing analyses of 10 denitrifying foraminiferal species, which reveals the high conservation of the foraminiferal denitrification pathway. We further find evidence for a complementation of denitrification by the foraminiferal microbiome. Together, these findings provide insights into the early evolution of a previously overlooked component in the marine nitrogen cycle. Abstract: Benthic foraminifera are unicellular eukaryotes that inhabit sediments of aquatic environments. Several foraminifera of the order Rotaliida are known to store and use nitrate for denitrification, a unique energy metabolism among eukaryotes. The rotaliid Globobulimina spp. has been shown to encode an incomplete denitrification pathway of bacterial origin. However, the prevalence of denitrification genes in foraminifera remains unknown, and the missing denitrification pathway components are elusive. Analyzing transcriptomes and metagenomes of 10 foraminiferal species from the Peruvian oxygen minimum zone, we show that denitrification genes are highly conserved in foraminifera. We infer the last common ancestor of denitrifying foraminifera, which enables us to predict the ability to denitrify for additional foraminiferal species. Additionally, an examination of the foraminiferal microbiota reveals evidence for a stable interaction with Desulfobacteraceae, which harbor genes that complement the foraminiferal denitrification pathway. Our results provide evidence that foraminiferal denitrification is complemented by the foraminifera-associated microbiome. The interaction of foraminifera with their resident bacteria is at the basis of foraminiferal adaptation to anaerobic environments that manifested in ecological success in oxygen depleted habitats.
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  • 7
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    Persistent deep water anoxia in the eastern South Atlantic during the last ice age (2021)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: During the last glacial interval, marine sediments recorded reduced current ventilation within the ocean interior below water depths of approximately 〉1,500 m [B. A. Hoogakker et al., Nat. Geosci. 8, 40–43 (2015)]. The degree of the associated oxygen depletion in the different ocean basins, however, is still poorly constrained. Here, we present sedimentary records of redox-sensitive metals from the southwest African margin. These records show evidence of continuous bottom water anoxia in the eastern South Atlantic during the last glaciation that led to enhanced carbon burial over a prolonged period of time. Our geochemical data indicate that upwelling-related productivity and the associated oxygen minimum zone in the eastern South Atlantic shifted far seaward during the last glacial period and only slowly retreated during deglaciation times. While increased productivity during the last ice age may have contributed to oxygen depletion in bottom waters, especially on the upper slope, slow-down of the Late Quaternary deep water circulation pattern [Rutberg et al., Nature 405, 935–938 (2000)] appears to be the ultimate driver of anoxic conditions in deep waters.
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  • 8
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    Long-term stability in the circumpolar foraging range of a Southern Ocean predator between the eras of whaling and rapid climate change (2023)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: Significance Assessing change in Southern Ocean ecosystems is challenging due to its remoteness. Large-scale datasets that allow comparison between present-day conditions and those prior to large-scale ecosystem disturbances caused by humans (e.g., fishing/whaling) are rare. We infer the contemporary offshore foraging distribution of a marine predator, southern right whales (n = 1,002), using a customized stable isotope-based assignment approach based on biogeochemical models of the Southern Ocean. We then compare the contemporary distributions during the late austral summer and autumn to whaling catch data representing historical distributions during the same seasons. We show remarkable consistency of mid-latitude distribution across four centuries but shifts in foraging grounds in the past 30 y, particularly in the high latitudes that are likely driven by climate-associated alterations in prey availability. Abstract Assessing environmental changes in Southern Ocean ecosystems is difficult due to its remoteness and data sparsity. Monitoring marine predators that respond rapidly to environmental variation may enable us to track anthropogenic effects on ecosystems. Yet, many long-term datasets of marine predators are incomplete because they are spatially constrained and/or track ecosystems already modified by industrial fishing and whaling in the latter half of the 20th century. Here, we assess the contemporary offshore distribution of a wide-ranging marine predator, the southern right whale (SRW, Eubalaena australis), that forages on copepods and krill from ~30°S to the Antarctic ice edge (〉60°S). We analyzed carbon and nitrogen isotope values of 1,002 skin samples from six genetically distinct SRW populations using a customized assignment approach that accounts for temporal and spatial variation in the Southern Ocean phytoplankton isoscape. Over the past three decades, SRWs increased their use of mid-latitude foraging grounds in the south Atlantic and southwest (SW) Indian oceans in the late austral summer and autumn and slightly increased their use of high-latitude (〉60°S) foraging grounds in the SW Pacific, coincident with observed changes in prey distribution and abundance on a circumpolar scale. Comparing foraging assignments with whaling records since the 18th century showed remarkable stability in use of mid-latitude foraging areas. We attribute this consistency across four centuries to the physical stability of ocean fronts and resulting productivity in mid-latitude ecosystems of the Southern Ocean compared with polar regions that may be more influenced by recent climate change.
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  • 9
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    Microbiome reduction and endosymbiont gain from a switch in sea urchin life history (2021)
    National Academy of Sciences
    Details
    Publication Date: 2024-02-07
    Description: Animal gastrointestinal tracts harbor a microbiome that is integral to host function, yet species from diverse phyla have evolved a reduced digestive system or lost it completely. Whether such changes are associated with alterations in the diversity and/or abundance of the microbiome remains an untested hypothesis in evolutionary symbiosis. Here, using the life history transition from planktotrophy (feeding) to lecithotrophy (nonfeeding) in the sea urchin Heliocidaris, we demonstrate that the lack of a functional gut corresponds with a reduction in microbial community diversity and abundance as well as the association with a diet-specific microbiome. We also determine that the lecithotroph vertically transmits a Rickettsiales that may complement host nutrition through amino acid biosynthesis and influence host reproduction. Our results indicate that the evolutionary loss of a functional gut correlates with a reduction in the microbiome and the association with an endosymbiont. Symbiotic transitions can therefore accompany life history transitions in the evolution of developmental strategies.
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  • 10
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    Rapid radiation in a highly diverse marine environment (2022)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: Significance: Adaptive radiation, the evolutionary process whereby a lineage diversifies over a short period of time, often occurs in geographically isolated or newly formed habitats where colonizing species encounter unoccupied niches and reduced selective pressures. Rapid radiations may also occur in diverse and complex environments, but these cases are less well documented. Here, we show that the hamlets, a group of Caribbean reef fishes, radiated within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. Genomic analysis suggests that color pattern diversity is generated by different combinations of alleles at a few genes with large effect. Such a modular genomic architecture of diversification is emerging as a common denominator to a variety of radiations. Abstract: Rapid diversification is often observed when founding species invade isolated or newly formed habitats that provide ecological opportunity for adaptive radiation. However, most of the Earth’s diversity arose in diverse environments where ecological opportunities appear to be more constrained. Here, we present a striking example of a rapid radiation in a highly diverse marine habitat. The hamlets, a group of reef fishes from the wider Caribbean, have radiated into a stunning diversity of color patterns but show low divergence across other ecological axes. Although the hamlet lineage is ∼26 My old, the radiation appears to have occurred within the last 10,000 generations in a burst of diversification that ranks among the fastest in fishes. As such, the hamlets provide a compelling backdrop to uncover the genomic elements associated with phenotypic diversification and an excellent opportunity to build a broader comparative framework for understanding the drivers of adaptive radiation. The analysis of 170 genomes suggests that color pattern diversity is generated by different combinations of alleles at a few large-effect loci. Such a modular genomic architecture of diversification has been documented before in Heliconius butterflies, capuchino finches, and munia finches, three other tropical radiations that took place in highly diverse and complex environments. The hamlet radiation also occurred in a context of high effective population size, which is typical of marine populations. This allows for the accumulation of new variants through mutation and the retention of ancestral genetic variation, both of which appear to be important in this radiation.
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  • 11
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    Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader (2021)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: Significance: A central goal in invasion genomics is to identify and determine the mechanisms that underlie the successful colonization, establishment, and subsequent range expansion of invasive populations of nonindigenous species. Using a whole-genome approach, we evaluate the importance of genetic diversity for the successful establishment of nonindigenous species. Our study shows that genetic diversity per se is not the major factor driving invasions, since we observed all possible scenarios with invasive populations showing reduced, similar but also increased, genetic diversity relative to the native population. Using coalescent methods, we reconstruct the demographic history of the invasion and infer the source population of each invasion event, which shows that propagule pressure and multiple introductions play an important role in determining invasion success. Abstract: Invasion rates have increased in the past 100 y irrespective of international conventions. What characterizes a successful invasion event? And how does genetic diversity translate into invasion success? Employing a whole-genome perspective using one of the most successful marine invasive species world-wide as a model, we resolve temporal invasion dynamics during independent invasion events in Eurasia. We reveal complex regionally independent invasion histories including cases of recurrent translocations, time-limited translocations, and stepping-stone range expansions with severe bottlenecks within the same species. Irrespective of these different invasion dynamics, which lead to contrasting patterns of genetic diversity, all nonindigenous populations are similarly successful. This illustrates that genetic diversity, per se, is not necessarily the driving force behind invasion success. Other factors such as propagule pressure and repeated introductions are an important contribution to facilitate successful invasions. This calls into question the dominant paradigm of the genetic paradox of invasions, i.e., the successful establishment of nonindigenous populations with low levels of genetic diversity.
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  • 12
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    Choanoflagellates alongside diverse uncultured predatory protists consume the abundant open-ocean cyanobacterium Prochlorococcus (2023)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: Prochlorococcus is a key member of open-ocean primary producer communities. Despite its importance, little is known about the predators that consume this cyanobacterium and make its biomass available to higher trophic levels. We identify potential predators along a gradient wherein Prochlorococcus abundance increased from near detection limits (coastal California) to 〉200,000 cells mL-1 (subtropical North Pacific Gyre). A replicated RNA-Stable Isotope Probing experiment involving the in situ community, and labeled Prochlorococcus as prey, revealed choanoflagellates as the most active predators of Prochlorococcus, alongside a radiolarian, chrysophytes, dictyochophytes, and specific MAST lineages. These predators were not appropriately highlighted in multiyear conventional 18S rRNA gene amplicon surveys where dinoflagellates and other taxa had highest relative amplicon abundances across the gradient. In identifying direct consumers of Prochlorococcus, we reveal food-web linkages of individual protistan taxa and resolve routes of carbon transfer from the base of marine food webs.
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  • 13
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    Spiny and soft-rayed fin domains in acanthomorph fish are established through a BMP-gremlin-shh signaling network (2021)
    National Academy of Sciences
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    Publication Date: 2024-02-07
    Description: With over 18,000 species, the Acanthomorpha, or spiny-rayed fishes, form the largest and arguably most diverse radiation of vertebrates. One of the key novelties that contributed to their evolutionary success are the spiny rays in their fins that serve as a defense mechanism. We investigated the patterning mechanisms underlying the differentiation of median fin Anlagen into discrete spiny and soft rayed domains during the ontogeny of the direct-developing cichlid fish Astatotilapia burtoni. Distinct transcription factor signatures characterize these two fin domains, whereby mutually exclusive expression of hoxa13a/b with alx4a/b and tbx2b marks the spine to soft-ray boundary. The soft-ray domain is established by BMP inhibition via gremlin1b, which synergizes in the posterior fin with shh secreted from a zone of polarizing activity. Modulation of BMP signaling by chemical inhibition or gremlin1b CRISPR/Cas9 knockout induces homeotic transformations of spines into soft rays and vice versa. The expression of spine and soft-ray genes in nonacanthomorph fins indicates that a combination of exaptation and posterior expansion of an ancestral developmental program for the anterior fin margin allowed the evolution of robustly individuated spiny and soft-rayed domains. We propose that a repeated exaptation of such pattern might underly the convergent evolution of anterior spiny fin elements across fishes.
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  • 14
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    Experimental evolution reveals the synergistic genomic mechanisms of adaptation to ocean warming and acidification in a marine copepod (2022)
    National Academy of Sciences
    Details
    Publication Date: 2024-02-07
    Description: Significance Resilience to global change will require adaptation to multiple concurrent environmental changes. However, it is unclear if adaptations to multiple stressors can be predicted from the sum of single-stressor adaptation. To answer this question, we experimentally evolved a marine copepod to warming, acidification, and their combination, finding that copepods were able to adapt to all conditions over 25 generations. Warming was a much stronger selective pressure than acidification alone and under multiple-stressor conditions. Nevertheless, the multiple-stressor response to selection was synergistic and unique from either single stressor. Thus, adaptation to single stressors may not reveal adaptive potential or mechanisms of adaptation under multiple stressors, demonstrating the complexity of predicting adaptive responses under multifaceted environmental change. Abstract Metazoan adaptation to global change relies on selection of standing genetic variation. Determining the extent to which this variation exists in natural populations, particularly for responses to simultaneous stressors, is essential to make accurate predictions for persistence in future conditions. Here, we identified the genetic variation enabling the copepod Acartia tonsa to adapt to experimental ocean warming, acidification, and combined ocean warming and acidification (OWA) over 25 generations of continual selection. Replicate populations showed a consistent polygenic response to each condition, targeting an array of adaptive mechanisms including cellular homeostasis, development, and stress response. We used a genome-wide covariance approach to partition the allelic changes into three categories: selection, drift and replicate-specific selection, and laboratory adaptation responses. The majority of allele frequency change in warming (57%) and OWA (63%) was driven by shared selection pressures across replicates, but this effect was weaker under acidification alone (20%). OWA and warming shared 37% of their response to selection but OWA and acidification shared just 1%, indicating that warming is the dominant driver of selection in OWA. Despite the dominance of warming, the interaction with acidification was still critical as the OWA selection response was highly synergistic with 47% of the allelic selection response unique from either individual treatment. These results disentangle how genomic targets of selection differ between single and multiple stressors and demonstrate the complexity that nonadditive multiple stressors will contribute to predictions of adaptation to complex environmental shifts caused by global change.
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  • 15
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    A metabologenomics approach to unlock the metabolome of the novel Antarctic deep-sea isolate Lacinutrix shetlandiensis sp. nov. WUR7 (2023)
    National Academy of Sciences
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    Publication Date: 2024-01-08
    Description: The South Shetland Trough, Antarctica, is an underexplored region for microbiological and biotechnological exploitation. Herein, we describe the isolation and characterization of the novel bacterium Lacinutrix shetlandiensis sp. nov. WUR7 from a deep-sea environment. We explored its chemical diversity via a metabologenomics approach, wherein the OSMAC strategy was strategically employed to upregulate cryptic genes for secondary metabolite production. Based on hybrid de novo whole genome sequencing and digital DNA–DNA hybridization, isolate WUR7 was identified as a novel species from the Gram-negative genus Lacinutrix. Its genome was mined for the presence of biosynthetic gene clusters with limited results. However, extensive investigation of its metabolism uncovered an unusual tryptophan decarboxylase with high sequence homology and conserved structure of the active site as compared to ZP_02040762, a highly specific tryptophan decarboxylase from Ruminococcus gnavus. Therefore, WUR7's metabolism was directed toward indole-based alkaloid biosynthesis by feeding it with L-tryptophan. As expected, its metabolome profile changed dramatically, by triggering the extracellular accumulation of a massive array of metabolites unexpressed in the absence of tryptophan. Untargeted LC-MS/MS coupled with molecular networking, followed along with chemoinformatic dereplication, allowed for the annotation of 10 indole alkaloids, belonging to β-carboline, bisindole, and monoindole classes, alongside several unknown alkaloids. These findings guided us to the isolation of a new natural bisindole alkaloid 8,9-dihydrocoscinamide B (1), as the first alkaloid from the genus Lacinutrix, whose structure was elucidated on the basis of extensive 1D and 2D NMR and HR-ESIMS experiments. This comprehensive strategy allowed us to unlock the previously unexploited metabolome of L. shetlandiensis sp. nov. WUR7.
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  • 16
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    Changes in biogenic carbon flow in response to sea surface warming (2009)
    National Academy of Sciences
    Details
    Publication Date: 2023-11-08
    Description: The pelagic ocean harbors one of the largest ecosystems on Earth. It is responsible for approximately half of global primary production, sustains worldwide fisheries, and plays an important role in the global carbon cycle. Ocean warming caused by anthropogenic climate change is already starting to impact the marine biota, with possible consequences for ocean productivity and ecosystem services. Because temperature sensitivities of marine autotrophic and heterotrophic processes differ greatly, ocean warming is expected to cause major shifts in the flow of carbon and energy through the pelagic system. Attempts to integrate such biological responses into marine ecosystem and biogeochemical models suffer from a lack of empirical data. Here, we show, using an indoor-mesocosm approach, that rising temperature accelerates respiratory consumption of organic carbon relative to autotrophic production in a natural plankton community. Increasing temperature by 2-6 degrees C hence decreased the biological drawdown of dissolved inorganic carbon in the surface layer by up to 31%. Moreover, warming shifted the partitioning between particulate and dissolved organic carbon toward an enhanced accumulation of dissolved compounds. In line with these findings, the loss of organic carbon through sinking was significantly reduced at elevated temperatures. The observed changes in biogenic carbon flow have the potential to reduce the transfer of primary produced organic matter to higher trophic levels, weaken the ocean's biological carbon pump, and hence provide a positive feedback to rising atmospheric CO2.
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  • 17
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    The magnitude and impact of the 431 CE Tierra Blanca Joven eruption of Ilopango, El Salvador (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-10-26
    Description: The Tierra Blanca Joven (TBJ) eruption from Ilopango volcano deposited thick ash over much of El Salvador when it was inhabited by the Maya, and rendered all areas within at least 80 km of the volcano uninhabitable for years to decades after the eruption. Nonetheless, the more widespread environmental and climatic impacts of this large eruption are not well known because the eruption magnitude and date are not well constrained. In this multifaceted study we have resolved the date of the eruption to 431 ± 2 CE by identifying the ash layer in a well-dated, high-resolution Greenland ice-core record that is 〉7,000 km from Ilopango; and calculated that between 37 and 82 km3 of magma was dispersed from an eruption coignimbrite column that rose to ∼45 km by modeling the deposit thickness using state-of-the-art tephra dispersal methods. Sulfate records from an array of ice cores suggest stratospheric injection of 14 ± 2 Tg S associated with the TBJ eruption, exceeding those of the historic eruption of Pinatubo in 1991. Based on these estimates it is likely that the TBJ eruption produced a cooling of around 0.5 °C for a few years after the eruption. The modeled dispersal and higher sulfate concentrations recorded in Antarctic ice cores imply that the cooling would have been more pronounced in the Southern Hemisphere. The new date confirms the eruption occurred within the Early Classic phase when Maya expanded across Central America.
    Description: Published
    Description: 26061-26068
    Description: 1V. Storia eruttiva
    Description: JCR Journal
    Keywords: Maya; eruption dispersal; large volcanic eruptions; radiocarbon; sulfate
    Repository Name: Istituto Nazionale di Geofisica e Vulcanologia (INGV)
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    The strength of the Earth's magnetic field from Pre-Pottery to Pottery Neolithic, Jordan (2023)
    National Academy of Sciences
    Details
    Publication Date: 2023-10-26
    Description: Constraining secular variation of the Earth's magnetic field strength in the past is fundamental to understanding short-term processes of the geodynamo. Such records also constitute a powerful and independent dating tool for archaeological sites and geological formations. In this study, we present 11 robust archaeointensity results from Pre-Pottery to Pottery Neolithic Jordan that are based on both clay and flint (chert) artifacts. Two of these results constitute the oldest archaeointensity data for the entire Levant, ancient Egypt, Turkey, and Mesopotamia, extending the archaeomagnetic reference curve for the Holocene. Virtual Axial Dipole Moments (VADMs) show that the Earth's magnetic field in the Southern Levant was weak (about two-thirds the present field) at around 7600 BCE, recovering its strength to greater than the present field around 7000 BCE, and gradually weakening again around 5200 BCE. In addition, successful results obtained from burnt flint demonstrate the potential of this very common, and yet rarely used, material in archaeomagnetic research, in particular for prehistoric periods from the first use of fire to the invention of pottery.
    Description: Published
    Description: e2100995118
    Description: 1A. Geomagnetismo e Paleomagnetismo
    Description: JCR Journal
    Keywords: Jordan ; Neolithic ; Pre-Pottery Neolithic ; archaeointensity
    Repository Name: Istituto Nazionale di Geofisica e Vulcanologia (INGV)
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    Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean (2023)
    National Academy of Sciences
    Details
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Saunders, J. K., McIlvin, M. R., Dupont, C. L., Kaul, D., Moran, D. M., Horner, T., Laperriere, S. M., Webb, E. A., Bosak, T., Santoro, A. E., & Saito, M. A. Microbial functional diversity across biogeochemical provinces in the central Pacific Ocean. Proceedings of the National Academy of Sciences of the United States of America, 119(37),(2022): e2200014119, https://doi.org/10.1073/pnas.2200014119.
    Description: Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.
    Description: Funding for this research was provided by the Gordon and Betty Moore Foundation (grants 3782 and 8453), the US NSF (NSF grants OCE-1924554, 2123055, 2125063, 2048774, and 2026933), the Center for Chemical Currencies on a Microbial Planet (NSF grant OCE-2019589), and the US NIH General Medicine (grant GM135709-01A1). J.K.S. was supported by a NASA Postdoctoral Program Fellowship with the NASA Astrobiology Program, administered by Universities Space Research Association under contract with NASA. A.E.S. was supported by the Sloan Foundation, the Simons Foundation, and NSF grant OCE-1437310. A portion of this research used resources at the US Department of Energy JGI sponsored by the Office of Biological and Environmental Research and operated under contract DE-AC02-05CH11231 (JGI). C.L.D. and D.K. were supported by NSF grants OCE-1558453 and OCE-2049299. T.H. was supported by NSF grant OCE-2023456.
    Keywords: Marine microbial ecology ; Metaproteomics ; Mesopelagic ; Nitrification ; Methylotrophy
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    Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows (2022)
    National Academy of Sciences
    Details
    Publication Date: 2023-03-08
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Schorn, S., Ahmerkamp, S., Bullock, E., Weber, M., Lott, C., Liebeke, M., Lavik, G., Kuypers, M. M. M., Graf, J. S., & Milucka, J. Diverse methylotrophic methanogenic archaea cause high methane emissions from seagrass meadows. Proceedings of the National Academy of Sciences of the United States of America, 119(9), (2022): e2106628119, https://doi.org/10.1073/pnas.2106628119.
