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  • Oxford University Press  (15)
  • National Academy of Sciences  (13)
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  • 2020  (32)
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  • 1
    Publication Date: 2022-01-07
    Description: Marine macroalgae, seaweeds, are exceptionally prolific producers of halogenated natural products. Biosynthesis of halogenated molecules in seaweeds is inextricably linked to reactive oxygen species (ROS) signaling as hydrogen peroxide serves as a substrate for haloperoxidase enzymes that participate in the construction these halogenated molecules. Here, using red macroalga Asparagopsis taxiformis, a prolific producer of the ozone depleting molecule bromoform, we provide the discovery and biochemical characterization of a ROS-producing NAD(P)H oxidase from seaweeds. This discovery was enabled by our sequencing of Asparagopsis genomes, in which we find the gene encoding the ROS-producing enzyme to be clustered with genes encoding bromoform-producing haloperoxidases. Biochemical reconstitution of haloperoxidase activities establishes that fatty acid biosynthesis can provide viable hydrocarbon substrates for bromoform production. The ROS production haloperoxidase enzymology that we describe here advances seaweed biology and biochemistry by providing the molecular basis for decades worth of physiological observations in ROS and halogenated natural product biosyntheses.
    Type: Article , PeerReviewed
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  • 2
    Publication Date: 2022-01-07
    Description: Fusarium oxysporum is a destructive root-infecting plant pathogen that causes significant yield losses in many economically important crop species. Hence, a deeper understanding of pathogen infection strategies is needed. With liquid chromatography-tandem mass spectrometry and gas chromatography-time of flight mass spectrometry platforms, we analyzed the metabolic changes in a time-course experiment with Arabidopsis accessions either resistant (Col-0) or susceptible (Ler-0) to isolates of Fusarium oxysporum forma specialis matthioli infection. We showed a concurrent effect of Fusarium-derived polyols and the mycotoxin beauvericin in the suppression of the immune response of susceptible hosts. A significant increase in oxidized glutathione in the resistant host was probably associated with effective reactive oxygen species-mediated resistance responses. Through a combination of targeted and untargeted metabolomics, we demonstrated the concurrent action of several Arabidopsis defense systems as well as the concurrent action of several virulence systems in the fungal attack of susceptible Arabidopsis.
    Type: Article , PeerReviewed
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  • 3
    Publication Date: 2022-01-07
    Description: Intense bottom-ice algal blooms, often dominated by diatoms, are an important source of food for grazers, organic matter for export during sea ice melt, and dissolved organic carbon. Sea-ice diatoms have a number of adaptations, including accumulation of compatible solutes, that allows them to inhabit this highly variable environment characterized by extremes in temperature, salinity, and light. In addition to protecting them from extreme conditions, these compounds present a labile, nutrient-rich source of organic matter, and include precursors to climate active compounds (e.g., dimethyl sulfide [DMS]), which are likely regulated with environmental change. Here, intracellular concentrations of 45 metabolites were quantified in three sea-ice diatom species and were compared to two temperate diatom species, with a focus on compatible solutes and free amino acid pools. There was a large diversity of metabolite concentrations between diatoms with no clear pattern identifiable for sea-ice species. Concentrations of some compatible solutes (isethionic acid, homarine) approached 1 M in the sea-ice diatoms, Fragilariopsis cylindrus and Navicula cf. perminuta, but not in the larger sea-ice diatom, Nitzschia lecointei or in the temperate diatom species. The differential use of compatible solutes in sea-ice diatoms suggests different adaptive strategies and highlights which small organic compounds may be important in polar biogeochemical cycles.