    Description: Marine coastlines colonized by seagrasses are a net source of methane to the atmosphere. However, methane emissions from these environments are still poorly constrained, and the underlying processes and responsible microorganisms remain largely unknown. Here, we investigated methane turnover in seagrass meadows of Posidonia oceanica in the Mediterranean Sea. The underlying sediments exhibited median net fluxes of methane into the water column of ca. 106 µmol CH4 ⋅ m−2 ⋅ d−1. Our data show that this methane production was sustained by methylated compounds produced by the plant, rather than by fermentation of buried organic carbon. Interestingly, methane production was maintained long after the living plant died off, likely due to the persistence of methylated compounds, such as choline, betaines, and dimethylsulfoniopropionate, in detached plant leaves and rhizomes. We recovered multiple mcrA gene sequences, encoding for methyl-coenzyme M reductase (Mcr), the key methanogenic enzyme, from the seagrass sediments. Most retrieved mcrA gene sequences were affiliated with a clade of divergent Mcr and belonged to the uncultured Candidatus Helarchaeota of the Asgard superphylum, suggesting a possible involvement of these divergent Mcr in methane metabolism. Taken together, our findings identify the mechanisms controlling methane emissions from these important blue carbon ecosystems.
    Description: This project was funded by theMax Planck Society.
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    Discovery of widely available abyssal rock patches reveals overlooked habitat type and prompts rethinking deep-sea biodiversity (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: Habitat heterogeneity and species diversity are often linked. On the deep seafloor, sediment variability and hard-substrate availability influence geographic patterns of species richness and turnover. The assumption of a generally homogeneous, sedimented abyssal seafloor is at odds with the fact that the faunal diversity in some abyssal regions exceeds that of shallow-water environments. Here we show, using a ground-truthed analysis of multibeam sonar data, that the deep seafloor may be much rockier than previously assumed. A combination of bathymetry data, ruggedness, and backscatter from a trans-Atlantic corridor along the Vema Fracture Zone, covering crustal ages from 0 to 100 Ma, show rock exposures occurring at all crustal ages. Extrapolating to the whole Atlantic, over 260,000 km2 of rock habitats potentially occur along Atlantic fracture zones alone, significantly increasing our knowledge about abyssal habitat heterogeneity. This implies that sampling campaigns need to be considerably more sophisticated than at present to capture the full deep-sea habitat heterogeneity and biodiversity.
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    Natural variability of the Arctic Ocean sea ice during the present interglacial (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: The impact of the ongoing anthropogenic warming on the Arctic Ocean sea ice is ascertained and closely monitored. However, its long-term fate remains an open question as its natural variability on centennial to millennial timescales is not well documented. Here, we use marine sedimentary records to reconstruct Arctic sea-ice fluctuations. Cores collected along the Lomonosov Ridge that extends across the Arctic Ocean from northern Greenland to the Laptev Sea were radiocarbon dated and analyzed for their micropaleontological and palynological contents, both bearing information on the past sea-ice cover. Results demonstrate that multiyear pack ice remained a robust feature of the western and central Lomonosov Ridge and that perennial sea ice remained present throughout the present interglacial, even during the climate optimum of the middle Holocene that globally peaked ∼6,500 y ago. In contradistinction, the southeastern Lomonosov Ridge area experienced seasonally sea-ice-free conditions, at least, sporadically, until about 4,000 y ago. They were marked by relatively high phytoplanktonic productivity and organic carbon fluxes at the seafloor resulting in low biogenic carbonate preservation. These results point to contrasted west–east surface ocean conditions in the Arctic Ocean, not unlike those of the Arctic dipole linked to the recent loss of Arctic sea ice. Hence, our data suggest that seasonally ice-free conditions in the southeastern Arctic Ocean with a dominant Arctic dipolar pattern, may be a recurrent feature under “warm world” climate.
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    Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: A fundamental problem for the evolution of pregnancy, the most specialized form of parental investment among vertebrates, is the rejection of the nonself-embryo. Mammals achieve immunological tolerance by down-regulating both major histocompatibility complex pathways (MHC I and II). Although pregnancy has evolved multiple times independently among vertebrates, knowledge of associated immune system adjustments is restricted to mammals. All of them (except monotremata) display full internal pregnancy, making evolutionary reconstructions within the class mammalia meaningless. Here, we study the seahorse and pipefish family (syngnathids) that have evolved male pregnancy across a gradient from external oviparity to internal gestation. We assess how immunological tolerance is achieved by reconstruction of the immune gene repertoire in a comprehensive sample of 12 seahorse and pipefish genomes along the “male pregnancy” gradient together with expression patterns of key immune and pregnancy genes in reproductive tissues. We found that the evolution of pregnancy coincided with a modification of the adaptive immune system. Divergent genomic rearrangements of the MHC II pathway among fully pregnant species were identified in both genera of the syngnathids: The pipefishes (Syngnathus) displayed loss of several genes of the MHC II pathway while seahorses (Hippocampus) featured a highly divergent invariant chain (CD74). Our findings suggest that a trade-off between immunological tolerance and embryo rejection accompanied the evolution of unique male pregnancy. That pipefishes survive in an ocean of microbes without one arm of the adaptive immune defense suggests a high degree of immunological flexibility among vertebrates, which may advance our understanding of immune-deficiency diseases.
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    Global reconstruction reduces the uncertainty of oceanic nitrous oxide emissions and reveals a vigorous seasonal cycle (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: Assessment of the global budget of the greenhouse gas nitrous oxide ([Formula: see text]O) is limited by poor knowledge of the oceanic [Formula: see text]O flux to the atmosphere, of which the magnitude, spatial distribution, and temporal variability remain highly uncertain. Here, we reconstruct climatological [Formula: see text]O emissions from the ocean by training a supervised learning algorithm with over 158,000 [Formula: see text]O measurements from the surface ocean-the largest synthesis to date. The reconstruction captures observed latitudinal gradients and coastal hot spots of [Formula: see text]O flux and reveals a vigorous global seasonal cycle. We estimate an annual mean [Formula: see text]O flux of 4.2 ± 1.0 Tg N[Formula: see text], 64% of which occurs in the tropics, and 20% in coastal upwelling systems that occupy less than 3% of the ocean area. This [Formula: see text]O flux ranges from a low of 3.3 ± 1.3 Tg N[Formula: see text] in the boreal spring to a high of 5.5 ± 2.0 Tg N[Formula: see text] in the boreal summer. Much of the seasonal variations in global [Formula: see text]O emissions can be traced to seasonal upwelling in the tropical ocean and winter mixing in the Southern Ocean. The dominant contribution to seasonality by productive, low-oxygen tropical upwelling systems (〉75%) suggests a sensitivity of the global [Formula: see text]O flux to El Niño-Southern Oscillation and anthropogenic stratification of the low latitude ocean. This ocean flux estimate is consistent with the range adopted by the Intergovernmental Panel on Climate Change, but reduces its uncertainty by more than fivefold, enabling more precise determination of other terms in the atmospheric [Formula: see text]O budget.
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    Latitudinal gradient in the respiration quotient and the implications for ocean oxygen availability (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: Climate-driven depletion of ocean oxygen strongly impacts the global cycles of carbon and nutrients as well as the survival of many animal species. One of the main uncertainties in predicting changes to marine oxygen levels is the regulation of the biological respiration demand associated with the biological pump. Derived from the Redfield ratio, the molar ratio of oxygen to organic carbon consumed during respiration (i.e., the respiration quotient, r−O2:C) is consistently assumed constant but rarely, if ever, measured. Using a prognostic Earth system model, we show that a 0.1 increase in the respiration quotient from 1.0 leads to a 2.3% decline in global oxygen, a large expansion of low-oxygen zones, additional water column denitrification of 38 Tg N/y, and the loss of fixed nitrogen and carbon production in the ocean. We then present direct chemical measurements of r−O2:C using a Pacific Ocean meridional transect crossing all major surface biome types. The observed r−O2:C has a positive correlation with temperature, and regional mean values differ significantly from Redfield proportions. Finally, an independent global inverse model analysis constrained with nutrients, oxygen, and carbon concentrations supports a positive temperature dependence of r−O2:C in exported organic matter. We provide evidence against the common assumption of a static biological link between the respiration of organic carbon and the consumption of oxygen. Furthermore, the model simulations suggest that a changing respiration quotient will impact multiple biogeochemical cycles and that future warming can lead to more intense deoxygenation than previously anticipated.
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    Opinion: We need a global movement to transform ocean science for a better world (2020)
    National Academy of Sciences
    Details
    Publication Date: 2023-02-08
    Description: The ocean is our planet’s largest life-support system. It stabilizes climate; stores carbon; produces oxygen; nurtures biodiversity; directly supports human well-being through food, mineral, and energy resources; and provides cultural and recreational services. The value of the ocean economy speaks to its importance: The Organization for Economic Cooperation and Development (OECD) estimates that by 2030, $3 trillion USD will be generated annually from ocean sectors such as transportation, fishing, tourism, and energy (1). Unsustainable resource extraction, pollution, climate change, and habitat destruction are on the rise and affecting many parts of the world’s oceans (2). The ocean is rapidly changing, and yet the ways in which these changes will play out are not yet clear.
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  • 27
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    The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-11-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Orvis, J., Albertin, C., Shrestha, P., Chen, S., Zheng, M., Rodriguez, C., Tallon, L., Mahurkar, A., Zimin, A., Kim, M., Liu, K., Kandel, E., Fraser, C., Sossin, W., & Abrams, T. The evolution of synaptic and cognitive capacity: insights from the nervous system transcriptome of Aplysia. Proceedings of the National Academy of Sciences of the United States of America, 119(28), (2022): e2122301119, https://doi.org/10.1073/pnas.2122301119.
    Description: The gastropod mollusk Aplysia is an important model for cellular and molecular neurobiological studies, particularly for investigations of molecular mechanisms of learning and memory. We developed an optimized assembly pipeline to generate an improved Aplysia nervous system transcriptome. This improved transcriptome enabled us to explore the evolution of cognitive capacity at the molecular level. Were there evolutionary expansions of neuronal genes between this relatively simple gastropod Aplysia (20,000 neurons) and Octopus (500 million neurons), the invertebrate with the most elaborate neuronal circuitry and greatest behavioral complexity? Are the tremendous advances in cognitive power in vertebrates explained by expansion of the synaptic proteome that resulted from multiple rounds of whole genome duplication in this clade? Overall, the complement of genes linked to neuronal function is similar between Octopus and Aplysia. As expected, a number of synaptic scaffold proteins have more isoforms in humans than in Aplysia or Octopus. However, several scaffold families present in mollusks and other protostomes are absent in vertebrates, including the Fifes, Lev10s, SOLs, and a NETO family. Thus, whereas vertebrates have more scaffold isoforms from select families, invertebrates have additional scaffold protein families not found in vertebrates. This analysis provides insights into the evolution of the synaptic proteome. Both synaptic proteins and synaptic plasticity evolved gradually, yet the last deuterostome-protostome common ancestor already possessed an elaborate suite of genes associated with synaptic function, and critical for synaptic plasticity.
    Description: This work was supported by NSF EAGER Award IOS-1255695 and NIH grant R01 MH 55880 grant to T.W.A.; by a Natural Sciences and Engineering Research Council of Canada Discovery grant and Canadian Institutes of Health Research project grant 340328 to W.S.; by funding from the HHMI to E.R.K.; and by a Hibbitt Early Career Fellowship to C.A. W.S. is James McGill Professor at McGill University.
    Keywords: Neural plasticity ; Synaptic plasticity ; Evolution ; Neuromodulation ; Aplysia
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    Discovery of active off-axis hydrothermal vents at 9° 54’N East Pacific Rise (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-11-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McDermott, J. M., Parnell-Turner, R., Barreyre, T., Herrera, S., Downing, C. C., Pittoors, N. C., Pehr, K., Vohsen, S. A., Dowd, W. S., Wu, J.-N., Marjanović, M., & Fornari, D. J. Discovery of active off-axis hydrothermal vents at 9° 54’N East Pacific Rise. Proceedings of the National Academy of Sciences of the United States of America, 119(30), (2022): e2205602119, https://doi.org/10.1073/pnas.2205602119.
    Description: Comprehensive knowledge of the distribution of active hydrothermal vent fields along midocean ridges is essential to understanding global chemical and heat fluxes and endemic faunal distributions. However, current knowledge is biased by a historical preference for on-axis surveys. A scarcity of high-resolution bathymetric surveys in off-axis regions limits vent identification, which implies that the number of vents may be underestimated. Here, we present the discovery of an active, high-temperature, off-axis hydrothermal field on a fast-spreading ridge. The vent field is located 750 m east of the East Pacific Rise axis and ∼7 km north of on-axis vents at 9° 50′N, which are situated in a 50- to 100-m-wide trough. This site is currently the largest vent field known on the East Pacific Rise between 9 and 10° N. Its proximity to a normal fault suggests that hydrothermal fluid pathways are tectonically controlled. Geochemical evidence reveals deep fluid circulation to depths only 160 m above the axial magma lens. Relative to on-axis vents at 9° 50′N, these off-axis fluids attain higher temperatures and pressures. This tectonically controlled vent field may therefore exhibit greater stability in fluid composition, in contrast to more dynamic, dike-controlled, on-axis vents. The location of this site indicates that high-temperature convective circulation cells extend to greater distances off axis than previously realized. Thorough high-resolution mapping is necessary to understand the distribution, frequency, and physical controls on active off-axis vent fields so that their contribution to global heat and chemical fluxes and role in metacommunity dynamics can be determined.
    Description: Financial support was provided by the NSF Awards OCE-1949938 (to J.M.M.), OCE-1948936 (to R.P.-T.), and OCE-1949485 (to D.J.F. and T.B.).
    Keywords: Hydrothermal activity ; Midocean ridge ; Ocean chemistry ; Chemosynthetic ecosystem ; East Pacific Rise
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    Molecular profiling of single neurons of known identity in two ganglia from the crab Cancer borealis (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-31
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Northcutt, A. J., Kick, D. R., Otopalik, A. G., Goetz, B. M., Harris, R. M., Santin, J. M., Hofmann, H. A., Marder, E., & Schulz, D. J. Molecular profiling of single neurons of known identity in two ganglia from the crab Cancer borealis. Proceedings of the National Academy of Sciences of the United States of America, 116 (52) (2019): 26980-26990, doi: 10.1073/pnas.1911413116.
    Description: Understanding circuit organization depends on identification of cell types. Recent advances in transcriptional profiling methods have enabled classification of cell types by their gene expression. While exceptionally powerful and high throughput, the ground-truth validation of these methods is difficult: If cell type is unknown, how does one assess whether a given analysis accurately captures neuronal identity? To shed light on the capabilities and limitations of solely using transcriptional profiling for cell-type classification, we performed 2 forms of transcriptional profiling—RNA-seq and quantitative RT-PCR, in single, unambiguously identified neurons from 2 small crustacean neuronal networks: The stomatogastric and cardiac ganglia. We then combined our knowledge of cell type with unbiased clustering analyses and supervised machine learning to determine how accurately functionally defined neuron types can be classified by expression profile alone. The results demonstrate that expression profile is able to capture neuronal identity most accurately when combined with multimodal information that allows for post hoc grouping, so analysis can proceed from a supervised perspective. Solely unsupervised clustering can lead to misidentification and an inability to distinguish between 2 or more cell types. Therefore, this study supports the general utility of cell identification by transcriptional profiling, but adds a caution: It is difficult or impossible to know under what conditions transcriptional profiling alone is capable of assigning cell identity. Only by combining multiple modalities of information such as physiology, morphology, or innervation target can neuronal identity be unambiguously determined.
    Description: We thank members of the D.J.S., H.A.H., and E.M. laboratories for helpful discussions. We thank the Genomic Sequencing and Analysis Facility (The University of Texas [UT] at Austin) for library preparation and sequencing and the bioinformatics consulting team at the UT Austin Center for Computational Biology and Bioinformatics for helpful advice. This work was supported by National Institutes of Health grant R01MH046742-29 (to E.M. and D.J.S.) and the National Institute of General Medical Sciences T32GM008396 (support for A.J.N.) and National Institute of Mental Health grant 5R25MH059472-18 and the Grass Foundation (support for Neural Systems and Behavior Course at the Marine Biological Laboratory).
    Keywords: qPCR ; RNA-seq ; Stomatogastric ; Expression profiling
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    Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Peredo, E. L., & Cardon, Z. G. Shared up-regulation and contrasting down-regulation of gene expression distinguish desiccation-tolerant from intolerant green algae. Proceedings of the National Academy of Sciences of the United States of America, 117(29), 1(2020): 7438-17445, doi:10.1073/pnas.1906904117.
    Description: Among green plants, desiccation tolerance is common in seeds and spores but rare in leaves and other vegetative green tissues. Over the last two decades, genes have been identified whose expression is induced by desiccation in diverse, desiccation-tolerant (DT) taxa, including, e.g., late embryogenesis abundant proteins (LEA) and reactive oxygen species scavengers. This up-regulation is observed in DT resurrection plants, mosses, and green algae most closely related to these Embryophytes. Here we test whether this same suite of protective genes is up-regulated during desiccation in even more distantly related DT green algae, and, importantly, whether that up-regulation is unique to DT algae or also occurs in a desiccation-intolerant relative. We used three closely related aquatic and desert-derived green microalgae in the family Scenedesmaceae and capitalized on extraordinary desiccation tolerance in two of the species, contrasting with desiccation intolerance in the third. We found that during desiccation, all three species increased expression of common protective genes. The feature distinguishing gene expression in DT algae, however, was extensive down-regulation of gene expression associated with diverse metabolic processes during the desiccation time course, suggesting a switch from active growth to energy-saving metabolism. This widespread downshift did not occur in the desiccation-intolerant taxon. These results show that desiccation-induced up-regulation of expression of protective genes may be necessary but is not sufficient to confer desiccation tolerance. The data also suggest that desiccation tolerance may require induced protective mechanisms operating in concert with massive down-regulation of gene expression controlling numerous other aspects of metabolism.
    Description: Dr. Louise Lewis (University of Connecticut) provided F. rotunda and A. deserticola. Suzanne Thomas and Jordan Stark provided expert technical assistance. This work was supported by the NSF, Division of Integrative Organismal Systems (1355085 to Z.G.C.), and an anonymous donor (to Z.G.C.).
    Keywords: Aquatic green algae ; Desert-evolved green algae ; Extremophiles ; Microbiotic ; Crusts ; Scenedesmaceae
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    Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Criswell, K. E., Roberts, L. E., Koo, E. T., Head, J. J., & Gillis, J. A. Hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea. Proceedings of the National Academy of Sciences of the United States of America, 118(51), (2021): e2114563118, https://doi.org/10.1073/pnas.2114563118.
    Description: The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.
    Description: This research was funded by a Natural Environment Research Council Grant (to J.J.H., J.A.G., and K.E.C.: NE/S000739/1) and a Royal Society University Research Fellowship (UF130182 and URF\R\191007), Royal Society Research Grant (RG140377), and University of Cambridge Sir Isaac Newton Trust Grant (14.23z) (to J.A.G.).
    Keywords: Hox genes ; Regionalization ; Chondrichthyan ; Vertebral column
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    Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Chakraborty, A., Ruff, S. E., Dong, X., Ellefson, E. D., Li, C., Brooks, J. M., McBee, J., Bernard, B. B., & Hubert, C. R. J. Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres. Proceedings of the National Academy of Sciences of the United States of America, 117(20), (2020): 11029-11037, doi: 10.1073/pnas.2002289117.
    Description: Marine cold seeps transmit fluids between the subseafloor and seafloor biospheres through upward migration of hydrocarbons that originate in deep sediment layers. It remains unclear how geofluids influence the composition of the seabed microbiome and if they transport deep subsurface life up to the surface. Here we analyzed 172 marine surficial sediments from the deep-water Eastern Gulf of Mexico to assess whether hydrocarbon fluid migration is a mechanism for upward microbial dispersal. While 132 of these sediments contained migrated liquid hydrocarbons, evidence of continuous advective transport of thermogenic alkane gases was observed in 11 sediments. Gas seeps harbored distinct microbial communities featuring bacteria and archaea that are well-known inhabitants of deep biosphere sediments. Specifically, 25 distinct sequence variants within the uncultivated bacterial phyla Atribacteria and Aminicenantes and the archaeal order Thermoprofundales occurred in significantly greater relative sequence abundance along with well-known seep-colonizing members of the bacterial genus Sulfurovum, in the gas-positive sediments. Metabolic predictions guided by metagenome-assembled genomes suggested these organisms are anaerobic heterotrophs capable of nonrespiratory breakdown of organic matter, likely enabling them to inhabit energy-limited deep subseafloor ecosystems. These results point to petroleum geofluids as a vector for the advection-assisted upward dispersal of deep biosphere microbes from subsurface to surface environments, shaping the microbiome of cold seep sediments and providing a general mechanism for the maintenance of microbial diversity in the deep sea.
    Description: We wish to thank Jody Sandel as well as the crew of R/V GeoExplorer for collection of piston cores, onboard core processing, sample preservation, and shipment. Cynthia Kwan and Oliver Horanszky are thanked for assistance with amplicon library preparation. We also wish to thank Jayne Rattray, Daniel Gittins, and Marc Strous for valuable discussions and suggestions, and Rhonda Clark for research support. Collaborations with Andy Mort from the Geological Survey of Canada, and Richard Hatton from Geoscience Wales are also gratefully acknowledged. This work was financially supported by a Mitacs Elevate Postdoctoral Fellowship awarded to A.C.; an Alberta Innovates-Technology Futures/Eyes High Postdoctoral Fellowship to S.E.R.; and a Natural Sciences and Engineering Research Council Strategic Project Grant, a Genome Canada Genomics Applications Partnership Program grant, a Canada Foundation for Innovation grant (CFI-JELF 33752) for instrumentation, and Campus Alberta Innovates Program Chair funding to C.R.J.H.
    Keywords: Deep biosphere ; Microbiome ; Dispersal
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    A demographic and evolutionary analysis of maternal effect senescence (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-27
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in MBL Hernandez, C. M., van Daalen, S. F., Caswell, H., Neubert, M. G., & Gribble, K. E. A demographic and evolutionary analysis of maternal effect senescence. Proceedings of the National Academy of Sciences of the United States of America, 17(28), (2020):16431-16437, doi: 10.1073/pnas.1919988117.
    Description: Maternal effect senescence—a decline in offspring survival or fertility with maternal age—has been demonstrated in many taxa, including humans. Despite decades of phenotypic studies, questions remain about how maternal effect senescence impacts evolutionary fitness. To understand the influence of maternal effect senescence on population dynamics, fitness, and selection, we developed matrix population models in which individuals are jointly classified by age and maternal age. We fit these models to data from individual-based culture experiments on the aquatic invertebrate, Brachionus manjavacas (Rotifera). By comparing models with and without maternal effects, we found that maternal effect senescence significantly reduces fitness for B. manjavacas and that this decrease arises primarily through reduced fertility, particularly at maternal ages corresponding to peak reproductive output. We also used the models to estimate selection gradients, which measure the strength of selection, in both high growth rate (laboratory) and two simulated low growth rate environments. In all environments, selection gradients on survival and fertility decrease with increasing age. They also decrease with increasing maternal age for late maternal ages, implying that maternal effect senescence can evolve through the same process as in Hamilton’s theory of the evolution of age-related senescence. The models we developed are widely applicable to evaluate the fitness consequences of maternal effect senescence across species with diverse aging and fertility schedule phenotypes.
    Description: K.E.G. was supported by Grant 5K01AG049049 from the National Institute on Aging and by the Bay and Paul Foundations. H.C. and S.F.v.D. were supported by the European Research Council through Advanced Grants 322829 and 788195 and by the Dutch Research Council through Grant ALWOP.2015.100. C.M.H. was supported by a National Science Foundation Graduate Research Fellowship. M.G.N. received funding from The Paul MacDonald Fye Chair for Excellence in Oceanography at the Woods Hole Oceanographic Institution.
    Keywords: Aging ; Demography ; Fitness ; Maternal effects ; Selection gradients
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    Neuromechanical wave resonance in jellyfish swimming (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-27
    Description: Author Posting. © National Academy of Sciences, 2021. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 118(11), (2021): e2020025118, https://doi.org/10.1073/pnas.2020025118.
    Description: For organisms to have robust locomotion, their neuromuscular organization must adapt to constantly changing environments. In jellyfish, swimming robustness emerges when marginal pacemakers fire action potentials throughout the bell’s motor nerve net, which signals the musculature to contract. The speed of the muscle activation wave is dictated by the passage times of the action potentials. However, passive elastic material properties also influence the emergent kinematics, with time scales independent of neuromuscular organization. In this multimodal study, we examine the interplay between these two time scales during turning. A three-dimensional computational fluid–structure interaction model of a jellyfish was developed to determine the resulting emergent kinematics, using bidirectional muscular activation waves to actuate the bell rim. Activation wave speeds near the material wave speed yielded successful turns, with a 76-fold difference in turning rate between the best and worst performers. Hyperextension of the margin occurred only at activation wave speeds near the material wave speed, suggesting resonance. This hyperextension resulted in a 34-fold asymmetry in the circulation of the vortex ring between the inside and outside of the turn. Experimental recording of the activation speed confirmed that jellyfish actuate within this range, and flow visualization using particle image velocimetry validated the corresponding fluid dynamics of the numerical model. This suggests that neuromechanical wave resonance plays an important role in the robustness of an organism’s locomotory system and presents an undiscovered constraint on the evolution of flexible organisms. Understanding these dynamics is essential for developing actuators in soft body robotics and bioengineered pumps.
    Description: This research was funded by the NSF Division of Mathematical Sciences, under Faculty Early Career Development Program Grant 1151478 (to L.A.M.).
    Description: 2021-09-16
    Keywords: Jellyfish ; Propulsion ; Neuromechanics ; Fluid-structure interaction ; Maneuverability
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    Teamwork in the viscous oceanic microscale (2021)
    National Academy of Sciences
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    Publication Date: 2022-10-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Kanso, E. A., Lopes, R. M., Strickler, J. R., Dabiri, J. O., & Costello, J. H. Teamwork in the viscous oceanic microscale. Proceedings of the National Academy of Sciences of the United States of America, 118(29), (2021): e2018193118, https://doi.org/10.1073/pnas.2018193118.
    Description: Nutrient acquisition is crucial for oceanic microbes, and competitive solutions to solve this challenge have evolved among a range of unicellular protists. However, solitary solutions are not the only approach found in natural populations. A diverse array of oceanic protists form temporary or even long-lasting attachments to other protists and marine aggregates. Do these planktonic consortia provide benefits to their members? Here, we use empirical and modeling approaches to evaluate whether the relationship between a large centric diatom, Coscinodiscus wailesii, and a ciliate epibiont, Pseudovorticella coscinodisci, provides nutrient flux benefits to the host diatom. We find that fluid flows generated by ciliary beating can increase nutrient flux to a diatom cell surface four to 10 times that of a still cell without ciliate epibionts. This cosmopolitan species of diatom does not form consortia in all environments but frequently joins such consortia in nutrient-depleted waters. Our results demonstrate that symbiotic consortia provide a cooperative alternative of comparable or greater magnitude to sinking for enhancement of nutrient acquisition in challenging environments.
    Description: We are grateful to Y. Garcia for help with organism sampling and sorting. E.A.K. is funded by NSF-2100209, NSF RAISE IOS-2034043 and NIH R01 HL 153622-01A1. R.M.L. is a CNPq research fellow (grant # 310642/2017-5). J.H.C. and J.O.D. are funded by Grant NSF-2100705.
    Keywords: Phytoplankton ; Nutrient limitation ; Symbiosis ; Diffusion limitation ; Cell size
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    Dynamics and functional diversity of the smallest phytoplankton on the Northeast US shelf (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(22), (2020): 12215-12221, doi: 10.1073/pnas.1918439117.
    Description: Picophytoplankton are the most abundant primary producers in the ocean. Knowledge of their community dynamics is key to understanding their role in marine food webs and global biogeochemical cycles. To this end, we analyzed a 16-y time series of observations of a phytoplankton community at a nearshore site on the Northeast US Shelf. We used a size-structured population model to estimate in situ division rates for the picoeukaryote assemblage and compared the dynamics with those of the picocyanobacteria Synechococcus at the same location. We found that the picoeukaryotes divide at roughly twice the rate of the more abundant Synechococcus and are subject to greater loss rates (likely from viral lysis and zooplankton grazing). We describe the dynamics of these groups across short and long timescales and conclude that, despite their taxonomic differences, their populations respond similarly to changes in the biotic and abiotic environment. Both groups appear to be temperature limited in the spring and light limited in the fall and to experience greater mortality during the day than at night. Compared with Synechococcus, the picoeukaryotes are subject to greater top-down control and contribute more to the region’s primary productivity than their standing stocks suggest.
    Description: We thank E. T. Crockford, E. E. Peacock, J. Fredericks, Z. Sandwith, the MVCO Operations Team, and divers of the Woods Hole Oceanographic Institution diving program. This work was supported by NSF Grants OCE-0119915 (to R.J.O. and H.M.S.) and OCE-1655686 (to M.G.N., R.J.O., A.R.S., and H.M.O.); NASA Grants NNX11AF07G (to H.M.S.) and NNX13AC98G (to H.M.S.); Gordon and Betty Moore Foundation Grant GGA#934 (to H.M.S.); and Simons Foundation Grant 561126 (to H.M.S.).
    Description: 2020-11-15
    Keywords: Picoeukaryotes ; Flow cytometry ; Matrix model ; Primary productivity
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    NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica (2019)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Diaz, J. M., Plummer, S., Hansel, C. M., Andeer, P. F., Saito, M. A., & McIlvin, M. R. NADPH-dependent extracellular superoxide production is vital to photophysiology in the marine diatom Thalassiosira oceanica. Proceedings of the National Academy of Sciences of the United States of America, 116 (33), (2019): 16448-16453, doi: 10.1073/pnas.1821233116.
    Description: Reactive oxygen species (ROS) like superoxide drive rapid transformations of carbon and metals in aquatic systems and play dynamic roles in biological health, signaling, and defense across a diversity of cell types. In phytoplankton, however, the ecophysiological role(s) of extracellular superoxide production has remained elusive. Here, the mechanism and function of extracellular superoxide production by the marine diatom Thalassiosira oceanica are described. Extracellular superoxide production in T. oceanica exudates was coupled to the oxidation of NADPH. A putative NADPH-oxidizing flavoenzyme with predicted transmembrane domains and high sequence similarity to glutathione reductase (GR) was implicated in this process. GR was also linked to extracellular superoxide production by whole cells via quenching by the flavoenzyme inhibitor diphenylene iodonium (DPI) and oxidized glutathione, the preferred electron acceptor of GR. Extracellular superoxide production followed a typical photosynthesis-irradiance curve and increased by 30% above the saturation irradiance of photosynthesis, while DPI significantly impaired the efficiency of photosystem II under a wide range of light levels. Together, these results suggest that extracellular superoxide production is a byproduct of a transplasma membrane electron transport system that serves to balance the cellular redox state through the recycling of photosynthetic NADPH. This photoprotective function may be widespread, consistent with the presence of putative homologs to T. oceanica GR in other representative marine phytoplankton and ocean metagenomes. Given predicted climate-driven shifts in global surface ocean light regimes and phytoplankton community-level photoacclimation, these results provide implications for future ocean redox balance, ecological functioning, and coupled biogeochemical transformations of carbon and metals.
    Description: This work was supported by a postdoctoral fellowship from the Ford Foundation (to J.M.D.), the National Science Foundation (NSF) under grants OCE 1225801 (to J.M.D.) and OCE 1246174 (to C.M.H.), a Junior Faculty Seed Grant from the University of Georgia Research Foundation (to J.M.D.), and a National Science Foundation Graduate Research Fellowship (to S.P.). The FIRe was purchased through a NSF equipment improvement grant (1624593).The authors thank Melissa Soule for assistance with LC/MS/MS analysis of peptide samples.
    Keywords: Reactive oxygen species ; Photosynthesis ; Oxidative stress ; Biogeochemistry
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    Abiotic redox reactions in hydrothermal mixing zones: decreased energy availability for the subsurface biosphere (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 202. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in McDermott, J. M., Sylva, S. P., Ono, S., German, C. R., & Seewald, J. S. Abiotic redox reactions in hydrothermal mixing zones: decreased energy availability for the subsurface biosphere. Proceedings of the National Academy of Sciences of the United States of America, 117(34), (2020): 20453-20461, doi:10.1073/pnas.2003108117.
    Description: Subseafloor mixing of high-temperature hot-spring fluids with cold seawater creates intermediate-temperature diffuse fluids that are replete with potential chemical energy. This energy can be harnessed by a chemosynthetic biosphere that permeates hydrothermal regions on Earth. Shifts in the abundance of redox-reactive species in diffuse fluids are often interpreted to reflect the direct influence of subseafloor microbial activity on fluid geochemical budgets. Here, we examine hydrothermal fluids venting at 44 to 149 °C at the Piccard hydrothermal field that span the canonical 122 °C limit to life, and thus provide a rare opportunity to study the transition between habitable and uninhabitable environments. In contrast with previous studies, we show that hydrocarbons are contributed by biomass pyrolysis, while abiotic sulfate (SO42−) reduction produces large depletions in H2. The latter process consumes energy that could otherwise support key metabolic strategies employed by the subseafloor biosphere. Available Gibbs free energy is reduced by 71 to 86% across the habitable temperature range for both hydrogenotrophic SO42− reduction to hydrogen sulfide (H2S) and carbon dioxide (CO2) reduction to methane (CH4). The abiotic H2 sink we identify has implications for the productivity of subseafloor microbial ecosystems and is an important process to consider within models of H2 production and consumption in young oceanic crust.
    Description: Financial support was provided by the National Aeronautics and Space Administration (NASA) Astrobiology program (Awards NNX09AB75G and 80NSSC19K1427 to C.R.G. and J.S.S.) and the NSF (Award OCE-1061863 to C.R.G. and J.S.S.). Ship and vehicle time for cruise FK008 was provided by the Schmidt Ocean Institute. We thank the ROV Jason II and HROV Nereus groups, and the captain, officers, and crew of R/V Atlantis (AT18-16) and R/V Falkor (FK008) for their dedication to skillful operations at sea. We thank our scientific colleagues from both cruises, as well as Meg Tivey, Frieder Klein, and Scott Wankel for insightful discussions. We are grateful to the editor and two anonymous reviewers for providing helpful comments and suggestions.
    Keywords: Hydrothermal vent ; Subsurface biosphere ; Bioenergetics ; Biogeochemistry
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    Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Reysenbach, A. L., St John, E., Meneghin, J., Flores, G. E., Podar, M., Dombrowski, N., Spang, A., L'Haridon, S., Humphris, S. E., de Ronde, C. E. J., Caratori Tontini, F., Tivey, M., Stucker, V. K., Stewart, L. C., Diehl, A., & Bach, W. Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities. Proceedings of the National Academy of Sciences of the United States of America, 117(51), (2020): 202019021, doi:10.1073/pnas.2019021117.
    Description: Hydrothermally active submarine volcanoes are mineral-rich biological oases contributing significantly to chemical fluxes in the deep sea, yet little is known about the microbial communities inhabiting these systems. Here we investigate the diversity of microbial life in hydrothermal deposits and their metagenomics-inferred physiology in light of the geological history and resulting hydrothermal fluid paths in the subsurface of Brothers submarine volcano north of New Zealand on the southern Kermadec arc. From metagenome-assembled genomes we identified over 90 putative bacterial and archaeal genomic families and nearly 300 previously unknown genera, many potentially endemic to this submarine volcanic environment. While magmatically influenced hydrothermal systems on the volcanic resurgent cones of Brothers volcano harbor communities of thermoacidophiles and diverse members of the superphylum “DPANN,” two distinct communities are associated with the caldera wall, likely shaped by two different types of hydrothermal circulation. The communities whose phylogenetic diversity primarily aligns with that of the cone sites and magmatically influenced hydrothermal systems elsewhere are characterized predominately by anaerobic metabolisms. These populations are probably maintained by fluids with greater magmatic inputs that have interacted with different (deeper) previously altered mineral assemblages. However, proximal (a few meters distant) communities with gene-inferred aerobic, microaerophilic, and anaerobic metabolisms are likely supported by shallower seawater-dominated circulation. Furthermore, mixing of fluids from these two distinct hydrothermal circulation systems may have an underlying imprint on the high microbial phylogenomic diversity. Collectively our results highlight the importance of considering geologic evolution and history of subsurface processes in studying microbial colonization and community dynamics in volcanic environments.
    Description: We thank the captain and crew of the R/V Thompson and the engineers from Woods Hole Oceanographic Institution for the successful operation of ROV Jason. The project was funded by NSF grants OCE‐1558356 (Principal Investigator S.E.H.) and OCE-1558795 (Principal Investigator A.-L.R.). S.L. received a grant from the University of Brest to work in the A.-L.R. laboratory. A travel fund from Interridge enabled A.D. to participate on the R/V Thompson cruise. Funding for this work for C.E.J.d.R., F.C.T., V.K.S., and L.C.S. was provided by the New Zealand government. A.S. was supported by the Swedish Research Council (Vetenskapsrådet starting grant 2016-03559 to A.S.) and the Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Dutch Research Council) Foundation of the Netherlands Organization for Scientific Research (Women In Science Excel [WISE] fellowship to A.S.). A.-L.R. and E.S.J. thank Rika Anderson for helpful methodological discussions and Sean Sylva for assistance in shipboard geochemical analysis.
    Keywords: Metagenomics ; Deep-sea hydrothermal ; Thermophiles ; Archaea ; Volcanics
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    Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Coesel, S. N., Durham, B. P., Groussman, R. D., Hu, S. K., Caron, D. A., Morales, R. L., Ribalet, F., & Armbrust, E. V. Diel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities. Proceedings of the National Academy of Sciences of the United States of America, 118(6), (2021): e2011038118, https://doi.org/10.1073./pnas.2011038118.
    Description: The 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.
    Description: This work was supported by a grant from the Simons Foundation (SCOPE Award 329108 [to E.V.A.]) and XSEDE Grant Allocation OCE160019 (to R.D.G.).
    Keywords: Photoreceptors ; Microbial eukaryotes ; Oligotrophic gyre ; Diel cycles ; Metatranscriptomics
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    Rapid mixing and exchange of deep-ocean waters in an abyssal boundary current. (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116(27), (2019): 13233-13238, doi: 10.1073/pnas.1904087116.
    Description: The overturning circulation of the global ocean is critically shaped by deep-ocean mixing, which transforms cold waters sinking at high latitudes into warmer, shallower waters. The effectiveness of mixing in driving this transformation is jointly set by two factors: the intensity of turbulence near topography and the rate at which well-mixed boundary waters are exchanged with the stratified ocean interior. Here, we use innovative observations of a major branch of the overturning circulation—an abyssal boundary current in the Southern Ocean—to identify a previously undocumented mixing mechanism, by which deep-ocean waters are efficiently laundered through intensified near-boundary turbulence and boundary–interior exchange. The linchpin of the mechanism is the generation of submesoscale dynamical instabilities by the flow of deep-ocean waters along a steep topographic boundary. As the conditions conducive to this mode of mixing are common to many abyssal boundary currents, our findings highlight an imperative for its representation in models of oceanic overturning.
    Description: The DynOPO project is supported by the UK Natural Environment Research Council (grants NE/K013181/1 and NE/K012843/1) and the US National Science Foundation (grants OCE-1536453 and OCE-1536779). A.C.N.G. acknowledges the support of the Royal Society and the Wolfson Foundation. S.L. acknowledges the support of award NA14OAR4320106 from the National Oceanic and Atmospheric Administration, US Department of Commerce. The statements, findings, conclusions, and recommendations are those of the authors, and do not necessarily reflect the views of the National Oceanic and Atmospheric Administration, or the US Department of Commerce. We are grateful to the scientific party, crew, and technicians on the RRS James Clark Ross for their hard work during data collection.
    Description: 2019-12-18
    Keywords: Ocean mixing ; Overturning circulation ; Submesoscale instabilities ; Turbulence
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    Aseismic transient slip on the Gofar transform fault, East Pacific Rise (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences (2020): 201913625, doi: 10.1073/pnas.1913625117.
    Description: Oceanic transform faults display a unique combination of seismic and aseismic slip behavior, including a large globally averaged seismic deficit, and the local occurrence of repeating magnitude (M) ∼6 earthquakes with abundant foreshocks and seismic swarms, as on the Gofar transform of the East Pacific Rise and the Blanco Ridge in the northeast Pacific Ocean. However, the underlying mechanisms that govern the partitioning between seismic and aseismic slip and their interaction remain unclear. Here we present a numerical modeling study of earthquake sequences and aseismic transient slip on oceanic transform faults. In the model, strong dilatancy strengthening, supported by seismic imaging that indicates enhanced fluid-filled porosity and possible hydrothermal circulation down to the brittle–ductile transition, effectively stabilizes along-strike seismic rupture propagation and results in rupture barriers where aseismic transients arise episodically. The modeled slow slip migrates along the barrier zones at speeds ∼10 to 600 m/h, spatiotemporally correlated with the observed migration of seismic swarms on the Gofar transform. Our model thus suggests the possible prevalence of episodic aseismic transients in M ∼6 rupture barrier zones that host active swarms on oceanic transform faults and provides candidates for future seafloor geodesy experiments to verify the relation between aseismic fault slip, earthquake swarms, and fault zone hydromechanical properties.
    Description: We thank Joan Gomberg, Ruth Harris, Steve Hickman, Shane Detweiler, Mike Diggles, and two anonymous external reviewers for their thoughtful comments that helped to improve the manuscript. This study was supported by Natural Sciences and Engineering Research Council of Canada Discovery Grants RGPIN/418338-2012 and RGPIN-2018-05389; and NSF Grants OCE-10-61203 and OCE-18-33279.
    Description: 2020-10-28
    Keywords: Oceanic transform faults ; Earthquake rupture segmentation ; Aseismic transients ; Seismic swarms
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    Metrics that matter for assessing the ocean biological carbon pump (2020)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Buesseler, K. O., Boyd, P. W., Black, E. E., & Siegel, D. A. Metrics that matter for assessing the ocean biological carbon pump. Proceedings of the National Academy of Sciences of the United States of America, (2020): 201918114, doi: 10.1073/pnas.1918114117.
    Description: The biological carbon pump (BCP) comprises wide-ranging processes that set carbon supply, consumption, and storage in the oceans’ interior. It is becoming increasingly evident that small changes in the efficiency of the BCP can significantly alter ocean carbon sequestration and, thus, atmospheric CO2 and climate, as well as the functioning of midwater ecosystems. Earth system models, including those used by the United Nation’s Intergovernmental Panel on Climate Change, most often assess POC (particulate organic carbon) flux into the ocean interior at a fixed reference depth. The extrapolation of these fluxes to other depths, which defines the BCP efficiencies, is often executed using an idealized and empirically based flux-vs.-depth relationship, often referred to as the “Martin curve.” We use a new compilation of POC fluxes in the upper ocean to reveal very different patterns in BCP efficiencies depending upon whether the fluxes are assessed at a fixed reference depth or relative to the depth of the sunlit euphotic zone (Ez). We find that the fixed-depth approach underestimates BCP efficiencies when the Ez is shallow, and vice versa. This adjustment alters regional assessments of BCP efficiencies as well as global carbon budgets and the interpretation of prior BCP studies. With several international studies recently underway to study the ocean BCP, there are new and unique opportunities to improve our understanding of the mechanistic controls on BCP efficiencies. However, we will only be able to compare results between studies if we use a common set of Ez-based metrics.