    Type: Article , PeerReviewed
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  • 4
    Publication Date: 2022-05-25
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Carroll, E. L., Ott, P. H., McMillan, L. F., Galletti Vernazzani, B., Neveceralova, P., Vermeulen, E., Gaggiotti, O. E., Andriolo, A., Baker, C. S., Bamford, C., Best, P., Cabrera, E., Calderan, S., Chirife, A., Fewster, R. M., Flores, P. A. C., Frasier, T., Freitas, T. R. O., Groch, K., Hulva, P., Kennedy, A., Leaper, R., Leslie, M. S., Moore, M., Oliveira, L., Seger, J., Stepien, E. N., Valenzuela, L. O., Zerbini, A., & Jackson, J. A. Genetic diversity and connectivity of southern right whales (Eubalaena australis) found in the Brazil and Chile-Peru wintering grounds and the South Georgia (Islas Georgias del Sur) feeding ground. Journal of Heredity, 111(3), (2020): 263-276, doi:10.1093/jhered/esaa010.
    Description: As species recover from exploitation, continued assessments of connectivity and population structure are warranted to provide information for conservation and management. This is particularly true in species with high dispersal capacity, such as migratory whales, where patterns of connectivity could change rapidly. Here we build on a previous long-term, large-scale collaboration on southern right whales (Eubalaena australis) to combine new (nnew) and published (npub) mitochondrial (mtDNA) and microsatellite genetic data from all major wintering grounds and, uniquely, the South Georgia (Islas Georgias del Sur: SG) feeding grounds. Specifically, we include data from Argentina (npub mtDNA/microsatellite = 208/46), Brazil (nnew mtDNA/microsatellite = 50/50), South Africa (nnew mtDNA/microsatellite = 66/77, npub mtDNA/microsatellite = 350/47), Chile–Peru (nnew mtDNA/microsatellite = 1/1), the Indo-Pacific (npub mtDNA/microsatellite = 769/126), and SG (npub mtDNA/microsatellite = 8/0, nnew mtDNA/microsatellite = 3/11) to investigate the position of previously unstudied habitats in the migratory network: Brazil, SG, and Chile–Peru. These new genetic data show connectivity between Brazil and Argentina, exemplified by weak genetic differentiation and the movement of 1 genetically identified individual between the South American grounds. The single sample from Chile–Peru had an mtDNA haplotype previously only observed in the Indo-Pacific and had a nuclear genotype that appeared admixed between the Indo-Pacific and South Atlantic, based on genetic clustering and assignment algorithms. The SG samples were clearly South Atlantic and were more similar to the South American than the South African wintering grounds. This study highlights how international collaborations are critical to provide context for emerging or recovering regions, like the SG feeding ground, as well as those that remain critically endangered, such as Chile–Peru.
    Description: This work was supported by the EU BEST 2.0 medium grant 1594 and UK DARWIN PLUS grant 057 and additional funding from the World Wildlife Fund GB107301. The collection of the Chile–Peru sample was supported by the Global Greengrants Fund and the Pacific Whale Foundation. The collection of the Brazilian samples was supported through grants by the Brazilian National Research Council to Paulo H. Ott (CNPq proc. n° 144064/98-7) and Paulo A.C. Flores (CNPq proc. n° 146609/1999-9) and with support from the World Wildlife Fund (WWF-Brazil). The collection of the South African samples was supported by the Global Greengrants Fund, the Pacific Whale Foundation and Charles University Grant Agency (1140217). E.L.C. was partially supported by a Rutherford Discovery Fellowship from the Royal Society of New Zealand. This study forms part of the Ecosystems component of the British Antarctic Survey Polar Sciences for Planet Earth Programme, funded by the Natural Environment Research Council.
    Keywords: population structure ; connectivity ; migration ; gene flow
    Repository Name: Woods Hole Open Access Server
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  • 5
    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 Johnson, W. M., Alexander, H., Bier, R. L., Miller, D. R., Muscarella, M. E., Pitz, K. J., & Smith, H. Auxotrophic interactions: A stabilizing attribute of aquatic microbial communities? FEMS Microbiology Ecology, (2020): fiaa115, doi: 10.1093/femsec/fiaa115.