    Description: We thank the many scientists whose ideas and contributions over the years are the foundation of this paper. This includes A. Martin, who led the organization of the BIARRITZ group (now JETZON) workshop in July 2019, discussions at which helped to motivate this article. We thank D. Karl for pointing us in the right direction for this paper format at PNAS and two thoughtful reviewers who through their comments helped to improve this manuscript. Support for writing this piece is acknowledged from several sources, including the Woods Hole Oceanographic Institution’s Ocean Twilight Zone project (K.O.B.); NASA as part of the EXport Processes in the global Ocean from RemoTe Sensing (EXPORTS) program (K.O.B. and D.A.S.). E.E.B. was supported by a postdoctoral fellowship through the Ocean Frontier Institute at Dalhousie University. P.W.B. was supported by the Australian Research Council through a Laureate (FL160100131).
    Keywords: Biological carbon pump ; Twilight zone ; Particle flux
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  • 44
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    Evidence for massive and recurrent toxic blooms of Alexandrium catenella in the Alaskan Arctic (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Anderson, D. M., Fachon, E., Pickart, R. S., Lin, P., Fischer, A. D., Richlen, M. L., Uva, V., Brosnahan, M. L., McRaven, L., Bahr, F., Lefebvre, K., Grebmeier, J. M., Danielson, S. L., Lyu, Y., & Fukai, Y. Evidence for massive and recurrent toxic blooms of Alexandrium catenella in the Alaskan Arctic. Proceedings of the National Academy of Sciences of the United States of America, 118(41) (2021): e2107387118, https://doi.org/10.1073/pnas.2107387118.
    Description: Among the organisms that spread into and flourish in Arctic waters with rising temperatures and sea ice loss are toxic algae, a group of harmful algal bloom species that produce potent biotoxins. Alexandrium catenella, a cyst-forming dinoflagellate that causes paralytic shellfish poisoning worldwide, has been a significant threat to human health in southeastern Alaska for centuries. It is known to be transported into Arctic regions in waters transiting northward through the Bering Strait, yet there is little recognition of this organism as a human health concern north of the Strait. Here, we describe an exceptionally large A. catenella benthic cyst bed and hydrographic conditions across the Chukchi Sea that support germination and development of recurrent, locally originating and self-seeding blooms. Two prominent cyst accumulation zones result from deposition promoted by weak circulation. Cyst concentrations are among the highest reported globally for this species, and the cyst bed is at least 6× larger in area than any other. These extraordinary accumulations are attributed to repeated inputs from advected southern blooms and to localized cyst formation and deposition. Over the past two decades, warming has likely increased the magnitude of the germination flux twofold and advanced the timing of cell inoculation into the euphotic zone by 20 d. Conditions are also now favorable for bloom development in surface waters. The region is poised to support annually recurrent A. catenella blooms that are massive in scale, posing a significant and worrisome threat to public and ecosystem health in Alaskan Arctic communities where economies are subsistence based.
    Description: Funding for D.M.A., R.S.P., E.F., P.L., A.D.F., V.U., M.L.B., L.M., F.B., and M.L.R. was provided by grants from the NSF Office of Polar Programs (Grants OPP-1823002 and OPP-1733564) and the National Ocanic and Atmospheric Administration (NOAA) Arctic Research program (through the Cooperative Institute for the North Atlantic Region [CINAR; Grants NA14OAR4320158 and NA19OAR4320074]), for J.M.G. through CINAR 22309.07 UMCES (University of Maryland Center for Environmental Science), and for D.M.A. and K.L. through NOAA’s Center for Coastal and Ocean Studies Ecology and Oceanography of Harmful Algal Blooms (ECOHAB) Program (NA20NOS4780195). Funding for D.M.A., M.L.R., M.L.B., E.F., V.U., and A.D.F. was also provided by NSF (Grant OCE-1840381) and NIH (Grant 1P01-ES028938-01) through the Woods Hole Center for Oceans and Human Health. S.L.D. was supported by North Pacific Research Board IERP Grants A91-99a and A91-00a. This is IERP publication ArcticIERP-41 and ECOHAB Contribution No. ECO983.
    Keywords: Harmful algal bloom ; HAB ; Alexandrium ; Alaskan Arctic ; Climate
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    Trivalent chromium isotopes in the eastern tropical North Pacific oxygen-deficient zone (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2021. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 118(8), (2021): e1918605118, https://doi.org/10.1073/pnas.1918605118.
    Description: Changes in chromium (Cr) isotope ratios due to fractionation between trivalent [Cr(III)] and hexavalent [Cr(VI)] are being utilized by geologists to infer oxygen conditions in past environments. However, there is little information available on Cr in the modern ocean to ground-truth these inferences. Transformations between the two chromium species are important processes in oceanic Cr cycling. Here we present profiles of hexavalent and trivalent Cr concentrations and stable isotope ratios from the eastern tropical North Pacific (ETNP) oxygen-deficient zone (ODZ) which support theoretical and experimental studies that predict that lighter Cr is preferentially reduced in low-oxygen environments and that residual dissolved Cr becomes heavier due to removal of particle-reactive Cr(III) on sinking particles. The Cr(III) maximum dominantly occurs in the upper portion of the ODZ, implying that microbial activity (dependent on the sinking flux of organic matter) may be the dominant mechanism for this transformation, rather than a simple inorganic chemical conversion between the species depending on the redox potential.
    Description: We thank chief scientist Gabrielle Rocap for accommodating us on cruises Roger Revelle 1804-5 and Kilo Moana 19-20 (sponsored by NSF Grant DEB-1542240 to G. Rocap, A. Devol, R. Kiel, and C. Deutch), Jim Moffett for helping with sampling on these cruises, and Mark Altabet and Frank Stewart for collecting the samples from station 2T on cruise New Horizon 1410. This research was supported by NSF Grant OCE-1736996 (to E.A.B.) and by a fellowship from the Massachusetts Institute of Technology/Woods Hole Oceanographic Institution Joint Program in Oceanography.
    Keywords: Chromium isotopes ; Oxygen-deficient zones ; Trace elements ; Trivalent chromium ; Hexavalent ; Chromium
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  • 46
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    Abiotic methane synthesis and serpentinization in olivine-hosted fluid inclusions (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17666-17672. doi:10.1073/pnas.1907871116.
    Description: The conditions of methane (CH4) formation in olivine-hosted secondary fluid inclusions and their prevalence in peridotite and gabbroic rocks from a wide range of geological settings were assessed using confocal Raman spectroscopy, optical and scanning electron microscopy, electron microprobe analysis, and thermodynamic modeling. Detailed examination of 160 samples from ultraslow- to fast-spreading midocean ridges, subduction zones, and ophiolites revealed that hydrogen (H2) and CH4 formation linked to serpentinization within olivine-hosted secondary fluid inclusions is a widespread process. Fluid inclusion contents are dominated by serpentine, brucite, and magnetite, as well as CH4(g) and H2(g) in varying proportions, consistent with serpentinization under strongly reducing, closed-system conditions. Thermodynamic constraints indicate that aqueous fluids entering the upper mantle or lower oceanic crust are trapped in olivine as secondary fluid inclusions at temperatures higher than ∼400 °C. When temperatures decrease below ∼340 °C, serpentinization of olivine lining the walls of the fluid inclusions leads to a near-quantitative consumption of trapped liquid H2O. The generation of molecular H2 through precipitation of Fe(III)-rich daughter minerals results in conditions that are conducive to the reduction of inorganic carbon and the formation of CH4. Once formed, CH4(g) and H2(g) can be stored over geological timescales until extracted by dissolution or fracturing of the olivine host. Fluid inclusions represent a widespread and significant source of abiotic CH4 and H2 in submarine and subaerial vent systems on Earth, and possibly elsewhere in the solar system.
    Description: We are indebted to J. Eckert for his support with FE-EMPA; to K. Aquinho and E. Codillo for providing samples from Zambales; to K. Aquinho for Raman analysis of some of the samples from Zambales and Mt. Dent; to H. Dick for providing access to his thin section collection; to the curators of the IODP core repositories for providing access to Ocean Drilling Program (ODP) and Integrated Ocean Drilling Program (IODP) samples; and to the captains and crews of the many cruises without whom the collection of these samples would not have been possible. Reviews by Peter Kelemen and an anonymous referee greatly improved this manuscript. This study is supported with funds provided by the National Science Foundation (NSF-OCE Award 1634032 to F.K. and J.S.S.).
    Description: 2020-02-19
    Keywords: Abiotic methane ; Fluid inclusions ; Serpentinization ; Methane seeps ; Carbon cycling
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  • 47
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    Complete arsenic-based respiratory cycle in the marine microbial communities of pelagic oxygen-deficient zones. (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © The Author(s), 2019. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 116(20), (2019):9925-9930, doi:10.1073/pnas.1818349116.
    Description: Microbial capacity to metabolize arsenic is ancient, arising in response to its pervasive presence in the environment, which was largely in the form of As(III) in the early anoxic ocean. Many biological arsenic transformations are aimed at mitigating toxicity; however, some microorganisms can respire compounds of this redox-sensitive element to reap energetic gains. In several modern anoxic marine systems concentrations of As(V) are higher relative to As(III) than what would be expected from the thermodynamic equilibrium, but the mechanism for this discrepancy has remained unknown. Here we present evidence of a complete respiratory arsenic cycle, consisting of dissimilatory As(V) reduction and chemoautotrophic As(III) oxidation, in the pelagic ocean. We identified the presence of genes encoding both subunits of the respiratory arsenite oxidase AioA and the dissimilatory arsenate reductase ArrA in the Eastern Tropical North Pacific (ETNP) oxygen-deficient zone (ODZ). The presence of the dissimilatory arsenate reductase gene arrA was enriched on large particles (〉30 um), similar to the forward bacterial dsrA gene of sulfate-reducing bacteria, which is involved in the cryptic cycling of sulfur in ODZs. Arsenic respiratory genes were expressed in metatranscriptomic libraries from the ETNP and the Eastern Tropical South Pacific (ETSP) ODZ, indicating arsenotrophy is a metabolic pathway actively utilized in anoxic marine water columns. Together these results suggest arsenic-based metabolisms support organic matter production and impact nitrogen biogeochemical cycling in modern oceans. In early anoxic oceans, especially during periods of high marine arsenic concentrations, they may have played a much larger role.
    Description: We thank John Baross and Rika Anderson for helpful discussions and feedback on this project. We also thank the chief scientists of the research cruise, Al Devol and Bess Ward, as well as the captain and crew of the R/V Thomas G. Thompson. This work was supported through a NASA Earth and Space Sciences Graduate Research Fellowship to J.K.S. and National Science Foundation Grant OCE-1138368 (to G.R.).
    Description: 2019-10-29
    Keywords: Oxygen deficient zones ; Arsenic ; Chemoautotrophy ; Dissimilatory arsenate reduction ; Marine metagenome
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  • 48
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    Decadal trends in the ocean carbon sink (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (24), (2019):11646-11651, doi:10.1073/pnas.1900371116.
    Description: Measurements show large decadal variability in the rate of CO2 accumulation in the atmosphere that is not driven by CO2 emissions. The decade of the 1990s experienced enhanced carbon accumulation in the atmosphere relative to emissions, while in the 2000s, the atmospheric growth rate slowed, even though emissions grew rapidly. These variations are driven by natural sources and sinks of CO2 due to the ocean and the terrestrial biosphere. In this study, we compare three independent methods for estimating oceanic CO2 uptake and find that the ocean carbon sink could be responsible for up to 40% of the observed decadal variability in atmospheric CO2 accumulation. Data-based estimates of the ocean carbon sink from pCO2 mapping methods and decadal ocean inverse models generally agree on the magnitude and sign of decadal variability in the ocean CO2 sink at both global and regional scales. Simulations with ocean biogeochemical models confirm that climate variability drove the observed decadal trends in ocean CO2 uptake, but also demonstrate that the sensitivity of ocean CO2 uptake to climate variability may be too weak in models. Furthermore, all estimates point toward coherent decadal variability in the oceanic and terrestrial CO2 sinks, and this variability is not well-matched by current global vegetation models. Reconciling these differences will help to constrain the sensitivity of oceanic and terrestrial CO2 uptake to climate variability and lead to improved climate projections and decadal climate predictions.
    Description: We thank Rebecca Wright and Erik Buitenhuis at University of East Anglia, Norwich, for providing updated runs from the NEMO-PlankTOM5 model. T.D. was supported by NSF Grant OCE-1658392. C.L.Q. thanks the UK Natural Environment Research Council for supporting the SONATA Project (Grant NE/P021417/1). P.L. was supported by the Max Planck Society for the Advancement of Science. J.H. was supported under Helmholtz Young Investigator Group Marine Carbon and Ecosystem Feedbacks in the Earth System (MarESys) Grant VH-NG-1301. S.B. and R.S. were supported by the H2020 project CRESCENDO “Coordinated Research in Earth Systems and Climate: Experiments, Knowledge, Dissemination and Outreach,” which received funding from the European Union’s Horizon 2020 research and innovation program under Grant No 641816. SOCAT is an international effort, endorsed by the International Ocean Carbon Coordination Project, the Surface Ocean-Lower Atmosphere Study, and the Integrated Marine Biosphere Research program, to deliver a uniformly quality-controlled surface ocean CO2 database. The many researchers and funding agencies responsible for the collection of data and quality control are thanked for their contributions to SOCAT.
    Description: 2019-11-28
    Keywords: Carbon dioxide ; Ocean carbon sink ; Terrestrial carbon sink ; Climate variability ; Carbon budget
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  • 49
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    Origin of interannual variability in global mean sea level (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(25), (2020): 13983-13990, doi: 10.1073/pnas.1922190117.
    Description: The two dominant drivers of the global mean sea level (GMSL) variability at interannual timescales are steric changes due to changes in ocean heat content and barystatic changes due to the exchange of water mass between land and ocean. With Gravity Recovery and Climate Experiment (GRACE) satellites and Argo profiling floats, it has been possible to measure the relative steric and barystatic contributions to GMSL since 2004. While efforts to “close the GMSL budget” with satellite altimetry and other observing systems have been largely successful with regards to trends, the short time period covered by these records prohibits a full understanding of the drivers of interannual to decadal variability in GMSL. One particular area of focus is the link between variations in the El Niño−Southern Oscillation (ENSO) and GMSL. Recent literature disagrees on the relative importance of steric and barystatic contributions to interannual to decadal variability in GMSL. Here, we use a multivariate data analysis technique to estimate variability in barystatic and steric contributions to GMSL back to 1982. These independent estimates explain most of the observed interannual variability in satellite altimeter-measured GMSL. Both processes, which are highly correlated with ENSO variations, contribute about equally to observed interannual GMSL variability. A theoretical scaling analysis corroborates the observational results. The improved understanding of the origins of interannual variability in GMSL has important implications for our understanding of long-term trends in sea level, the hydrological cycle, and the planet’s radiation imbalance.
    Description: The research was carried out at JPL, California Institute of Technology, under a contract with NASA. This study was funded by NASA Grants NNX17AH35G (Ocean Surface Topography Science Team), 80NSSC17K0564, and 80NSSC17K0565 (NASA Sea Level Change Team). The efforts of J.T.F. in this work were also supported by NSF Award AGS-1419571, and by the Regional and Global Model Analysis component of the Earth and Environmental System Modeling Program of the US Department of Energy's Office of Biological & Environmental Research via National Science Foundation Grant IA 1844590. C.G.P. was supported by the J. Lamar Worzel Assistant Scientist Fund and the Penzance Endowed Fund in Support of Assistant Scientists at the Woods Hole Oceanographic Institution.
    Description: 2020-12-08
    Keywords: Sea level ; Climate variability ; Global mean sea level ; Satellite altimetry
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  • 50
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    Climate control on terrestrial biospheric carbon turnover (2021)
    National Academy of Sciences
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    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Eglinton, T. I., Galy, V. V., Hemingway, J. D., Feng, X., Bao, H., Blattmann, T. M., Dickens, A. F., Gies, H., Giosan, L., Haghipour, N., Hou, P., Lupker, M., McIntyre, C. P., Montluçon, D. B., Peucker-Ehrenbrink, B., Ponton, C., Schefuß, E., Schwab, M. S., Voss, B. M., Wacker, L., Wu, Y., & Zhao, M. Climate control on terrestrial biospheric carbon turnover. Proceedings of the National Academy of Sciences of the United States of America, 118(8), (2021): e2011585118, htps://doi.org/ 10.1073/pnas.2011585118.
    Description: Terrestrial vegetation and soils hold three times more carbon than the atmosphere. Much debate concerns how anthropogenic activity will perturb these surface reservoirs, potentially exacerbating ongoing changes to the climate system. Uncertainties specifically persist in extrapolating point-source observations to ecosystem-scale budgets and fluxes, which require consideration of vertical and lateral processes on multiple temporal and spatial scales. To explore controls on organic carbon (OC) turnover at the river basin scale, we present radiocarbon (14C) ages on two groups of molecular tracers of plant-derived carbon—leaf-wax lipids and lignin phenols—from a globally distributed suite of rivers. We find significant negative relationships between the 14C age of these biomarkers and mean annual temperature and precipitation. Moreover, riverine biospheric-carbon ages scale proportionally with basin-wide soil carbon turnover times and soil 14C ages, implicating OC cycling within soils as a primary control on exported biomarker ages and revealing a broad distribution of soil OC reactivities. The ubiquitous occurrence of a long-lived soil OC pool suggests soil OC is globally vulnerable to perturbations by future temperature and precipitation increase. Scaling of riverine biospheric-carbon ages with soil OC turnover shows the former can constrain the sensitivity of carbon dynamics to environmental controls on broad spatial scales. Extracting this information from fluvially dominated sedimentary sequences may inform past variations in soil OC turnover in response to anthropogenic and/or climate perturbations. In turn, monitoring riverine OC composition may help detect future climate-change–induced perturbations of soil OC turnover and stocks.
    Description: This work was supported by grants from the US NSF (OCE-0928582 to T.I.E. and V.V.G.; OCE-0851015 to B.P.-E., T.I.E., and V.V.G.; and EAR-1226818 to B.P.-E.), Swiss National Science Foundation (200021_140850, 200020_163162, and 200020_184865 to T.I.E.), and National Natural Science Foundation of China (41520104009 to M.Z.).
    Keywords: Radiocarbon ; Plant biomarkers ; Carbon turnover times ; Fluvial carbon ; Carbon cycle
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    Human arrival and landscape dynamics in the northern Bahamas (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fall, P. L., van Hengstum, P. J., Lavold-Foote, L., Donnelly, J. P., Albury, N. A., & Tamalavage, A. E. Human arrival and landscape dynamics in the northern Bahamas. Proceedings of the National Academy of Sciences of the United States of America, 118(10), (2021): e2015764118, https://doi.org/10.1073/pnas.2015764118.
    Description: The first Caribbean settlers were Amerindians from South America. Great Abaco and Grand Bahama, the final islands colonized in the northernmost Bahamas, were inhabited by the Lucayans when Europeans arrived. The timing of Lucayan arrival in the northern Bahamas has been uncertain because direct archaeological evidence is limited. We document Lucayan arrival on Great Abaco Island through a detailed record of vegetation, fire, and landscape dynamics based on proxy data from Blackwood Sinkhole. From about 3,000 to 1,000 y ago, forests dominated by hardwoods and palms were resilient to the effects of hurricanes and cooling sea surface temperatures. The arrival of Lucayans by about 830 CE (2σ range: 720 to 920 CE) is demarcated by increased burning and followed by landscape disturbance and a time-transgressive shift from hardwoods and palms to the modern pine forest. Considering that Lucayan settlements in the southern Bahamian archipelago are dated to about 750 CE (2σ range: 600 to 900 CE), these results demonstrate that Lucayans spread rapidly through the archipelago in less than 100 y. Although precontact landscapes would have been influenced by storms and climatic trends, the most pronounced changes follow more directly from landscape burning and ecosystem shifts after Lucayan arrival. The pine forests of Abaco declined substantially between 1500 and 1670 CE, a period of increased regional hurricane activity, coupled with fires on an already human-impacted landscape. Any future intensification of hurricane activity in the tropical North Atlantic Ocean threatens the sustainability of modern pine forests in the northern Bahamas.
    Description: This research was supported by NSF Awards GSS-1118340 (P.L.F.), OCE-1356509 (P.J.v.H.), OCE-1703087 (P.J.v.H.), and OCE-1356708 (J.P.D.).
    Keywords: Anthropogenic burning ; Lucayan ; Caribbean ; Pollen ; Vegetation change
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    Identification of chondritic krypton and xenon in Yellowstone gases and the timing of terrestrial volatile accretion (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), [year]. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Broadley, M. W., Barry, P. H., Bekaert, D. V., Byrne, D. J., Caracausi, A., Ballentine, C. J., & Marty, B. Identification of chondritic krypton and xenon in Yellowstone gases and the timing of terrestrial volatile accretion. Proceedings of the National Academy of Sciences of the United States of America, 117 (25), (2020): 13997-14004, doi: 10.1073/pnas.2003907117.
    Description: Identifying the origin of noble gases in Earth’s mantle can provide crucial constraints on the source and timing of volatile (C, N, H2O, noble gases, etc.) delivery to Earth. It remains unclear whether the early Earth was able to directly capture and retain volatiles throughout accretion or whether it accreted anhydrously and subsequently acquired volatiles through later additions of chondritic material. Here, we report high-precision noble gas isotopic data from volcanic gases emanating from, in and around, the Yellowstone caldera (Wyoming, United States). We show that the He and Ne isotopic and elemental signatures of the Yellowstone gas requires an input from an undegassed mantle plume. Coupled with the distinct ratio of 129Xe to primordial Xe isotopes in Yellowstone compared with mid-ocean ridge basalt (MORB) samples, this confirms that the deep plume and shallow MORB mantles have remained distinct from one another for the majority of Earth’s history. Krypton and xenon isotopes in the Yellowstone mantle plume are found to be chondritic in origin, similar to the MORB source mantle. This is in contrast with the origin of neon in the mantle, which exhibits an isotopic dichotomy between solar plume and chondritic MORB mantle sources. The co-occurrence of solar and chondritic noble gases in the deep mantle is thought to reflect the heterogeneous nature of Earth’s volatile accretion during the lifetime of the protosolar nebula. It notably implies that the Earth was able to retain its chondritic volatiles since its earliest stages of accretion, and not only through late additions.