    Description: Auxotrophy, or an organism's requirement for an exogenous source of an organic molecule, is widespread throughout species and ecosystems. Auxotrophy can result in obligate interactions between organisms, influencing ecosystem structure and community composition. We explore how auxotrophy-induced interactions between aquatic microorganisms affect microbial community structure and stability. While some studies have documented auxotrophy in aquatic microorganisms, these studies are not widespread, and we therefore do not know the full extent of auxotrophic interactions in aquatic environments. Current theoretical and experimental work suggests that auxotrophy links microbial community members through a complex web of metabolic dependencies. We discuss the proposed ways in which auxotrophy may enhance or undermine the stability of aquatic microbial communities, highlighting areas where our limited understanding of these interactions prevents us from being able to predict the ecological implications of auxotrophy. Finally, we examine an example of auxotrophy in harmful algal blooms to place this often theoretical discussion in a field context where auxotrophy may have implications for the development and robustness of algal bloom communities. We seek to draw attention to the relationship between auxotrophy and community stability in an effort to encourage further field and theoretical work that explores the underlying principles of microbial interactions.
    Description: This work was supported by the National Science Foundation [OCE-1356192].
    Keywords: Auxotrophy ; Microbial community stability ; Microbial interactions ; Aquatic
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  • 6
    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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  • 7
    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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  • 8
    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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  • 9
    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 Wang, P., Huang, C., Lin, J., Jian, Z., Sun, Z., & Zhao, M. The South China Sea is not a mini-Atlantic: plate-edge rifting vs intra-plate rifting. National Science Review, 6(5), (2019): 902-913, doi:10.1093/nsr/nwz135.
    Description: The South China Sea, as ‘a non-volcanic passive margin basin’ in the Pacific, has often been considered as a small-scale analogue of the Atlantic. The recent ocean drilling in the northern South China Sea margin found, however, that the Iberian model of non-volcanic rifted margin from the Atlantic does not apply to the South China Sea. In this paper, we review a variety of rifted basins and propose to discriminate two types of rifting basins: plate-edge type such as the South China Sea and intra-plate type like the Atlantic. They not only differ from each other in structure, formation process, lifespan and geographic size, but also occur at different stages of the Wilson cycle. The intra-plate rifting occurred in the Mesozoic and gave rise to large oceans, whereas the plate-edge rifting took place mainly in the mid-Cenozoic, with three-quarters of the basins concentrated in the Western Pacific. As a member of the Western Pacific system of marginal seas, the South China Sea should be studied not in isolation on its origin and evolution, but in a systematic context to include also its neighboring counterparts.
    Description: This work was supported by the National Natural Science Foundation of China as a part of the ‘South China Sea Deep’ Project (91128000).
    Keywords: Rifting ; Marginal basin ; Passive margin ; South China Sea ; Western Pacific ; Subduction
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  • 10
    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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  • 11
    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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  • 12
    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 Lasek-Nesselquist, E., & Johnson, M. D. A phylogenomic approach to clarifying the relationship of Mesodinium within the Ciliophora: a case study in the complexity of mixed-species transcriptome analyses. Genome Biology and Evolution, 11(11), (2019): 3218–3232, doi:10.1093/gbe/evz233.
    Description: Recent high-throughput sequencing endeavors have yielded multigene/protein phylogenies that confidently resolve several inter- and intra-class relationships within the phylum Ciliophora. We leverage the massive sequencing efforts from the Marine Microbial Eukaryote Transcriptome Sequencing Project, other SRA submissions, and available genome data with our own sequencing efforts to determine the phylogenetic position of Mesodinium and to generate the most taxonomically rich phylogenomic ciliate tree to date. Regardless of the data mining strategy, the multiprotein data set, or the molecular models of evolution employed, we consistently recovered the same well-supported relationships among ciliate classes, confirming many of the higher-level relationships previously identified. Mesodinium always formed a monophyletic group with members of the Litostomatea, with mixotrophic species of Mesodinium—M. rubrum, M. major, and M. chamaeleon—being more closely related to each other than to the heterotrophic member, M. pulex. The well-supported position of Mesodinium as sister to other litostomes contrasts with previous molecular analyses including those from phylogenomic studies that exploited the same transcriptomic databases. These topological discrepancies illustrate the need for caution when mining mixed-species transcriptomes and indicate that identifying ciliate sequences among prey contamination—particularly for Mesodinium species where expression from stolen prey nuclei appears to dominate—requires thorough and iterative vetting with phylogenies that incorporate sequences from a large outgroup of prey.
    Description: We thank David Beaudoin and Holly V. Moeller for their assistance in collecting cells and extracting RNA. We thank the Josephine Bay Paul Center for Comparative Molecular Biology and Evolution at the Marine Biological Laboratory for the generous use of their servers. This work was supported in part by a National Science Foundation grant to both authors (IOS 1354773).
    Keywords: Mesodinium ; Litostomatea ; ciliate phylogenomics ; mixed-species transcriptomes ; sequence contamination
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  • 13
    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 Xu, X., Li, G., Li, C., Zhang, J., Wang, Q., Simmons, D. K., Chen, X., Wijesena, N., Zhu, W., Wang, Z., Wang, Z., Ju, B., Ci, W., Lu, X., Yu, D., Wang, Q., Aluru, N., Oliveri, P., Zhang, Y. E., Martindale, M. Q., & Liu, J. Evolutionary transition between invertebrates and vertebrates via methylation reprogramming in embryogenesis. National Science Review, 6(5), (2019):993-1003, doi:10.1093/nsr/nwz064.
    Description: Major evolutionary transitions are enigmas, and the most notable enigma is between invertebrates and vertebrates, with numerous spectacular innovations. To search for the molecular connections involved, we asked whether global epigenetic changes may offer a clue by surveying the inheritance and reprogramming of parental DNA methylation across metazoans. We focused on gametes and early embryos, where the methylomes are known to evolve divergently between fish and mammals. Here, we find that methylome reprogramming during embryogenesis occurs neither in pre-bilaterians such as cnidarians nor in protostomes such as insects, but clearly presents in deuterostomes such as echinoderms and invertebrate chordates, and then becomes more evident in vertebrates. Functional association analysis suggests that DNA methylation reprogramming is associated with development, reproduction and adaptive immunity for vertebrates, but not for invertebrates. Interestingly, the single HOX cluster of invertebrates maintains unmethylated status in all stages examined. In contrast, the multiple HOX clusters show dramatic dynamics of DNA methylation during vertebrate embryogenesis. Notably, the methylation dynamics of HOX clusters are associated with their spatiotemporal expression in mammals. Our study reveals that DNA methylation reprogramming has evolved dramatically during animal evolution, especially after the evolutionary transitions from invertebrates to vertebrates, and then to mammals.
    Description: This work was supported by the National Key Research and Development Program of China (2018YFC1003303), the Strategic Priority Research Program of the CAS (XDB13040200), the National Natural Science Foundation of China (91519306, 31425015), the Youth Innovation Promotion Association of the CAS and the Key Research Program of Frontier Sciences, CAS (QYZDY-SSW-SMC016).
    Keywords: DNA methylation ; evolution ; development ; reprogramming
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  • 14
    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 Vallecillo-Viejo, I. C., Liscovitch-Brauer, N., Diaz Quiroz, J. F., Montiel-Gonzalez, Maria F., Nemes, Sonya E., Rangan, K. J., Levinson, S. R., Eisenberg, E., & Rosenthal, J. J. C. Spatially regulated editing of genetic information within a neuron. Nucleic Acids Research, (2020): gkaa172, doi: 10.1093/nar/gkaa172.