    Description: Samples were collected as part of Study YELL-08056: Xenon Anomalies in the Yellowstone Hotspot. We thank Annie Carlson and all of the rangers at the Yellowstone National Park for providing invaluable advice and help when collecting the samples. M.W.B., D.V.B., D.J.B., and B.M. were supported by the European Research Council (PHOTONIS Project Grant 695618). This work was partially supported by Grants G-2016-7206 and G-2017-9696 from the Alfred P. Sloan Foundation and the Deep Carbon Observatory (to P.H.B.) and UK National Environment Research Council Deep Volatile Grant NE/M000427/1 (to C.J.B.). We also thank Laurent Zimmerman for providing help with the analysis. Finally, we thank the editor for efficient handling of our manuscript and the two anonymous reviewers for their insightful comments. This is CRPG contribution 2998.
    Keywords: Origin of Earth’s volatiles ; Accretion ; Mantle plume ; Noble gases ; Yellowstone
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    Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Sutherland, K. M., Wankel, S. D., & Hansel, C. M. Dark biological superoxide production as a significant flux and sink of marine dissolved oxygen. Proceedings of the National Academy of Sciences of the United States of America, 117(7), (2020): 3433-3439, doi:10.1073/pnas.1912313117.
    Description: The balance between sources and sinks of molecular oxygen in the oceans has greatly impacted the composition of Earth’s atmosphere since the evolution of oxygenic photosynthesis, thereby exerting key influence on Earth’s climate and the redox state of (sub)surface Earth. The canonical source and sink terms of the marine oxygen budget include photosynthesis, respiration, photorespiration, the Mehler reaction, and other smaller terms. However, recent advances in understanding cryptic oxygen cycling, namely the ubiquitous one-electron reduction of O2 to superoxide by microorganisms outside the cell, remains unexplored as a potential player in global oxygen dynamics. Here we show that dark extracellular superoxide production by marine microbes represents a previously unconsidered global oxygen flux and sink comparable in magnitude to other key terms. We estimate that extracellular superoxide production represents a gross oxygen sink comprising about a third of marine gross oxygen production, and a net oxygen sink amounting to 15 to 50% of that. We further demonstrate that this total marine dark extracellular superoxide flux is consistent with concentrations of superoxide in marine environments. These findings underscore prolific marine sources of reactive oxygen species and a complex and dynamic oxygen cycle in which oxygen consumption and corresponding carbon oxidation are not necessarily confined to cell membranes or exclusively related to respiration. This revised model of the marine oxygen cycle will ultimately allow for greater reconciliation among estimates of primary production and respiration and a greater mechanistic understanding of redox cycling in the ocean.
    Description: This work was supported by NASA Earth and Space Science Fellowship NNX15AR62H to K.M.S., NASA Exobiology grant NNX15AM04G to S.D.W. and C.M.H., and NSF Division of Ocean Sciences grant 1355720 to C.M.H. This research was further supported in part by Hanse-Wissenschaftskolleg Institute of Advanced Study fellowships to C.M.H. and S.D.W. We thank Danielle Hicks for assistance with figures and Community Earth Systems Model (CESM) Large Ensemble Project for the availability and use of its data product. The CESM project is primarily supported by the NSF.
    Keywords: Microbial superoxide ; Reactive oxygen species ; Marine dissolved oxygen
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    Thermodynamic feasibility of shipboard conversion of marine plastics to blue diesel for self-powered ocean cleanup (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Belden, E. R., Kazantzis, N. K., Reddy, C. M., Kite-Powell, H., Timko, M. T., Italiani, E., & Herschbach, D. R. Thermodynamic feasibility of shipboard conversion of marine plastics to blue diesel for self-powered ocean cleanup. Proceedings of the National Academy of Sciences of the United States of America, 118(46),(2021): e2107250118, https://doi.org/10.1073/pnas.2107250118.
    Description: Collecting and removing ocean plastics can mitigate their environmental impacts; however, ocean cleanup will be a complex and energy-intensive operation that has not been fully evaluated. This work examines the thermodynamic feasibility and subsequent implications of hydrothermally converting this waste into a fuel to enable self-powered cleanup. A comprehensive probabilistic exergy analysis demonstrates that hydrothermal liquefaction has potential to generate sufficient energy to power both the process and the ship performing the cleanup. Self-powered cleanup reduces the number of roundtrips to port of a waste-laden ship, eliminating the need for fossil fuel use for most plastic concentrations. Several cleanup scenarios are modeled for the Great Pacific Garbage Patch (GPGP), corresponding to 230 t to 11,500 t of plastic removed yearly; the range corresponds to uncertainty in the surface concentration of plastics in the GPGP. Estimated cleanup times depends mainly on the number of booms that can be deployed in the GPGP without sacrificing collection efficiency. Self-powered cleanup may be a viable approach for removal of plastics from the ocean, and gaps in our understanding of GPGP characteristics should be addressed to reduce uncertainty.
    Description: The US NSF supported this work as part of its 2026 Idea Machine initiative (Chemical, Bioengineering, Environmental, and Transport Systems, EArly-concept Grants for Exploratory Research Award #2032621). E.R.B.’s contribution was funded, in part, by the NSF Graduate Research Fellowship Program under Grant No. 2038257.
    Keywords: Ocean plastic ; Hydrothermal liquefaction ; Exergy analysis ; Monte Carlo simulation
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    High (3)He/(4)He in central Panama reveals a distal connection to the Galápagos plume (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-26
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bekaert, D. V., Gazel, E., Turner, S., Behn, M. D., de Moor, J. M., Zahirovic, S., Manea, V. C., Hoernle, K., Fischer, T. P., Hammerstrom, A., Seltzer, A. M., Kulongoski, J. T., Patel, B. S., Schrenk, M. O., Halldórsson, S. A., Nakagawa, M., Ramírez, C. J., Krantz, J. A., Yücel, M., Ballentine, C. J., Giovannelli, D., Lloyd, K. G., Barry, P. H. High (3)He/(4)He in central Panama reveals a distal connection to the Galápagos plume. Proceedings of the National Academy of Sciences of the United States of America, 118(47), (2021): e2110997118, https://doi.org/10.1073/pnas.2110997118.
    Description: It is well established that mantle plumes are the main conduits for upwelling geochemically enriched material from Earth's deep interior. The fashion and extent to which lateral flow processes at shallow depths may disperse enriched mantle material far (〉1,000 km) from vertical plume conduits, however, remain poorly constrained. Here, we report He and C isotope data from 65 hydrothermal fluids from the southern Central America Margin (CAM) which reveal strikingly high 3He/4He (up to 8.9RA) in low-temperature (≤50 °C) geothermal springs of central Panama that are not associated with active volcanism. Following radiogenic correction, these data imply a mantle source 3He/4He 〉10.3RA (and potentially up to 26RA, similar to Galápagos hotspot lavas) markedly greater than the upper mantle range (8 ± 1RA). Lava geochemistry (Pb isotopes, Nb/U, and Ce/Pb) and geophysical constraints show that high 3He/4He values in central Panama are likely derived from the infiltration of a Galápagos plume–like mantle through a slab window that opened ∼8 Mya. Two potential transport mechanisms can explain the connection between the Galápagos plume and the slab window: 1) sublithospheric transport of Galápagos plume material channeled by lithosphere thinning along the Panama Fracture Zone or 2) active upwelling of Galápagos plume material blown by a “mantle wind” toward the CAM. We present a model of global mantle flow that supports the second mechanism, whereby most of the eastward transport of Galápagos plume material occurs in the shallow asthenosphere. These findings underscore the potential for lateral mantle flow to transport mantle geochemical heterogeneities thousands of kilometers away from plume conduits.
    Description: This work was principally supported by Grant G-2016-7206 from the Alfred P. Sloan Foundation and the Deep Carbon Observatory to P.H.B. We also acknowledge the NSF awards (1144559, 1923915, and 2015789) to P.H.B., which partially supported this work. S.Z. was supported by the Australian Research Council Grant DE210100084 and a University of Sydney Robinson Fellowship. D.G. was partially supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program Grant Agreement No. 948972—COEVOLVE—ERC-2020-STG. This study was also supported in part by NSF award No. EAR 1826673 to E.G. Folkmar Hauff is acknowledged for contributing to the analysis of the La Providencia samples at GEOMAR.
    Keywords: Helium ; Mantle plume ; Slab window ; Mantle flow ; Geochemistry
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    Nutrient availability and senescence spatially structure the dynamics of a foundation species (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-20
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bell, T. W., & Siegel, D. A. Nutrient availability and senescence spatially structure the dynamics of a foundation species. Proceedings of the National Academy of Sciences of the United States of America, 119(1), (2021): e2105135118, https://doi.org/10.1073/pnas.2105135118.
    Description: Disentangling the roles of the external environment and internal biotic drivers of plant population dynamics is challenging due to the absence of relevant physiological and abundance information over appropriate space and time scales. Remote observations of giant kelp biomass and photosynthetic pigment concentrations are used to show that spatiotemporal patterns of physiological condition, and thus growth and production, are regulated by different processes depending on the scale of observation. Nutrient supply was linked to regional scale (〉1 km) physiological condition dynamics, and kelp forest stands were more persistent where nutrient levels were consistently high. However, on local scales (〈1 km), internal senescence processes related to canopy age demographics determined patterns of biomass loss across individual kelp forests despite uniform nutrient conditions. Repeat measurements of physiology over continuous spatial fields can provide insights into complex dynamics that are unexplained by the environmental drivers thought to regulate abundance. Emerging remote sensing technologies that provide simultaneous estimates of abundance and physiology can quantify the roles of environmental change and demographics governing plant population dynamics for a wide range of aquatic and terrestrial ecosystems.
    Description: This work was supported by the US NSF (Grants OCE 1232779 and 1831937), by the US Department of Energy (Cooperative Agreement DE-AR0000922), and by NASA (Grant NNX14AR62A) and the NASA Earth and Space Sciences Fellowship program in support of T.W.B.
    Keywords: Physiology ; Population ; Biomass ; Hyperspectral ; Giant kelp
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    Holocene bidirectional river system along the Kenya Rift and its influence on East African faunal exchange and diversity gradients (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-10-19
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Dommain, R., Riedl, S., Olaka, L. A., deMenocal, P., Deino, A. L., Owen, R. B., Muiruri, V., Müller, J., Potts, R., & Strecker, M. R. Holocene bidirectional river system along the Kenya Rift and its influence on East African faunal exchange and diversity gradients. Proceedings of the National Academy of Sciences of the United States of America, 119(28),(2022): e2121388119, https://doi.org/10.1073/pnas.2121388119.
    Description: East Africa is a global biodiversity hotspot and exhibits distinct longitudinal diversity gradients from west to east in freshwater fishes and forest mammals. The assembly of this exceptional biodiversity and the drivers behind diversity gradients remain poorly understood, with diversification often studied at local scales and less attention paid to biotic exchange between Afrotropical regions. Here, we reconstruct a river system that existed for several millennia along the now semiarid Kenya Rift Valley during the humid early Holocene and show how this river system influenced postglacial dispersal of fishes and mammals due to its dual role as a dispersal corridor and barrier. Using geomorphological, geochronological, isotopic, and fossil analyses and a synthesis of radiocarbon dates, we find that the overflow of Kenyan rift lakes between 12 and 8 ka before present formed a bidirectional river system consisting of a “Northern River” connected to the Nile Basin and a “Southern River,” a closed basin. The drainage divide between these rivers represented the only viable terrestrial dispersal corridor across the rift. The degree and duration of past hydrological connectivity between adjacent river basins determined spatial diversity gradients for East African fishes. Our reconstruction explains the isolated distribution of Nilotic fish species in modern Kenyan rift lakes, Guineo-Congolian mammal species in forests east of the Kenya Rift, and recent incipient vertebrate speciation and local endemism in this region. Climate-driven rearrangements of drainage networks unrelated to tectonic activity contributed significantly to the assembly of species diversity and modern faunas in the East African biodiversity hotspot.
    Description: R.D. was funded by a Smithsonian Human Origins Postdoctoral Fellowship and by Geo.X—the Research Network for Geosciences in Berlin and Potsdam. Fig. 1 D, E, and G and SI Appendix, Figs. S1 and S3 are based on the TanDEM-X Science DEM granted to L.A.O. and S.R. by the German Aerospace Center (DLR) in 2017. L.A.O. acknowledges the Volkswagen Foundation for funding this study with Grant No. 89369. M.R.S. and S.R. were supported by funds from Potsdam University and the Geothermal Development Company of Kenya, and R.B.O. and V.M. were supported by the Hong Kong General Research Fund. We acknowledge support from the National Museums of Kenya and the Kenya Government permission granted by the Ministry of Sports, Culture and the Arts, and by the National Commission for Science, Technology and Innovation (NACOSTI) Permits P/14/7709/683 (to R.P.) and P/16/11924/11448 (to L.A.O.). This work is a contribution of the Olorgesailie Drilling Project, for which support from the National Museums of Kenya, the Oldonyo Nyokie Group Ranch, the Peter Buck Fund for Human Origins Research (Smithsonian Institution), the William H. Donner Foundation, the Ruth and Vernon Taylor Foundation, Whitney and Betty MacMillan, and the Smithsonian Human Origins Program is gratefully acknowledged. LacCore is acknowledged for support in drilling and core storage.
    Keywords: East Africa ; Biogeography ; Biodiversity ; Hydrological connectivity ; Holocene
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    Century-scale trends and seasonality in pH and temperature for shallow zones of the Bering Sea (2015)
    National Academy of Sciences
    Details
    Publication Date: 2022-09-20
    Description: No records exist to evaluate long-term pH dynamics in high-latitude oceans, which have the greatest probability of rapid acidification from anthropogenic CO2 emissions. We reconstructed both seasonal variability and anthropogenic change in seawater pH and temperature by using laser ablation high-resolution 2D images of stable boron isotopes (δ11B) on a long-lived coralline alga that grew continuously through the 20th century. Analyses focused on four multiannual growth segments. We show a long-term decline of 0.08 ± 0.01 pH units between the end of the 19th and 20th century, which is consistent with atmospheric CO2 records. Additionally, a strong seasonal cycle (∼0.22 pH units) is observed and interpreted as episodic annual pH increases caused by the consumption of CO2 during strong algal (kelp) growth in spring and summer. The rate of acidification intensifies from –0.006 ± 0.007 pH units per decade (between 1920s and 1960s) to –0.019 ± 0.009 pH units per decade (between 1960s and 1990s), and the episodic pH increases show a continuous shift to earlier times of the year throughout the centennial record. This is indicative of ecosystem shifts in shallow water algal productivity in this high-latitude habitat resulting from warming and acidification.
    Type: Article , PeerReviewed
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    Sulfur and lead isotopic evidence of relic Archean sediments in the Pitcairn mantle plume (2016)
    National Academy of Sciences
    Details
    Publication Date: 2022-09-20
    Description: The isotopic diversity of oceanic island basalts (OIB) is usually attributed to the influence, in their sources, of ancient material recycled into the mantle, although the nature, age, and quantities of this material remain controversial. The unradiogenic Pb isotope signature of the enriched mantle I (EM I) source of basalts from, for example, Pitcairn or Walvis Ridge has been variously attributed to recycled pelagic sediments, lower continental crust, or recycled subcontinental lithosphere. Our study helps resolve this debate by showing that Pitcairn lavas contain sulfides whose sulfur isotopic compositions are affected by mass-independent fractionation (S-MIF down to Δ33S = −0.8), something which is thought to have occurred on Earth only before 2.45 Ga, constraining the youngest possible age of the EM I source component. With this independent age constraint and a Monte Carlo refinement modeling of lead isotopes, we place the likely Pitcairn source age at 2.5 Ga to 2.6 Ga. The Pb, Sr, Nd, and Hf isotopic mixing arrays show that the Archean EM I material was poor in trace elements, resembling Archean sediment. After subduction, this Archean sediment apparently remained stored in the deep Earth for billions of years before returning to the surface as Pitcairn´s characteristic EM I signature. The presence of negative S-MIF in the deep mantle may also help resolve the problem of an apparent deficit of negative Δ33S anomalies so far found in surface reservoirs.
    Type: Article , PeerReviewed
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    Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-08-15
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Womersley, F. C., Humphries, N. E., Queiroz, N., Vedor, M., da Costa, I., Furtado, M., Tyminski, J. P., Abrantes, K., Araujo, G., Bach, S. S., Barnett, A., Berumen, M. L., Bessudo Lion, S., Braun, C. D., Clingham, E., Cochran, J. E. M., de la Parra, R., Diamant, S., Dove, A. D. M., Dudgeon, C. L., Erdmann, M. V., Espinoza, E., Fitzpatrick, R., González Cano, J., Green, J. R., Guzman, H. M., Hardenstine, R., Hasan, A., Hazin, F. H. V., Hearn, A. R., Hueter, R. E., Jaidah, M. Y., Labaja, J., Ladinol, F., Macena, B. C. L., Morris Jr., J. J., Norman, B. M., Peñaherrera-Palmav, C., Pierce, S. J., Quintero, L. M., Ramırez-Macías, D., Reynolds, S. D., Richardson, A. J., Robinson, D. P., Rohner, C. A., Rowat, D. R. L., Sheaves, M., Shivji, M. S., Sianipar, A. B., Skomal, G. B., Soler, G., Syakurachman, I., Thorrold, S. R., Webb, D. H., Wetherbee, B. M., White, T. D., Clavelle, T., Kroodsma, D. A., Thums, M., Ferreira, L. C., Meekan, M. G., Arrowsmith, L. M., Lester, E. K., Meyers, M. M., Peel, L. R., Sequeira, A. M. M., Eguıluz, V. M., Duarte, C. M., & Sims, D. W. Global collision-risk hotspots of marine traffic and the world’s largest fish, the whale shark. Proceedings of the National Academy of Sciences of the United States of America, 119(20), (2022): e2117440119, https://doi.org/10.1073/pnas.2117440119.
    Description: Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks’ horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (〉300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial “cryptic” lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.
    Description: Funding for data analysis was provided by the UK Natural Environment Research Council (NERC) through a University of Southampton INSPIRE DTP PhD Studentship to F.C.W. Additional funding for data analysis was provided by NERC Discovery Science (NE/R00997/X/1) and the European Research Council (ERC-AdG-2019 883583 OCEAN DEOXYFISH) to D.W.S., Fundação para a Ciência e a Tecnologia (FCT) under PTDC/BIA/28855/2017 and COMPETE POCI-01–0145-FEDER-028855, and MARINFO–NORTE-01–0145-FEDER-000031 (funded by Norte Portugal Regional Operational Program [NORTE2020] under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund–ERDF) to N.Q. FCT also supported N.Q. (CEECIND/02857/2018) and M.V. (PTDC/BIA-COM/28855/2017). D.W.S. was supported by a Marine Biological Association Senior Research Fellowship. All tagging procedures were approved by institutional ethical review bodies and complied with all relevant ethical regulations in the jurisdictions in which they were performed. Details for individual research teams are given in SI Appendix, section 8. Full acknowledgments for tagging and field research are given in SI Appendix, section 7. This research is part of the Global Shark Movement Project (https://www.globalsharkmovement.org).
    Keywords: ship strike ; marine megafauna ; conservation ; movement ecology ; human impact
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    Phosphonate production by marine microbes: exploring new sources and potential function (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-06-10
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Acker, M., Hogle, S. L., Berube, P. M., Hackl, T., Coe, A., Stepanauskas, R., Chisholm, S. W., & Repeta, D. J. Phosphonate production by marine microbes: exploring new sources and potential function. Proceedings of the National Academy of Sciences of the United States of America, 119(11), (2022): e2113386119, https://doi.org/10.1073/pnas.2113386119.
    Description: Phosphonates are organophosphorus metabolites with a characteristic C-P bond. They are ubiquitous in the marine environment, their degradation broadly supports ecosystem productivity, and they are key components of the marine phosphorus (P) cycle. However, the microbial producers that sustain the large oceanic inventory of phosphonates as well as the physiological and ecological roles of phosphonates are enigmatic. Here, we show that phosphonate synthesis genes are rare but widely distributed among diverse bacteria and archaea, including Prochlorococcus and SAR11, the two major groups of bacteria in the ocean. In addition, we show that Prochlorococcus can allocate over 40% of its total cellular P-quota toward phosphonate production. However, we find no evidence that Prochlorococcus uses phosphonates for surplus P storage, and nearly all producer genomes lack the genes necessary to degrade and assimilate phosphonates. Instead, we postulate that phosphonates are associated with cell-surface glycoproteins, suggesting that phosphonates mediate ecological interactions between the cell and its surrounding environment. Our findings indicate that the oligotrophic surface ocean phosphonate pool is sustained by a relatively small fraction of the bacterioplankton cells allocating a significant portion of their P quotas toward secondary metabolism and away from growth and reproduction.
    Description: This work was supported in part by grants from the NSF (OCE-1153588 and DBI-0424599 to S.W.C.; OCE-1335810 and OIA-1826734 to R.S.; and OCE-1634080 to D.J.R.), the Gordon and Betty Moore Foundation (no. 6000 to D.J.R.), and the Simons Foundation (Life Sciences Project Award IDs 337262 and 647135 to S.W.C.; 510023 to R.S.; and Simons Collaboration on Ocean Processes and Ecology [SCOPE] Award ID 329108 to S.W.C. and D.J.R.).
    Keywords: phosphonate ; Prochlorococcus ; marine ; biogeochemistry ; phosphorus
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    Unifying chemical and biological perspectives of carbon accumulation in the environment (2021)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Repeta, D. J. Unifying chemical and biological perspectives of carbon accumulation in the environment. Proceedings of the National Academy of Sciences of the United States of America, 118(11), (2021); e2100935118, https://doi.org/10.1073/pnas.2100935118.
    Description: Heterotrophic microorganisms are fiendishly clever at degrading all shapes and sizes of organic compounds to extract the energy they need to build biomass. Every year marine phytoplankton fix ∼50 billion tons of carbon dioxide into organic matter, and every year marine heterotrophs respire nearly all of this organic matter back to carbon dioxide (1). Nearly all, but not all. With each spin of this carbon cycle, a small amount of organic matter escapes respiration and becomes sequestered in seawater, sediments, and soils. Over time, this small “leak” in the system leads to the accumulation of a vast reservoir of carbon; some 5 × 1019 kg of organic matter are thought to be sequestered in sedimentary rocks (2). This carbon sequestration has immense consequences for life on Earth, as illustrated by the change in climate we are now experiencing due in part to the transfer of a minute portion of this inventory from geologic reservoirs into the atmosphere.