    Description: In eukaryotic cells, with the exception of the specialized genomes of mitochondria and plastids, all genetic information is sequestered within the nucleus. This arrangement imposes constraints on how the information can be tailored for different cellular regions, particularly in cells with complex morphologies like neurons. Although messenger RNAs (mRNAs), and the proteins that they encode, can be differentially sorted between cellular regions, the information itself does not change. RNA editing by adenosine deamination can alter the genome’s blueprint by recoding mRNAs; however, this process too is thought to be restricted to the nucleus. In this work, we show that ADAR2 (adenosine deaminase that acts on RNA), an RNA editing enzyme, is expressed outside of the nucleus in squid neurons. Furthermore, purified axoplasm exhibits adenosine-to-inosine activity and can specifically edit adenosines in a known substrate. Finally, a transcriptome-wide analysis of RNA editing reveals that tens of thousands of editing sites (〉70% of all sites) are edited more extensively in the squid giant axon than in its cell bodies. These results indicate that within a neuron RNA editing can recode genetic information in a region-specific manner.
    Description: National Science Foundation (NSF) [IOS1557748 to J.R.]; United States–Israel Binational Science Foundation [BSF2013094 to J.R. and E.E.]; The Grass Foundation grant in support of the Doryteuthis pealeii Genome Project, and a gift by Mr. Edward Owens. Funding for open access charge: United States–Israel Binational Science Foundation [BSF2013094].
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  • 15
    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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  • 16
    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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  • 17
    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 da Fonseca, R. R., Couto, A., Machado, A. M., Brejova, B., Albertin, C. B., Silva, F., Gardner, P., Baril, T., Hayward, A., Campos, A., Ribeiro, A. M., Barrio-Hernandez, I., Hoving, H. J., Tafur-Jimenez, R., Chu, C., Frazao, B., Petersen, B., Penaloza, F., Musacchia, F., Alexander, G. C., Osorio, H., Winkelmann, I., Simakov, O., Rasmussen, S., Rahman, M. Z., Pisani, D., Vinther, J., Jarvis, E., Zhang, G., Strugnell, J. M., Castro, L. F. C., Fedrigo, O., Patricio, M., Li, Q., Rocha, S., Antunes, A., Wu, Y., Ma, B., Sanges, R., Vinar, T., Blagoev, B., Sicheritz-Ponten, T., Nielsen, R., & Gilbert, M. T. P. A draft genome sequence of the elusive giant squid, Architeuthis dux. Gigascience, 9(1), (2020): giz152. doi: 10.1093/gigascience/giz152.
    Description: Background: The giant squid (Architeuthis dux; Steenstrup, 1857) is an enigmatic giant mollusc with a circumglobal distribution in the deep ocean, except in the high Arctic and Antarctic waters. The elusiveness of the species makes it difficult to study. Thus, having a genome assembled for this deep-sea–dwelling species will allow several pending evolutionary questions to be unlocked. Findings: We present a draft genome assembly that includes 200 Gb of Illumina reads, 4 Gb of Moleculo synthetic long reads, and 108 Gb of Chicago libraries, with a final size matching the estimated genome size of 2.7 Gb, and a scaffold N50 of 4.8 Mb. We also present an alternative assembly including 27 Gb raw reads generated using the Pacific Biosciences platform. In addition, we sequenced the proteome of the same individual and RNA from 3 different tissue types from 3 other species of squid (Onychoteuthis banksii, Dosidicus gigas, and Sthenoteuthis oualaniensis) to assist genome annotation. We annotated 33,406 protein-coding genes supported by evidence, and the genome completeness estimated by BUSCO reached 92%. Repetitive regions cover 49.17% of the genome. Conclusions: This annotated draft genome of A. dux provides a critical resource to investigate the unique traits of this species, including its gigantism and key adaptations to deep-sea environments.