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    The Earth BioGenome Project 2020: starting the clock (2022)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lewin, H. A., Richards, S., Lieberman Aiden, E., Allende, M. L., Archibald, J. M., Bálint, M., Barker, K. B., Baumgartner, B., Belov, K., Bertorelle, G., Blaxter, Mark L., Cai, J., Caperello, N. D., Carlson, K., Castilla-Rubio, J. C., Chaw, S-M., Chen, L., Childers, A. K., Coddington, J. A., Conde, D. A., Corominas, M., Crandall, K. A., Crawford, A. J., DiPalma, F., Durbin, R., Ebenezer, T. E., Edwards, S. V., Fedrigo, O., Flicek, P., Formenti, G., Gibbs, R. A., Gilbert, M. Thomas P., Goldstein, M. M., Graves, J. M., Greely, H. T., Grigoriev, I. V., Hackett, K. J., Hall, N., Haussler, D., Helgen, K. M., Hogg, C. J., Isobe, S., Jakobsen, K. S., Janke, A., Jarvis, E. D., Johnson, W. E., Jones, S. J. M., Karlsson, E. K., Kersey, P. J., Kim, J-H., Kress, W. J., Kuraku, S., Lawniczak, M. K. N., Leebens-Mack, J. H., Li, X., Lindblad-Toh, K., Liu, X., Lopez, J. V., Marques-Bonet, T., Mazard, S., Mazet, J. A. K., Mazzoni, C. J., Myers, E. W., O’Neill, R. J., Paez, S., Park, H., Robinson, G. E., Roquet, C., Ryder, O. A., Sabir, J. S. M., Shaffer, H. B., Shank, T. M., Sherkow, J. S., Soltis, P. S., Tang, B., Tedersoo, L., Uliano-Silva, M., Wang, K., Wei, X., Wetzer, R., Wilson, J. L., Xu, X., Yang, H., Yoder, A. D., Zhang, G. The Earth BioGenome Project 2020: starting the clock. Proceedings of the National Academy of Sciences of the United States of America, 119(4), (2022): e2115635118, https://doi.org/10.1073/pnas.2115635118.
    Description: November 2020 marked 2 y since the launch of the Earth BioGenome Project (EBP), which aims to sequence all known eukaryotic species in a 10-y timeframe. Since then, significant progress has been made across all aspects of the EBP roadmap, as outlined in the 2018 article describing the project’s goals, strategies, and challenges (1). The launch phase has ended and the clock has started on reaching the EBP’s major milestones. This Special Feature explores the many facets of the EBP, including a review of progress, a description of major scientific goals, exemplar projects, ethical legal and social issues, and applications of biodiversity genomics. In this Introduction, we summarize the current status of the EBP, held virtually October 5 to 9, 2020, including recent updates through February 2021. References to the nine Perspective articles included in this Special Feature are cited to guide the reader toward deeper understanding of the goals and challenges facing the EBP.
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    A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 116(36), (2019): 17934-17942, doi:10.1073/pnas.1910121116.
    Description: Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host.
    Description: We are grateful to Martin Kolisko and Fabien Burki for helpful discussion about and comments on the phylogenetic analysis; and Filip Husnik and Vittorio Boscaro for valuable comments on the manuscript. This work was supported by a grant from the National Science Foundation to R.J.G. and P.J.K. (PLR-1341362) and from the Natural Sciences and Engineering Research Council of Canada to P.J.K. (RGPIN-2014-03994).
    Description: 2020-02-19
    Keywords: plastid endosymbiosis ; kleptoplasty ; dinoflagellates ; plastid integration
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    Global variability in seawater Mg:Ca and Sr:Ca ratios in the modern ocean (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lebrato, M., Garbe-Schönberg, D., Müller, M. N., Blanco-Ameijeiras, S., Feely, R. A., Lorenzoni, L., Molinero, J. C., Bremer, K., Jones, D. O. B., Iglesias-Rodriguez, D., Greeley, D., Lamare, M. D., Paulmier, A., Graco, M., Cartes, J., Barcelos E Ramos, J., de Lara, A., Sanchez-Leal, R., Jimenez, P., Paparazzo, F. E., Hartman, S. E., Westernströer, U., Küter, M., Benavides, R., da Silva, A. F., Bell, S., Payne, C., Olafsdottir, S., Robinson, K., Jantunen, L. M., Korablev, A., Webster, R. J., Jones, E. M., Gilg, O., Bailly du Bois, P., Beldowski, J., Ashjian, C., Yahia, N. D., Twining, B., Chen, X. G., Tseng, L. C., Hwang, J. S., Dahms, H. U., & Oschlies, A. Global variability in seawater Mg:Ca and Sr:Ca ratios in the modern ocean. Proceedings of the National Academy of Sciences of the United States of America, 117(36), (2020): 22281-22292, doi:10.1073/pnas.1918943117.
    Description: Seawater Mg:Ca and Sr:Ca ratios are biogeochemical parameters reflecting the Earth–ocean–atmosphere dynamic exchange of elements. The ratios’ dependence on the environment and organisms' biology facilitates their application in marine sciences. Here, we present a measured single-laboratory dataset, combined with previous data, to test the assumption of limited seawater Mg:Ca and Sr:Ca variability across marine environments globally. High variability was found in open-ocean upwelling and polar regions, shelves/neritic and river-influenced areas, where seawater Mg:Ca and Sr:Ca ratios range from ∼4.40 to 6.40 mmol:mol and ∼6.95 to 9.80 mmol:mol, respectively. Open-ocean seawater Mg:Ca is semiconservative (∼4.90 to 5.30 mol:mol), while Sr:Ca is more variable and nonconservative (∼7.70 to 8.80 mmol:mol); both ratios are nonconservative in coastal seas. Further, the Ca, Mg, and Sr elemental fluxes are connected to large total alkalinity deviations from International Association for the Physical Sciences of the Oceans (IAPSO) standard values. Because there is significant modern seawater Mg:Ca and Sr:Ca ratios variability across marine environments we cannot absolutely assume that fossil archives using taxa-specific proxies reflect true global seawater chemistry but rather taxa- and process-specific ecosystem variations, reflecting regional conditions. This variability could reconcile secular seawater Mg:Ca and Sr:Ca ratio reconstructions using different taxa and techniques by assuming an error of 1 to 1.50 mol:mol, and 1 to 1.90 mmol:mol, respectively. The modern ratios’ variability is similar to the reconstructed rise over 20 Ma (Neogene Period), nurturing the question of seminonconservative behavior of Ca, Mg, and Sr over modern Earth geological history with an overlooked environmental effect.
    Description: We thank the researchers, staff, students, and volunteers in all the expeditions around the world for their contributions. One anonymous referee and Bernhard Peucker-Ehenbrink, Woods Hole Oceanographic Institution, contributed significantly to the final version of the manuscript. This study was developed under a grant from the Federal Ministry of Education and Research to D.G.-S. under contract 03F0722A, by the Kiel Cluster of Excellence “The Future Ocean” (D1067/87) to A.O. and M.L., and by the “European project on Ocean Acidification” (European Community’s Seventh Framework Programme FP7/2007-2013, grant agreement 211384) to A.O. and M.L. Additional funding was provided from project DOSMARES CTM2010-21810-C03-02, by the UK Natural Environment Research Council, to the National Oceanography Centre. This is Pacific Marine Environmental Laboratory contribution number 5046.
    Keywords: global ; seawater ; Mg:Ca ; Sr:Ca ; biogeochemistry
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    Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 1997. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 94 (1997): 13743-13748.
    Description: The aryl hydrocarbon receptor (AHR) is a ligand-activated transcription factor through which halogenated aromatic hydrocarbons such as 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) cause altered gene expression and toxicity. The AHR belongs to the basic helix-loop-helix/Per-ARNT-Sim (bHLH-PAS) family of transcriptional regulatory proteins, whose members play key roles in development, circadian rhythmicity, and environmental homeostasis; however, the normal cellular function of the AHR is not yet known. As part of a phylogenetic approach to understanding the function and evolutionary origin of the AHR, we sequenced the PAS homology domain of AHRs from several species of early vertebrates and performed phylogenetic analyses of these AHR amino acid sequences in relation to mammalian AHRs and 24 other members of the PAS family. AHR sequences were identified in a teleost (the killifish Fundulus heteroclitus), two elasmobranch species (the skate Raja erinacea and the dogfish Mustelus canis), and a jawless fish (the lamprey Petromyzon marinus). Two putative AHR genes, designated AHR1 and AHR2, were found both in Fundulus and Mustelus. Phylogenetic analyses indicate that the AHR2 genes in these two species are orthologous, suggesting that an AHR gene duplication occurred early in vertebrate evolution and that multiple AHR genes may be present in other vertebrates. Database searches and phylogenetic analyses identified four putative PAS proteins in the nematode Caenorhabditis elegans, including possible AHR and ARNT homologs. Phylogenetic analysis of the PAS gene family reveals distinct clades containing both invertebrate and vertebrate PAS family members; the latter include paralogous sequences that we propose have arisen by gene duplication early in vertebrate evolution. Overall, our analyses indicate that the AHR is a phylogenetically ancient protein present in all living vertebrate groups (with a possible invertebrate homolog), thus providing an evolutionary perspective to the study of dioxin toxicity and AHR function.
    Description: This work was supported in part by the National Institute of Environmental Health Sciences (Grants R29 ES06272, F32 ES05644, and P42 ES07381), the Donaldson Charitable Trust, and a Christopher Haebler Frantz Fellowship (to M.A.S.).
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    Opinion: we need better data about the environmental persistence of plastic goods (2020)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2020. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 117(26), (2020): 14618-14621, doi:10.1073/pnas.2008009117.
    Description: Plastic pollution is one of the most visible and complex environmental issues today. Interested and concerned parties include researchers, governmental agencies, nongovernmental organizations, industry, media, and the general public. One key assumption behind the issue and the public outcry is that plastics last indefinitely in the environment, resulting in chronic exposure that harms animals and humans. But the data supporting this assumption are scant.
    Description: We thank Briana Prado, Cassia Armstrong, and Anna Walsh for their help with the review, Kenneth Kostel, Katie Linehan, Daniel Ward, and Rose Cory for feedback on an earlier version of this piece, John Furfey for assistance with tracking down the original sources of the environmental lifetime estimates, and Natalie Reiner for help with Fig. 1. We acknowledge financial support from Woods Hole Oceanographic Institution (Woods Hole, MA) and the Seaver Institute (Los Angeles, CA).
    Description: 2020-12-10
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    Causes of ice age intensification across the Mid-Pleistocene Transition (2017)
    National Academy of Sciences
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    Publication Date: 2022-05-26
    Description: © The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 114 (2017): 13114-13119, doi: 10.1073/pnas.1702143114.
    Description: During the Mid-Pleistocene Transition (MPT; 1,200–800 kya), Earth’s orbitally paced ice age cycles intensified, lengthened from ∼40,000 (∼40 ky) to ∼100 ky, and became distinctly asymmetrical. Testing hypotheses that implicate changing atmospheric CO2 levels as a driver of the MPT has proven difficult with available observations. Here, we use orbitally resolved, boron isotope CO2 data to show that the glacial to interglacial CO2 difference increased from ∼43 to ∼75 μatm across the MPT, mainly because of lower glacial CO2 levels. Through carbon cycle modeling, we attribute this decline primarily to the initiation of substantive dust-borne iron fertilization of the Southern Ocean during peak glacial stages. We also observe a twofold steepening of the relationship between sea level and CO2-related climate forcing that is suggestive of a change in the dynamics that govern ice sheet stability, such as that expected from the removal of subglacial regolith or interhemispheric ice sheet phase-locking. We argue that neither ice sheet dynamics nor CO2 change in isolation can explain the MPT. Instead, we infer that the MPT was initiated by a change in ice sheet dynamics and that longer and deeper post-MPT ice ages were sustained by carbon cycle feedbacks related to dust fertilization of the Southern Ocean as a consequence of larger ice sheets.
    Description: Research was supported by National Environmental Research Council (NERC) Studentship NE/I528626/1 (to T.B.C.); NERC Grant NE/P011381/1 (to T.B.C., M.P.H., G.L.F., E.J.R., and P.A.W.); NERC Fellowships NE/K00901X/1 (to M.P.H.), NE/I006346/1 (to G.L.F. and R.D.P), and NE/H006273/1 (to R.D.P.); Royal Society Wolfson Awards (to G.L.F. and P.A.W.); Australian Research Council Laureate Fellowship FL1201000050 (to E.J.R.); Swiss National Science Foundation Grant PP00P2-144811 (to S.L.J.); ETH Research Grant ETH-04 11-1 (to S.L.J.); European Research Council Consolidator Grant (ERC CoG) Grant 617462 (to H.P.); and NERC UK IODP Grant NE/F00141X/1 (to P.A.W.).
    Keywords: Boron isotopes ; MPT ; Geochemistry ; Carbon dioxide ; Paleoclimate
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    On the occurrence of cytochrome P450 in viruses (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2019. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 116(25), (2019):12343-12352, doi:10.1073/pnas.1901080116.
    Description: Genes encoding cytochrome P450 (CYP; P450) enzymes occur widely in the Archaea, Bacteria, and Eukarya, where they play important roles in metabolism of endogenous regulatory molecules and exogenous chemicals. We now report that genes for multiple and unique P450s occur commonly in giant viruses in the Mimiviridae, Pandoraviridae, and other families in the proposed order Megavirales. P450 genes were also identified in a herpesvirus (Ranid herpesvirus 3) and a phage (Mycobacterium phage Adler). The Adler phage P450 was classified as CYP102L1, and the crystal structure of the open form was solved at 2.5 Å. Genes encoding known redox partners for P450s (cytochrome P450 reductase, ferredoxin and ferredoxin reductase, and flavodoxin and flavodoxin reductase) were not found in any viral genome so far described, implying that host redox partners may drive viral P450 activities. Giant virus P450 proteins share no more than 25% identity with the P450 gene products we identified in Acanthamoeba castellanii, an amoeba host for many giant viruses. Thus, the origin of the unique P450 genes in giant viruses remains unknown. If giant virus P450 genes were acquired from a host, we suggest it could have been from an as yet unknown and possibly ancient host. These studies expand the horizon in the evolution and diversity of the enormously important P450 superfamily. Determining the origin and function of P450s in giant viruses may help to discern the origin of the giant viruses themselves.
    Description: We thank Dr. David Nes (Texas Tech University) for providing sterols and Dr. Matthieu Legendre and Dr. Chantal Abergel (CNRS, Marseille) for access to the P. celtis sequences. Drs. Irina Arkhipova, Mark Hahn, Judith Luborsky, and Ann Bucklin commented on the manuscript. The research was supported by a USA-UK Fulbright Scholarship and a Royal Society grant (to D.C.L.), the Boston University Superfund Research Program [NIH Grant 5P42ES007381 (to J.J.S. and J.V.G.) and NIH Grant 5U41HG003345 (to J.V.G.)], the European Regional Development Fund and Welsh Government Project BEACON (S.L.K.), the Woods Hole Center for Oceans and Human Health [NIH Grant P01ES021923 and National Science Foundation Grant OCE-1314642 (to J.J.S.)], and NIH Grant R01GM53753 (to T.L.P.).
    Description: 2019-12-05
    Keywords: cytochrome P450 ; virus ; evolution ; domains of life ; redox partner
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    Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone (2019)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (35), (2019): 17187-17192, doi:10.1073/pnas.1903067116.
    Description: Mesoscale eddies are critical components of the ocean’s “internal weather” system. Mixing and stirring by eddies exerts significant control on biogeochemical fluxes in the open ocean, and eddies may trap distinctive plankton communities that remain coherent for months and can be transported hundreds to thousands of kilometers. Debate regarding how and why predators use fronts and eddies, for example as a migratory cue, enhanced forage opportunities, or preferred thermal habitat, has been ongoing since the 1950s. The influence of eddies on the behavior of large pelagic fishes, however, remains largely unexplored. Here, we reconstruct movements of a pelagic predator, the blue shark (Prionace glauca), in the Gulf Stream region using electronic tags, earth-observing satellites, and data-assimilating ocean forecasting models. Based on 〉2,000 tracking days and nearly 500,000 high-resolution time series measurements collected by 15 instrumented individuals, we show that blue sharks seek out the interiors of anticyclonic eddies where they dive deep while foraging. Our observations counter the existing paradigm that anticyclonic eddies are unproductive ocean “deserts” and suggest anomalously warm temperatures in these features connect surface-oriented predators to the most abundant fish community on the planet in the mesopelagic. These results also shed light on the ecosystem services provided by mesopelagic prey. Careful consideration will be needed before biomass extraction from the ocean twilight zone to avoid interrupting a key link between planktonic production and top predators. Moreover, robust associations between targeted fish species and oceanographic features increase the prospects for effective dynamic ocean management.
    Description: We thank D. McGillicuddy, G. Lawson, and G. Flierl for helpful discussions while developing this work and 2 anonymous reviewers whose feedback significantly improved the manuscript. We also thank C. Fischer and the OCEARCH team for their support of this research. This work was funded by awards to C.D.B. from the Martin Family Society of Fellows for Sustainability Fellowship at the Massachusetts Institute of Technology; the Grassle Fellowship and Ocean Venture Fund at the Woods Hole Oceanographic Institution; and the National Aeronatics and Space Administration (NASA) Earth and Space Science Fellowship. C.D.B. and P.G. acknowledge support from the NASA New Investigator Program Award 80NSSC18K0757, and P.G. acknowledges support from NSF Award OCE-1558809. This research is partially supported by funding to S.R.T. as part of the Audacious Project, a collaborative endeavor, housed at TED. We thank donors to the Woods Hole Oceanographic Institution (WHOI) ProjectWHOI crowdfunding campaign: The Secret Lives of Sharks. Computational support was provided by the Amazon Web Services Cloud Credits for Research program. Funding for the development of HYCOM has been provided by the National Ocean Partnership Program and the Office of Naval Research.
    Description: 2020-02-06
    Keywords: remote sensing ; oceanographic model ; satellite telemetry ; marine predator ; mesopelagic
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    A productivity collapse to end earth's great oxidation (2019)
    National Academy of Sciences
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    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (35), (2019): 17207-17212, doi:10.1073/pnas.1900325116.
    Description: It has been hypothesized that the overall size of—or efficiency of carbon export from—the biosphere decreased at the end of the Great Oxidation Event (GOE) (ca. 2,400 to 2,050 Ma). However, the timing, tempo, and trigger for this decrease remain poorly constrained. Here we test this hypothesis by studying the isotope geochemistry of sulfate minerals from the Belcher Group, in subarctic Canada. Using insights from sulfur and barium isotope measurements, combined with radiometric ages from bracketing strata, we infer that the sulfate minerals studied here record ambient sulfate in the immediate aftermath of the GOE (ca. 2,018 Ma). These sulfate minerals captured negative triple-oxygen isotope anomalies as low as ∼ −0.8‰. Such negative values occurring shortly after the GOE require a rapid reduction in primary productivity of 〉80%, although even larger reductions are plausible. Given that these data imply a collapse in primary productivity rather than export efficiency, the trigger for this shift in the Earth system must reflect a change in the availability of nutrients, such as phosphorus. Cumulatively, these data highlight that Earth’s GOE is a tale of feast and famine: A geologically unprecedented reduction in the size of the biosphere occurred across the end-GOE transition.
    Description: Olivia M. J. Dagnaud assisted during fieldwork. S. V. Lalonde and E. A. Sperling provided helpful comments on an early version of the manuscript. We thank N. J. Planavsky and an anonymous reviewer for their constructive feedback. M.S.W.H. was supported by an NSERC PGS-D and student research grants from National Geographic, the APS Lewis and Clark Fund, Northern Science Training Program, McGill University Graduate Research Enhancement and Travel Awards, Geological Society of America, Mineralogical Association of Canada, and Stanford University. P.W.C. acknowledges support from the University of Colorado Boulder, the Agouron Institute Geobiology postdoctoral Fellowship program, a Natural Sciences and Engineering Council of Canada Postgraduate Scholarship–Doctoral Program scholarship, and the NSTP. Y.P. was supported by the Strategic Priority Research Program of CAS (XDB26000000). T.J.H. thanks Maureen E. Auro for laboratory assistance and the NSF for supporting isotope research in the NIRVANA Labs.
    Description: 2020-02-12
    Keywords: Proterozoic ; primary productivity ; Great Oxidation Event ; triple-oxygen isotopes ; nutrient limitation
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    Sustained wood burial in the Bengal Fan over the last 19 My (2019)
    National Academy of Sciences
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    Publication Date: 2022-05-26
    Description: Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116(45), (2019): 22518-22525, doi:10.1073/pnas.1913714116.
    Description: The Ganges–Brahmaputra (G-B) River system transports over a billion tons of sediment every year from the Himalayan Mountains to the Bay of Bengal and has built the world’s largest active sedimentary deposit, the Bengal Fan. High sedimentation rates drive exceptional organic matter preservation that represents a long-term sink for atmospheric CO2. While much attention has been paid to organic-rich fine sediments, coarse sediments have generally been overlooked as a locus of organic carbon (OC) burial. However, International Ocean Discovery Program Expedition 354 recently discovered abundant woody debris (millimeter- to centimeter-sized fragments) preserved within the coarse sediment layers of turbidite beds recovered from 6 marine drill sites along a transect across the Bengal Fan (∼8°N, ∼3,700-m water depth) with recovery spanning 19 My. Analysis of bulk wood and lignin finds mostly lowland origins of wood delivered episodically. In the last 5 My, export included C4 plants, implying that coarse woody, lowland export continued after C4 grassland expansion, albeit in reduced amounts. Substantial export of coarse woody debris in the last 1 My included one wood-rich deposit (∼0.05 Ma) that encompassed coniferous wood transported from the headwaters. In coarse layers, we found on average 0.16 weight % OC, which is half the typical biospheric OC content of sediments exported by the modern G-B Rivers. Wood burial estimates are hampered by poor drilling recovery of sands. However, high-magnitude, low-frequency wood export events are shown to be a key mechanism for C burial in turbidites.