    Description: R.R.F. thanks the Villum Fonden for grant VKR023446 (Villum Fonden Young Investigator Grant), the Portuguese Science Foundation (FCT) for grant PTDC/MAR/115347/2009; COMPETE-FCOMP-01-012; FEDER-015453, Marie Curie Actions (FP7-PEOPLE-2010-IEF, Proposal 272927), and the Danish National Research Foundation (DNRF96) for its funding of the Center for Macroecology, Evolution, and Climate. H.O. thanks the Rede Nacional de Espectrometria de Massa, ROTEIRO/0028/2013, ref. LISBOA-01-0145-FEDER-022125, supported by COMPETE and North Portugal Regional Operational Programme (Norte2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF). A.C. thanks FCT for project UID/Multi/04423/2019. M.P. acknowledges the support from the Wellcome Trust (grant number WT108749/Z/15/Z) and the European Molecular Biology Laboratory. M.P.T.G. thanks the Danish National Research Foundation for its funding of the Center for GeoGenetics (grant DNRF94) and Lundbeck Foundation for grant R52–5062 on Pathogen Palaeogenomics. S.R. was supported by the Novo Nordisk Foundation grant NNF14CC0001. A.H. is supported by a Biotechnology and Biological Sciences Research Council David Phillips Fellowship (fellowship reference: BB/N020146/1). T.B. is supported by the Biotechnology and Biological Sciences Research Council-funded South West Biosciences Doctoral Training Partnership (training grant reference BB/M009122/1). This work was partially funded by the Lundbeck Foundation (R52-A4895 to B.B.). H.J.T.H. was supported by the David and Lucile Packard Foundation, the Netherlands Organization for Scientific Research (#825.09.016), and currently by the Deutsche Forschungsgemeinschaft (DFG) under grant HO 5569/2-1 (Emmy Noether Junior Research Group). T.V. and B. Brejova were supported by grants from the Slovak grant agency VEGA (1/0684/16, 1/0458/18). F.S. was supported by a PhD grant (SFRH/BD/126560/2016) from FCT. A.A. was partly supported by the FCT project PTDC/CTA-AMB/31774/2017. C.C. and Y.W. are partly supported by grant IIS-1526415 from the US National Science Foundation. Computation for the work described in this article was partially supported by the DeiC National Life Science Supercomputer at DTU.
    Keywords: Cephalopod ; Invertebrate ; Genome assembly
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  • 18
    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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  • 19
    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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  • 20
    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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  • 21
    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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  • 22
    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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  • 23
    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 McLean, C., & Kujawinski, E. B. AutoTuner: high fidelity and robust parameter selection for metabolomics data processing. Analytical Chemistry, 92(8), (2020): 5724-5732, doi:10.1021/acs.analchem.9b04804.
    Description: Untargeted metabolomics experiments provide a snapshot of cellular metabolism but remain challenging to interpret due to the computational complexity involved in data processing and analysis. Prior to any interpretation, raw data must be processed to remove noise and to align mass-spectral peaks across samples. This step requires selection of dataset-specific parameters, as erroneous parameters can result in noise inflation. While several algorithms exist to automate parameter selection, each depends on gradient descent optimization functions. In contrast, our new parameter optimization algorithm, AutoTuner, obtains parameter estimates from raw data in a single step as opposed to many iterations. Here, we tested the accuracy and the run-time of AutoTuner in comparison to isotopologue parameter optimization (IPO), the most commonly used parameter selection tool, and compared the resulting parameters’ influence on the properties of feature tables after processing. We performed a Monte Carlo experiment to test the robustness of AutoTuner parameter selection and found that AutoTuner generated similar parameter estimates from random subsets of samples. We conclude that AutoTuner is a desirable alternative to existing tools, because it is scalable, highly robust, and very fast (∼100–1000× speed improvement from other algorithms going from days to minutes). AutoTuner is freely available as an R package through BioConductor.
    Description: We thank Titus Brown and Ben Temperton for advice on the algorithm validation, Arthur Eschenlauer for constructive feedback on the software design, Krista Longnecker for continuous support and discussions, Gabriel Leventhal for mathematics advice, the users of AutoTuner for debugging help through Github, and David Angeles-Albores and two anonymous reviewers for critical feedback on the manuscript. Funding support included the National GEM Consortium and NSF graduate research program fellowships (C.M.) and grants from the MIT Microbiome Center (Award 6936800, E.B.K.) and the Simons Foundation (Award ID #509034, E.B.K.).