    Description: This work was funded by National Science Foundation Grants OCE-1401217 and COL-T354A55 to S.J.F. and OCE-1400805 to V.G. Graduate student participation in the project received support from University of Southern California Provost’s Fellowship to H.L. Samples were provided by the International Ocean Discovery Program. We are grateful for the efforts of the Expedition 354 Science Party, Carl Johnson, and Zongguang Liu. C.F.-L. and A.G. were supported by IODP-France. We thank Colin Osborne and Maria Vorontsova for helpful discussions.
    Description: 2020-04-21
    Keywords: carbon cycle ; wood ; lignin ; Himalaya ; Bengal Fan
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    Sodium channel genes and the evolution of diversity in communication signals of electric fishes : convergent molecular evolution (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © National Academy of Sciences, 2006. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 103 (2006): 3675-3680, doi:10.1073/pnas.0600160103.
    Description: We investigated whether the evolution of electric organs and electric signal diversity in two independently evolved lineages of electric fishes was accompanied by convergent changes on the molecular level. We found that a sodium channel gene (Nav1.4a) that is expressed in muscle in nonelectric fishes has lost its expression in muscle and is expressed instead in the evolutionarily novel electric organ in both lineages of electric fishes. This gene appears to be evolving under positive selection in both lineages, facilitated by its restricted expression in the electric organ. This view is reinforced by the lack of evidence for selection on this gene in one electric species in which expression of this gene is retained in muscle. Amino acid replacements occur convergently in domains that influence channel inactivation, a key trait for shaping electric communication signals. Some amino acid replacements occur at or adjacent to sites at which disease-causing mutations have been mapped in human sodium channel genes, emphasizing that these replacements occur in functionally important domains. Selection appears to have acted on the final step in channel inactivation, but complementarily on the inactivation "ball" in one lineage, and its receptor site in the other lineage. Thus, changes in the expression and sequence of the same gene are associated with the independent evolution of signal complexity.
    Description: This work was funded by National Institutes of Health Grant R01 NS025513 (to H.H.Z. and Y.L.) and National Science Foundation Integrative Graduate Education and Research Traineeship Program DGE-0114387 (to D.J.Z. and D.M.H.).
    Keywords: Animal communication ; Electric organ ; Channel inactivation ; Protein evolution ; Positive selection
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    Vailulu'u Seamount, Samoa : life and death on an active submarine volcano (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © National Academy of Sciences, 2006. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 103 (2006): 6448-6453, doi:10.1073/pnas.0600830103.
    Description: Submersible exploration of the Samoan hotspot revealed a new, 300-m-tall, volcanic cone, named Nafanua, in the summit crater of Vailulu'u seamount. Nafanua grew from the 1,000-m-deep crater floor in 〈4 years and could reach the sea surface within decades. Vents fill Vailulu'u crater with a thick suspension of particulates and apparently toxic fluids that mix with seawater entering from the crater breaches. Low-temperature vents form Fe oxide chimneys in many locations and up to 1-m-thick layers of hydrothermal Fe floc on Nafanua. High-temperature (81°C) hydrothermal vents in the northern moat (945-m water depth) produce acidic fluids (pH 2.7) with rising droplets of (probably) liquid CO2. The Nafanua summit vent area is inhabited by a thriving population of eels (Dysommina rugosa) that feed on midwater shrimp probably concentrated by anticyclonic currents at the volcano summit and rim. The moat and crater floor around the new volcano are littered with dead metazoans that apparently died from exposure to hydrothermal emissions. Acid-tolerant polychaetes (Polynoidae) live in this environment, apparently feeding on bacteria from decaying fish carcasses. Vailulu'u is an unpredictable and very active underwater volcano presenting a potential long-term volcanic hazard. Although eels thrive in hydrothermal vents at the summit of Nafanua, venting elsewhere in the crater causes mass mortality. Paradoxically, the same anticyclonic currents that deliver food to the eels may also concentrate a wide variety of nektonic animals in a death trap of toxic hydrothermal fluids.
    Description: This work was supported by the National Oceanic and Atmospheric Administration (NOAA) Oceans Exploration and the Hawaii Undersea Research Laboratory–NOAA Undersea Research Program, the National Science Foundation, the Australian Research Council, and the SERPENT program.
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    Nitrate is an important nitrogen source for Arctic tundra plants (2018)
    National Academy of Sciences
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    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 115 (2018): 3398-3403, doi:10.1073/pnas.1715382115.
    Description: Plant nitrogen (N) use is a key component of the N cycle in terrestrial ecosystems. The supply of N to plants affects community species composition and ecosystem processes such as photosynthesis and carbon (C) accumulation. However, the availabilities and relative importance of different N forms to plants are not well understood. While nitrate (NO3−) is a major N form used by plants worldwide, it is discounted as a N source for Arctic tundra plants because of extremely low NO3− concentrations in Arctic tundra soils, undetectable soil nitrification, and plant-tissue NO3− that is typically below detection limits. Here we reexamine NO3− use by tundra plants using a sensitive denitrifier method to analyze plant-tissue NO3−. Soil-derived NO3− was detected in tundra plant tissues, and tundra plants took up soil NO3− at comparable rates to plants from relatively NO3−-rich ecosystems in other biomes. Nitrate assimilation determined by 15N enrichments of leaf NO3− relative to soil NO3− accounted for 4 to 52% (as estimated by a Bayesian isotope-mixing model) of species-specific total leaf N of Alaskan tundra plants. Our finding that in situ soil NO3− availability for tundra plants is high has important implications for Arctic ecosystems, not only in determining species compositions, but also in determining the loss of N from soils via leaching and denitrification. Plant N uptake and soil N losses can strongly influence C uptake and accumulation in tundra soils. Accordingly, this evidence of NO3− availability in tundra soils is crucial for predicting C storage in tundra.
    Description: his study was supported by the Kyoto University Foundation, the Sumitomo Foundation, Program for Next Generation World-Leading Researcher (Grant GS008) and Grant-in-Aid for Scientific Research (KAKENHI Grants 26252020, 26550004, 17H06297, and P09316) from the Japan Society for Promotion of Science, the National Natural Science Foundation of China (Grants 41730855, 41522301, and 41473081), the National Key Research and Development Program of China (Grants 2016YFA0600802 and 2017YFC0210101), and the 11th Recruitment Program of Global Experts (the Thousand Talents Plan) for Young Professionals granted by the central budget of China.
    Keywords: Arctic tundra plants ; Nitrogen dynamics ; Plant nitrate ; Soil nitrate ; Stable isotopes
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    Primary productivity below the seafloor at deep-sea hot springs (2018)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 115 (2018): 6756–6761, doi:10.1073/pnas.1804351115.
    Description: The existence of a chemosynthetic subseafloor biosphere was immediately recognized when deep-sea hot springs were discovered in 1977. However, quantifying how much new carbon is fixed in this environment has remained elusive. In this study, we incubated natural subseafloor communities under in situ pressure/temperature and measured their chemosynthetic growth efficiency and metabolic rates. Combining these data with fluid flux and in situ chemical measurements, we derived empirical constraints on chemosynthetic activity in the natural environment. Our study shows subseafloor microorganisms are highly productive (up to 1.4 Tg C produced yearly), fast-growing (turning over every 17–41 hours), and physiologically diverse. These estimates place deep-sea hot springs in a quantitative framework and allow us to assess their importance for global biogeochemical cycles.
    Description: This research was funded by a grant of the Dimensions of Biodiversity program of the US National Science Foundation (NSF-OCE-1136727 to S.M.S. and J.S.S.). Funding for J.M. was further provided by doctoral fellowships from the Natural Sciences and Engineering Research Council of Canada (PGSD3-430487-2013, PGSM-405117-2011) and the National Aeronautics and Space Administration Earth Systems Science Fellowship (PLANET14F-0075), an award from the Canadian Meteorological and Oceanographic Society, and the WHOI Academic Programs Office.
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    Heterotrophic Archaea dominate sedimentary subsurface ecosystems off Peru (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © National Academy of Sciences, 2006. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 103 (2006): 3846-3851, doi:10.1073/pnas.0600035103.
    Description: Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane–carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100–2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.
    Description: This work was supported by Deutsche Forschungsgemeinschaft (to J.S.L., R.A., M.E., and K.-U.H. at Research Center for Ocean Margins and Grant Hi 616/4 to K.U.-H.); National Aeronautics and Space Administration Astrobiology Institute Grants NNA04CC06A (to J.E.B. and C.H.H. at Pennsylvania State University), NCC 2-1275 (to M.A.L., K.G.L., K.B.S., H.F.F., A.T., and K.-U.H. at the University of Rhode Island), and NCC 2-1054 (to M.L.S. and A.T. at the Marine Biological Laboratory); the G. Unger Vetlesen Foundation; U.S. Department of Energy Grant DE-FG02-93ER20117; and NSF Grant MCB03-48492. J.F.B. was supported by NSF Integrative Graduate Education and Research Traineeship Program Grant DGE-9972759 and a Schlanger fellowship from the Joint Oceanographic Institutions (JOI). M.A.L. was supported in part by postcruise support from JOI.
    Keywords: Anaerobic methanotrophy ; Deep biosphere ; FISH–secondary ion MS ; Intact polar lipids ; Stable carbon isotopes
    Repository Name: Woods Hole Open Access Server
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    A ligand for the aryl hydrocarbon receptor isolated from lung (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © National Academy of Sciences, 2002. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 99 (2002): 14694-14699, doi:10.1073/pnas.232562899.
    Description: The aryl hydrocarbon receptor (AHR) is a ligand-inducible transcription factor that is best known because it mediates the actions of polycyclic and halogenated aromatic hydrocarbon environmental toxicants such as 3-methylcholanthrene and 2,3,7,8-tetrachlorodibenzo-p-dioxin. We report here the successful identification of an endogenous ligand for this receptor; {approx}20 µg was isolated in pure form from 35 kg of porcine lung. Its structure was deduced as 2-(1'H-indole-3'-carbonyl)-thiazole-4-carboxylic acid methyl ester from extensive physical measurements and quantum mechanical calculations. In a reporter gene assay, this ligand activates the AHR with a potency five times greater than that of {beta}-naphthoflavone, a prototypical synthetic AHR ligand. 2-(1'H-indole-3'-carbonyl)-thiazole-4-carboxylic acid methyl ester competes with 2,3,7,8-[3H]tetrachlorodibenzo-p-dioxin for binding to human, murine, and fish AHRs, thus showing that AHR activation is caused by direct receptor binding, and that recognition of this endogenous ligand is conserved from early vertebrates (fish) to humans.
    Description: This work was supported by the Wisconsin Alumni Research Foundation, the University of Wisconsin Sea Grant Institute, and the National Institutes of Health.
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    The molecular basis for differential dioxin sensitivity in birds : role of the aryl hydrocarbon receptor (2006)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: Author Posting. © National Academy of Sciences, 2006. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 103 (2006): 6252-6257, doi:10.1073/pnas.0509950103.
    Description: 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and related halogenated aromatic hydrocarbons (HAHs) are highly toxic to most vertebrate animals, but there are dramatic differences in sensitivity among species and strains. Aquatic birds including the common tern (Sterna hirundo) are highly exposed to HAHs in the environment, but are up to 250-fold less sensitive to these compounds than the typical avian model, the domestic chicken (Gallus gallus). The mechanism of HAH toxicity involves altered gene expression subsequent to activation of the aryl hydrocarbon receptor (AHR), a basic helix–loop–helix-PAS transcription factor. AHR polymorphisms underlie mouse strain differences in sensitivity to HAHs and polynuclear aromatic hydrocarbons, but the role of the AHR in species differences in HAH sensitivity is not well understood. Here, we show that although chicken and tern AHRs both exhibit specific binding of [3H]TCDD, the tern AHR has a lower binding affinity and exhibits a reduced ability to support TCDD-dependent transactivation as compared to AHRs from chicken or mouse. We further show through use of chimeric AHR proteins and site-directed mutagenesis that the difference between the chicken and tern AHRs resides in the ligand-binding domain and that two amino acids (Val-325 and Ala-381) are responsible for the reduced activity of the tern AHR. Other avian species with reduced sensitivity to HAHs also possess these residues. These studies provide a molecular understanding of species differences in sensitivity to dioxin-like compounds and suggest an approach to using the AHR as a marker of dioxin susceptibility in wildlife.
    Description: This research was supported by the National Oceanographic and Atmospheric Administration National Sea Grant College Program, Department of Commerce, under Grants NA46RG0470 and NA16RG2273.
    Keywords: Basic helix–loop–helix-PAS ; Comparative toxicology ; Mechanisms ; Risk assessment ; Susceptibility
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    River-discharge effects on United States Atlantic and Gulf coast sea-level changes (2018)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences.of the United States of America 115 (2018): 7729-7734, doi:10.1073/pnas.1805428115.
    Description: Identifying physical processes responsible for historical coastal sea-level changes is important for anticipating future impacts. Recent studies sought to understand the drivers of interannual to multidecadal sea-level changes on the United States Atlantic and Gulf coasts. Ocean dynamics, terrestrial water storage, vertical land motion, and melting of land ice were highlighted as important mechanisms of sea-level change along this densely populated coast on these time scales. While known to exert an important control on coastal ocean circulation, variable river discharge has been absent from recent discussions of drivers of sea-level change. We update calculations from the 1970s, comparing annual river-discharge and coastal sea-level data along the Gulf of Maine, Mid-Atlantic Bight, South Atlantic Bight, and Gulf of Mexico during 1910–2017. We show that river-discharge and sea-level changes are significantly correlated (p〈0.01), such that sea level rises between 0.01 and 0.08 cm for a 1 km3 annual river-discharge increase, depending on region. We formulate a theory that describes the relation between river-discharge and halosteric sea-level changes (i.e., changes in sea level related to salinity) as a function of river discharge, Earth’s rotation, and density stratification. This theory correctly predicts the order of observed increment sea-level change per unit river-discharge anomaly, suggesting a causal relation. Our results have implications for remote sensing, climate modeling, interpreting Common Era proxy sea-level reconstructions, and projecting coastal flood risk.
    Description: C.G.P. and R.M.P. acknowledge support from NASA Contract NNH16CT01C (which also supported C.M.L.), NASA Jet Propulsion Laboratory Subcontract 1569246, and National Science Foundation Award 1558966. C.G.P. also acknowledges support from The Investment in Science Fund at Woods Hole Oceanographic Institution. A.C.K. and S.E.E. acknowledge NSF Awards OCE-1458921 and OCE-1458903, respectively.
    Keywords: Coastal sea level ; Coastal river plumes ; Coastal flood risk ; Climate modeling ; Physical oceanography
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    Different iron storage strategies among bloom-forming diatoms (2019)
    National Academy of Sciences
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    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2018. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 115(52), (2018): E12275-E12284. doi: 10.1073/pnas.1805243115.
    Description: Diatoms are prominent eukaryotic phytoplankton despite being limited by the micronutrient iron in vast expanses of the ocean. As iron inputs are often sporadic, diatoms have evolved mechanisms such as the ability to store iron that enable them to bloom when iron is resupplied and then persist when low iron levels are reinstated. Two iron storage mechanisms have been previously described: the protein ferritin and vacuolar storage. To investigate the ecological role of these mechanisms among diatoms, iron addition and removal incubations were conducted using natural phytoplankton communities from varying iron environments. We show that among the predominant diatoms, Pseudo-nitzschia were favored by iron removal and displayed unique ferritin expression consistent with a long-term storage function. Meanwhile, Chaetoceros and Thalassiosira gene expression aligned with vacuolar storage mechanisms. Pseudo-nitzschia also showed exceptionally high iron storage under steady-state high and low iron conditions, as well as following iron resupply to iron-limited cells. We propose that bloom-forming diatoms use different iron storage mechanisms and that ferritin utilization may provide an advantage in areas of prolonged iron limitation with pulsed iron inputs. As iron distributions and availability change, this speculated ferritin-linked advantage may result in shifts in diatom community composition that can alter marine ecosystems and biogeochemical cycles.
    Description: We thank the captain and crew of the R/V Melville and the CCGS J. P. Tully as well as the participants of the IRNBRU (MV1405) cruise for the California-based data, particularly K. Ellis [University of North Carolina (UNC)], T. Coale (University of California, San Diego), F. Kuzminov (Rutgers), H. McNair [University of California, Santa Barbara (UCSB)], and J. Jones (UCSB). W. Burns (UNC), S. Haines (UNC), and S. Bargu (Louisiana State University) assisted with sample processing and analysis. This work was funded by the National Science Foundation Grants OCE-1334935 (to A.M.), OCE-1334632 (to B.S.T.), OCE-1333929 (to K.T.), OCE-1334387 (to M.A.B.), OCE-1259776 (to K.W.B), and DGE-1650116 (Graduate Research Fellowship to R.H.L).
    Description: 2019-06-11
    Keywords: phytoplankton ; iron limitation ; Pseudo-nitzschia ; ferritin ; metatranscriptomics
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    Elesclomol restores mitochondrial function in genetic models of copper deficiency (2018)
    National Academy of Sciences
    Details
    Publication Date: 2022-05-25
    Description: © The Author(s), 2018. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 115 (2018): 8161-8166, doi:10.1073/pnas.1806296115.
    Description: Copper is an essential cofactor of cytochrome c oxidase (CcO), the terminal enzyme of the mitochondrial respiratory chain. Inherited loss-of-function mutations in several genes encoding proteins required for copper delivery to CcO result in diminished CcO activity and severe pathologic conditions in affected infants. Copper supplementation restores CcO function in patient cells with mutations in two of these genes, COA6 and SCO2, suggesting a potential therapeutic approach. However, direct copper supplementation has not been therapeutically effective in human patients, underscoring the need to identify highly efficient copper transporting pharmacological agents. By using a candidate-based approach, we identified an investigational anticancer drug, elesclomol (ES), that rescues respiratory defects of COA6-deficient yeast cells by increasing mitochondrial copper content and restoring CcO activity. ES also rescues respiratory defects in other yeast mutants of copper metabolism, suggesting a broader applicability. Low nanomolar concentrations of ES reinstate copper-containing subunits of CcO in a zebrafish model of copper deficiency and in a series of copper-deficient mammalian cells, including those derived from a patient with SCO2 mutations. These findings reveal that ES can restore intracellular copper homeostasis by mimicking the function of missing transporters and chaperones of copper, and may have potential in treating human disorders of copper metabolism.
    Description: This work was supported by National Institutes of Health Awards R01GM111672 (to V.M.G.), R01 DK110195 (to B.-E.K.), and DK 44464 (to J.D.G.); Welch Foundation Grant A-1810 (to V.M.G.); and Canadian Institutes of Health Research Operating Grant MOP 133562 (to S.C.L.).
    Keywords: Copper ; Mitochondria ; Elesclomol ; Cytochrome c oxidase
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    A kleptoplastidic dinoflagellate and the tipping point between transient and fully integrated plastid endosymbiosis (2019)
    National Academy of Sciences
    In:  PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (36). pp. 17934-17942.
    Details
    Publication Date: 2022-01-31
    Description: Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduced, lost, and replaced by new plastids, leading to a spectrum of ages and integration levels. Here we describe deep-transcriptomic analyses of the Antarctic Ross Sea dinoflagellate (RSD), which harbors long-term but temporary kleptoplasts stolen from haptophyte prey, and is closely related to dinoflagellates with fully integrated plastids derived from different haptophytes. In some members of this lineage, called the Kareniaceae, their tertiary haptophyte plastids have crossed a tipping point to stable integration, but RSD has not, and may therefore reveal the order of events leading up to endosymbiotic integration. We show that RSD has retained its ancestral secondary plastid and has partitioned functions between this plastid and the kleptoplast. It has also obtained genes for kleptoplast-targeted proteins via horizontal gene transfer (HGT) that are not derived from the kleptoplast lineage. Importantly, many of these HGTs are also found in the related species with fully integrated plastids, which provides direct evidence that genetic integration preceded organelle fixation. Finally, we find that expression of kleptoplast-targeted genes is unaffected by environmental parameters, unlike prey-encoded homologs, suggesting that kleptoplast-targeted HGTs have adapted to posttranscriptional regulation mechanisms of the host.
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    A distinct lineage of giant viruses brings a rhodopsin photosystem to unicellular marine predators (2019)
    National Academy of Sciences
    In:  PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (41). pp. 20574-20583.
    Details
    Publication Date: 2022-01-31
    Description: Significance: Although viruses are well-characterized regulators of eukaryotic algae, little is known about those infecting unicellular predators in oceans. We report the largest marine virus genome yet discovered, found in a wild predatory choanoflagellate sorted away from other Pacific microbes and pursued using integration of cultivation-independent and laboratory methods. The giant virus encodes nearly 900 proteins, many unlike known proteins, others related to cellular metabolism and organic matter degradation, and 3 type-1 rhodopsins. The viral rhodopsin that is most abundant in ocean metagenomes, and also present in an algal virus, pumps protons when illuminated, akin to cellular rhodopsins that generate a proton-motive force. Giant viruses likely provision multiple host species with photoheterotrophic capacities, including predatory unicellular relatives of animals. Abstract: Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovered a Mimiviridae lineage of giant viruses, which infects choanoflagellates, widespread protistan predators related to metazoans. The ChoanoVirus genomes are the largest yet from pelagic ecosystems, with 442 of 862 predicted proteins lacking known homologs. They are enriched in enzymes for modifying organic compounds, including degradation of chitin, an abundant polysaccharide in oceans, and they encode 3 divergent type-1 rhodopsins (VirR) with distinct evolutionary histories from those that capture sunlight in cellular organisms. One (VirRDTS) is similar to the only other putative rhodopsin from a virus (PgV) with a known host (a marine alga). Unlike the algal virus, ChoanoViruses encode the entire pigment biosynthesis pathway and cleavage enzyme for producing the required chromophore, retinal. We demonstrate that the rhodopsin shared by ChoanoViruses and PgV binds retinal and pumps protons. Moreover, our 1.65-Å resolved VirRDTS crystal structure and mutational analyses exposed differences from previously characterized type-1 rhodopsins, all of which come from cellular organisms. Multiple VirR types are present in metagenomes from across surface oceans, where they are correlated with and nearly as abundant as a canonical marker gene from Mimiviridae. Our findings indicate that light-dependent energy transfer systems are likely common components of giant viruses of photosynthetic and phagotrophic unicellular marine eukaryotes.
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    Metabolic preference of nitrate over oxygen as an electron acceptor in foraminifera from the Peruvian oxygen minimum zone (2019)
    National Academy of Sciences
    In:  PNAS Proceedings of the National Academy of Sciences of the United States of America, 116 (8). pp. 2860-2865.
    Details
    Publication Date: 2022-01-31
    Description: Benthic foraminifera populate a diverse range of marine habitats. Their ability to use alternative electron acceptors—nitrate (NO3−) or oxygen (O2)—makes them important mediators of benthic nitrogen cycling. Nevertheless, the metabolic scaling of the two alternative respiration pathways and the environmental determinants of foraminiferal denitrification rates are yet unknown. We measured denitrification and O2 respiration rates for 10 benthic foraminifer species sampled in the Peruvian oxygen minimum zone (OMZ). Denitrification and O2 respiration rates significantly scale sublinearly with the cell volume. The scaling is lower for O2 respiration than for denitrification, indicating that NO3− metabolism during denitrification is more efficient than O2 metabolism during aerobic respiration in foraminifera from the Peruvian OMZ. The negative correlation of the O2 respiration rate with the surface/volume ratio is steeper than for the denitrification rate. This is likely explained by the presence of an intracellular NO3− storage in denitrifying foraminifera. Furthermore, we observe an increasing mean cell volume of the Peruvian foraminifera, under higher NO3− availability. This suggests that the cell size of denitrifying foraminifera is not limited by O2 but rather by NO3− availability. Based on our findings, we develop a mathematical formulation of foraminiferal cell volume as a predictor of respiration and denitrification rates, which can further constrain foraminiferal biogeochemical cycling in biogeochemical models. Our findings show that NO3− is the preferred electron acceptor in foraminifera from the OMZ, where the foraminiferal contribution to denitrification is governed by the ratio between NO3− and O2.
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    Widespread global peatland establishment and persistence over the last 130,000 y (2019)
    National Academy of Sciences
    In:  Proceedings of the National Academy of Sciences of the United States of America (PNAS), 116 (11). pp. 4822-4827.
    Details
    Publication Date: 2022-01-31
    Description: Significance During the Holocene (11,600 y ago to present), northern peatlands accumulated significant C stocks over millennia. However, virtually nothing is known about peatlands that are no longer in the landscape, including ones formed prior to the Holocene: Where were they, when did they form, and why did they disappear? We used records of peatlands buried by mineral sediments for a reconstruction of peat-forming wetlands for the past 130,000 y. Northern peatlands expanded across high latitudes during warm periods and were buried during periods of glacial advance in northern latitudes. Thus, peat accumulation and burial represent a key long-term C storage mechanism in the Earth system. Abstract Glacial−interglacial variations in CO2 and methane in polar ice cores have been attributed, in part, to changes in global wetland extent, but the wetland distribution before the Last Glacial Maximum (LGM, 21 ka to 18 ka) remains virtually unknown. We present a study of global peatland extent and carbon (C) stocks through the last glacial cycle (130 ka to present) using a newly compiled database of 1,063 detailed stratigraphic records of peat deposits buried by mineral sediments, as well as a global peatland model. Quantitative agreement between modeling and observations shows extensive peat accumulation before the LGM in northern latitudes (〉40°N), particularly during warmer periods including the last interglacial (130 ka to 116 ka, MIS 5e) and the interstadial (57 ka to 29 ka, MIS 3). During cooling periods of glacial advance and permafrost formation, the burial of northern peatlands by glaciers and mineral sediments decreased active peatland extent, thickness, and modeled C stocks by 70 to 90% from warmer times. Tropical peatland extent and C stocks show little temporal variation throughout the study period. While the increased burial of northern peats was correlated with cooling periods, the burial of tropical peat was predominately driven by changes in sea level and regional hydrology. Peat burial by mineral sediments represents a mechanism for long-term terrestrial C storage in the Earth system. These results show that northern peatlands accumulate significant C stocks during warmer times, indicating their potential for C sequestration during the warming Anthropocene.
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    Volcanic ash layers illuminate the resilience of Neanderthals and early modern humans to natural hazards (2012)
    National Academy of Sciences
    Details
    Publication Date: 2021-12-06
    Description: Marked changes in human dispersal and development during the Middle to Upper Paleolithic transition have been attributed to massive volcanic eruption and/or severe climatic deterioration. We test this concept using records of volcanic ash layers of the Campanian Ignimbrite eruption dated to ca. 40,000 y ago (40 ka B.P.). The distribution of the Campanian Ignimbrite has been enhanced by the discovery of cryptotephra deposits (volcanic ash layers that are not visible to the naked eye) in archaeological cave sequences. They enable us to synchronize archaeological and paleoclimatic records through the period of transition from Neanderthal to the earliest anatomically modern human populations in Europe. Our results con!rm that the combined effects of a major volcanic eruption and severe climatic cooling failed to have lasting impacts on Neanderthals or early modern humans in Europe. We infer that modern humans proved a greater competitive threat to indigenous populations than natural disasters.
    Description: funded by the United Kingdom Natural Environment Research Council through a Response of Humans to Abrupt Environmental Transitions (RESET) Consortium Grant
    Description: Published
    Description: 13532–13537
    Description: 3.5. Geologia e storia dei vulcani ed evoluzione dei magmi
    Description: JCR Journal
    Description: restricted
    Keywords: Neanderthals ; modern humans ; cryptotephra deposits ; 01. Atmosphere::01.01. Atmosphere::01.01.07. Volcanic effects
    Repository Name: Istituto Nazionale di Geofisica e Vulcanologia (INGV)
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    SARS-CoV-2 evolution in animals suggests mechanisms for rapid variant selection (2021)
    National Academy of Sciences
    Details
    Publication Date: 2021-10-29
    Description: SARS-CoV-2 spillback from humans into domestic and wild animals has been well documented, and an accumulating number of studies illustrate that human-to-animal transmission is widespread in cats, mink, deer, and other species. Experimental inoculations of cats, mink, and ferrets have perpetuated transmission cycles. We sequenced full genomes of Vero cell–expanded SARS-CoV-2 inoculum and viruses recovered from cats (n = 6), dogs (n = 3), hamsters (n = 3), and a ferret (n = 1) following experimental exposure. Five nonsynonymous changes relative to the USA-WA1/2020 prototype strain were near fixation in the stock used for inoculation but had reverted to wild-type sequences at these sites in dogs, cats, and hamsters within 1- to 3-d postexposure. A total of 14 emergent variants (six in nonstructural genes, six in spike, and one each in orf8 and nucleocapsid) were detected in viruses recovered from animals. This included substitutions in spike residues H69, N501, and D614, which also vary in human lineages of concern. Even though a live virus was not cultured from dogs, substitutions in replicase genes were detected in amplified sequences. The rapid selection of SARS-CoV-2 variants in vitro and in vivo reveals residues with functional significance during host switching. These observations also illustrate the potential for spillback from animal hosts to accelerate the evolution of new viral lineages, findings of particular concern for dogs and cats living in households with COVID-19 patients. More generally, this glimpse into viral host switching reveals the unrealized rapidity and plasticity of viral evolution in experimental animal model systems.
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    The middle cingulate cortex and dorso-central insula: A mirror circuit encoding observation and execution of vitality forms (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Actions with identical goals can be executed in different ways (gentle, rude, vigorous, etc.), which D. N. Stern called vitality forms [D. N. Stern, Forms of Vitality Exploring Dynamic Experience in Psychology, Arts, Psychotherapy, and Development (2010)]. Vitality forms express the agent’s attitudes toward others. In a series of fMRI studies, we found that the dorso-central insula (DCI) is the region that is selectively active during both vitality form observation and execution. In one previous experiment, however, the middle cingulate gyrus also exhibited activation. In the present study, in order to assess the role of the cingulate cortex in vitality form processing, we adopted a classical vitality form paradigm, but making the control condition devoid of vitality forms using jerky movements. Participants performed two different tasks: Observation of actions performed gently or rudely and execution of the same actions. The results showed that in addition to the insula, the middle cingulate cortex (MCC) was strongly activated during both action observation and execution. Using a voxel-based analysis, voxels showing a similar trend of the blood-oxygen-level-dependent (BOLD) signal in both action observation and execution were found in the DCI and in the MCC. Finally, using a multifiber tractography analysis, we showed that the active sites in MCC and DCI are reciprocally connected.
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    Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Yersinia pestis causes human plague and colonizes both a mammalian host and a flea vector during its transmission cycle. A key barrier to bacterial infection is the host’s ability to actively sequester key biometals (e.g., iron, zinc, and manganese) required for bacterial growth. This is referred to as nutritional immunity. Mechanisms to overcome nutritional immunity are essential virulence factors for bacterial pathogens. Y. pestis produces an iron-scavenging siderophore called yersiniabactin (Ybt) that is required to overcome iron-mediated nutritional immunity and cause lethal infection. Recently, Ybt has been shown to bind to zinc, and in the absence of the zinc transporter ZnuABC, Ybt improves Y. pestis growth in zinc-limited medium. These data suggest that, in addition to iron acquisition, Ybt may also contribute to overcoming zinc-mediated nutritional immunity. To test this hypothesis, we used a mouse model defective in iron-mediated nutritional immunity to demonstrate that Ybt contributes to virulence in an iron-independent manner. Furthermore, using a combination of bacterial mutants and mice defective in zinc-mediated nutritional immunity, we identified calprotectin as the primary barrier for Y. pestis to acquire zinc during infection and that Y. pestis uses Ybt to compete with calprotectin for zinc. Finally, we discovered that Y. pestis encounters zinc limitation within the flea midgut, and Ybt contributes to overcoming this limitation. Together, these results demonstrate that Ybt is a bona fide zinc acquisition mechanism used by Y. pestis to surmount zinc limitation during the infection of both the mammalian and insect hosts.
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    Fevers and the social costs of acute infection in wild vervet monkeys (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Fevers are considered an adaptive response by the host to infection. For gregarious animals, however, fever and the associated sickness behaviors may signal a temporary loss of capacity, offering other group members competitive opportunities. We implanted wild vervet monkeys (Chlorocebus pygerythrus) with miniature data loggers to obtain continuous measurements of core body temperature. We detected 128 fevers in 43 monkeys, totaling 776 fever-days over a 6-year period. Fevers were characterized by a persistent elevation in mean and minimum 24-h body temperature of at least 0.5 °C. Corresponding behavioral data indicated that febrile monkeys spent more time resting and less time feeding, consistent with the known sickness behaviors of lethargy and anorexia, respectively. We found no evidence that fevers influenced the time individuals spent socializing with conspecifics, suggesting social transmission of infection within a group is likely. Notably, febrile monkeys were targeted with twice as much aggression from their conspecifics and were six times more likely to become injured compared to afebrile monkeys. Our results suggest that sickness behavior, together with its agonistic consequences, can carry meaningful costs for highly gregarious mammals. The degree to which social factors modulate the welfare of infected animals is an important aspect to consider when attempting to understand the ecological implications of disease.
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    Power spectra reveal distinct BOLD resting-state time courses in white matter (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Accurate characterization of the time courses of blood-oxygen-level–dependent (BOLD) signal changes is crucial for the analysis and interpretation of functional MRI data. While several studies have shown that white matter (WM) exhibits distinct BOLD responses evoked by tasks, there have been no comprehensive investigations into the time courses of spontaneous signal fluctuations in WM. We measured the power spectra of the resting-state time courses in a set of regions within WM identified as showing synchronous signals using independent components analysis. In each component, a clear separation between voxels into two categories was evident, based on their power spectra: one group exhibited a single peak, and the other had an additional peak at a higher frequency. Their groupings are location specific, and their distributions reflect unique neurovascular and anatomical configurations. Importantly, the two categories of voxels differed in their engagement in functional integration, revealed by differences in the number of interregional connections based on the two categories separately. Taken together, these findings suggest WM signals are heterogeneous in nature and depend on local structural-vascular-functional associations.
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    Accurate model of liquid–liquid phase behavior of intrinsically disordered proteins from optimization of single-chain properties (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Many intrinsically disordered proteins (IDPs) may undergo liquid–liquid phase separation (LLPS) and participate in the formation of membraneless organelles in the cell, thereby contributing to the regulation and compartmentalization of intracellular biochemical reactions. The phase behavior of IDPs is sequence dependent, and its investigation through molecular simulations requires protein models that combine computational efficiency with an accurate description of intramolecular and intermolecular interactions. We developed a general coarse-grained model of IDPs, with residue-level detail, based on an extensive set of experimental data on single-chain properties. Ensemble-averaged experimental observables are predicted from molecular simulations, and a data-driven parameter-learning procedure is used to identify the residue-specific model parameters that minimize the discrepancy between predictions and experiments. The model accurately reproduces the experimentally observed conformational propensities of a set of IDPs. Through two-body as well as large-scale molecular simulations, we show that the optimization of the intramolecular interactions results in improved predictions of protein self-association and LLPS.
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    Mammalian face as an evolutionary novelty (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: The anterior end of the mammalian face is characteristically composed of a semimotile nose, not the upper jaw as in other tetrapods. Thus, the therian nose is covered ventrolaterally by the “premaxilla,” and the osteocranium possesses only a single nasal aperture because of the absence of medial bony elements. This stands in contrast to those in other tetrapods in whom the premaxilla covers the rostral terminus of the snout, providing a key to understanding the evolution of the mammalian face. Here, we show that the premaxilla in therian mammals (placentals and marsupials) is not entirely homologous to those in other amniotes; the therian premaxilla is a composite of the septomaxilla and the palatine remnant of the premaxilla of nontherian amniotes (including monotremes). By comparing topographical relationships of craniofacial primordia and nerve supplies in various tetrapod embryos, we found that the therian premaxilla is predominantly of the maxillary prominence origin and associated with mandibular arch. The rostral-most part of the upper jaw in nonmammalian tetrapods corresponds to the motile nose in therian mammals. During development, experimental inhibition of primordial growth demonstrated that the entire mammalian upper jaw mostly originates from the maxillary prominence, unlike other amniotes. Consistently, cell lineage tracing in transgenic mice revealed a mammalian-specific rostral growth of the maxillary prominence. We conclude that the mammalian-specific face, the muzzle, is an evolutionary novelty obtained by overriding ancestral developmental constraints to establish a novel topographical framework in craniofacial mesenchyme.
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    Demonstration of the role of cell wall homeostasis in Staphylococcus aureus growth and the action of bactericidal antibiotics (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Bacterial cell wall peptidoglycan is essential, maintaining both cellular integrity and morphology, in the face of internal turgor pressure. Peptidoglycan synthesis is important, as it is targeted by cell wall antibiotics, including methicillin and vancomycin. Here, we have used the major human pathogen Staphylococcus aureus to elucidate both the cell wall dynamic processes essential for growth (life) and the bactericidal effects of cell wall antibiotics (death) based on the principle of coordinated peptidoglycan synthesis and hydrolysis. The death of S. aureus due to depletion of the essential, two-component and positive regulatory system for peptidoglycan hydrolase activity (WalKR) is prevented by addition of otherwise bactericidal cell wall antibiotics, resulting in stasis. In contrast, cell wall antibiotics kill via the activity of peptidoglycan hydrolases in the absence of concomitant synthesis. Both methicillin and vancomycin treatment lead to the appearance of perforating holes throughout the cell wall due to peptidoglycan hydrolases. Methicillin alone also results in plasmolysis and misshapen septa with the involvement of the major peptidoglycan hydrolase Atl, a process that is inhibited by vancomycin. The bactericidal effect of vancomycin involves the peptidoglycan hydrolase SagB. In the presence of cell wall antibiotics, the inhibition of peptidoglycan hydrolase activity using the inhibitor complestatin results in reduced killing, while, conversely, the deregulation of hydrolase activity via loss of wall teichoic acids increases the death rate. For S. aureus, the independent regulation of cell wall synthesis and hydrolysis can lead to cell growth, death, or stasis, with implications for the development of new control regimes for this important pathogen.
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    Configurational fingerprints of multicellular living systems (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Cells cooperate as groups to achieve structure and function at the tissue level, during which specific material characteristics emerge. Analogous to phase transitions in classical physics, transformations in the material characteristics of multicellular assemblies are essential for a variety of vital processes including morphogenesis, wound healing, and cancer. In this work, we develop configurational fingerprints of particulate and multicellular assemblies and extract volumetric and shear order parameters based on this fingerprint to quantify the system disorder. Theoretically, these two parameters form a complete and unique pair of signatures for the structural disorder of a multicellular system. The evolution of these two order parameters offers a robust and experimentally accessible way to map the phase transitions in expanding cell monolayers and during embryogenesis and invasion of epithelial spheroids.
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    Serum apolipoprotein A-I depletion is causative to silica nanoparticles–induced cardiovascular damage (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: The rapid development of nanotechnology has greatly benefited modern science and engineering and also led to an increased environmental exposure to nanoparticles (NPs). While recent research has established a correlation between the exposure of NPs and cardiovascular diseases, the intrinsic mechanisms of such a connection remain unclear. Inhaled NPs can penetrate the air–blood barrier from the lung to systemic circulation, thereby intruding the cardiovascular system and generating cardiotoxic effects. In this study, on-site cardiovascular damage was observed in mice upon respiratory exposure of silica nanoparticles (SiNPs), and the corresponding mechanism was investigated by focusing on the interaction of SiNPs and their encountered biomacromolecules en route. SiNPs were found to collect a significant amount of apolipoprotein A-I (Apo A-I) from the blood, in particular when the SiNPs were preadsorbed with pulmonary surfactants. While the adsorbed Apo A-I ameliorated the cytotoxic and proinflammatory effects of SiNPs, the protein was eliminated from the blood upon clearance of the NPs. However, supplementation of Apo A-I mimic peptide mitigated the atherosclerotic lesion induced by SiNPs. In addition, we found a further declined plasma Apo A-I level in clinical silicosis patients than coronary heart disease patients, suggesting clearance of SiNPs sequestered Apo A-I to compromise the coronal protein’s regular biological functions. Together, this study has provided evidence that the protein corona of SiNPs acquired in the blood depletes Apo A-I, a biomarker for prediction of cardiovascular diseases, which gives rise to unexpected toxic effects of the nanoparticles.
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    Phase separation in the outer membrane of Escherichia coli (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Gram-negative bacteria are surrounded by a protective outer membrane (OM) with phospholipids in its inner leaflet and lipopolysaccharides (LPS) in its outer leaflet. The OM is also populated with many β-barrel outer-membrane proteins (OMPs), some of which have been shown to cluster into supramolecular assemblies. However, it remains unknown how abundant OMPs are organized across the entire bacterial surface and how this relates to the lipids in the membrane. Here, we reveal how the OM is organized from molecular to cellular length scales, using atomic force microscopy to visualize the OM of live bacteria, including engineered Escherichia coli strains and complemented by specific labeling of abundant OMPs. We find that a predominant OMP in the E. coli OM, the porin OmpF, forms a near-static network across the surface, which is interspersed with barren patches of LPS that grow and merge with other patches during cell elongation. Embedded within the porin network is OmpA, which forms noncovalent interactions to the underlying cell wall. When the OM is destabilized by mislocalization of phospholipids to the outer leaflet, a new phase appears, correlating with bacterial sensitivity to harsh environments. We conclude that the OM is a mosaic of phase-separated LPS-rich and OMP-rich regions, the maintenance of which is essential to the integrity of the membrane and hence to the lifestyle of a gram-negative bacterium.
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    Live agent preference and social action monitoring in the macaque mid-superior temporal sulcus region (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Mentalizing, the ability to infer the mental states of others, is a cornerstone of adaptive social intelligence. While functional brain mapping of human mentalizing has progressed considerably, its evolutionary signature in nonhuman primates remains debated. The discovery that the middle part of the macaque superior temporal sulcus (mid-STS) region has a connectional fingerprint most similar to the human temporoparietal junction (TPJ)—a crucial node in the mentalizing network—raises the possibility that these cortical areas may also share basic functional properties associated with mentalizing. Here, we show that this is the case in aspects of a preference for live social interactions and in a theoretical framework of predictive coding. Macaque monkeys were trained to perform a turn-taking choice task with another real monkey partner sitting directly face-to-face or a filmed partner appearing in prerecorded videos. We found that about three-fourths of task-related mid-STS neurons exhibited agent-dependent activity, most responding selectively or preferentially to the partner’s action. At the population level, activities of these partner-type neurons were significantly greater under live-partner compared to video-recorded–partner task conditions. Furthermore, a subset of the partner-type neurons responded proactively when predictions about the partner’s action were violated. This prediction error coding was specific to the action domain; almost none of the neurons signaled error in the prediction of reward. The present findings highlight unique roles of the macaque mid-STS at the single-neuron level and further delineate its functional parallels with the human TPJ in social cognitive processes associated with mentalizing.
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    Kinetic proofreading of lipochitooligosaccharides determines signal activation of symbiotic plant receptors (2021)
    National Academy of Sciences
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    Publication Date: 2021-10-29
    Description: Plants and animals use cell surface receptors to sense and interpret environmental signals. In legume symbiosis with nitrogen-fixing bacteria, the specific recognition of bacterial lipochitooligosaccharide (LCO) signals by single-pass transmembrane receptor kinases determines compatibility. Here, we determine the structural basis for LCO perception from the crystal structures of two lysin motif receptor ectodomains and identify a hydrophobic patch in the binding site essential for LCO recognition and symbiotic function. We show that the receptor monitors the composition of the amphiphilic LCO molecules and uses kinetic proofreading to control receptor activation and signaling specificity. We demonstrate engineering of the LCO binding site to fine-tune ligand selectivity and correct binding kinetics required for activation of symbiotic signaling in plants. Finally, the hydrophobic patch is found to be a conserved structural signature in this class of LCO receptors across legumes that can be used for in silico predictions. Our results provide insights into the mechanism of cell-surface receptor activation by kinetic proofreading of ligands and highlight the potential in receptor engineering to capture benefits in plant–microbe interactions.
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