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  • 24
    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 Beckman, N. G., Asian, C. E., Rogers, H. S., Kogan, O., Bronstein, J. L., Bullock, J. M., Hartig, F., HilleRisLambers, J., Zhou, Y., Zurell, D., Brodie, J. F., Bruna, E. M., Cantrell, R. S., Decker, R. R., Efiom, E., Fricke, E. C., Gurski, K., Hastings, A., Johnson, J. S., Loiselle, B. A., Miriti, M. N., Neubert, M. G., Pejchar, L., Poulsen, J. R., Pufal, G., Razafindratsima, O. H., Sandor, M. E., Shea, K., Schreiber, S., Schupp, E. W., Snell, R. S., Strickland, C., & Zambrano, J. Advancing an interdisciplinary framework to study seed dispersal ecology. Aob Plants, 12(2), (2020): plz048, doi:10.1093/aobpla/plz048.
    Description: Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant’s life history and environmental variability that ultimately influences a population’s ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.
    Description: Ideas for this manuscript initiated during the Seed Dispersal Workshop held in May 2016 at the Socio-Environmental Synthesis Center in Annapolis, MD and supported by the US National Science Foundation Grant DEB-1548194 to N.G.B. and the National Socio-Environmental Synthesis Center under the US National Science Foundation Grant DBI-1052875. D.Z. received funding from the Swiss National Science Foundation (SNF, grant: PZ00P3_168136/1) and from the German Science Foundation (DFG, grant: ZU 361/1-1).
    Keywords: Analytical models ; demography ; global change ; individual-based models ; long-distance seed dispersal ; population models ; seed dispersal
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  • 25
    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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  • 26
    Publication Date: 2022-05-26
    Description: Author Posting. © American Chemical Society, 2020. This is an open access article published under an ACS AuthorChoice License. The definitive version was published in Chemical Research in Toxicology, 33(4), (2020): 860-879, doi:10.1021/acs.chemrestox.9b00476.
    Description: The Ah receptor (AHR) has been studied for almost five decades. Yet, we still have many important questions about its role in normal physiology and development. Moreover, we still do not fully understand how this protein mediates the adverse effects of a variety of environmental pollutants, such as the polycyclic aromatic hydrocarbons (PAHs), the chlorinated dibenzo-p-dioxins (“dioxins”), and many polyhalogenated biphenyls. To provide a platform for future research, we provide the historical underpinnings of our current state of knowledge about AHR signal transduction, identify a few areas of needed research, and then develop concepts such as adaptive metabolism, ligand structural diversity, and the importance of proligands in receptor activation. We finish with a discussion of the cognate physiological role of the AHR, our perspective on why this receptor is so highly conserved, and how we might think about its cognate ligands in the future.
    Description: This review is dedicated in memory of the career of Alan Poland, one of the truly great minds in pharmacology and toxicology. This work was supported by the National Institutes of Health Grants R35-ES028377, T32-ES007015, P30-CA014520, P42-ES007381, and U01-ES1026127, The UW SciMed GRS Program, and The Morgridge Foundation. The authors would like to thank Catherine Stanley of UW Media Solutions for her artwork.
    Repository Name: Woods Hole Open Access Server
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  • 27
    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2020. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Toxicological Sciences (2020): kfaa158, doi:10.1093/toxsci/kfaa158.
    Description: Chemical modifications of proteins, DNA, and RNA moieties play critical roles in regulating gene expression. Emerging evidence suggests the RNA modifications (epitranscriptomics) have substantive roles in basic biological processes. One of the most common modifications in mRNA and noncoding RNAs is N6-methyladenosine (m6A). In a subset of mRNAs, m6A sites are preferentially enriched near stop codons, in 3′ UTRs, and within exons, suggesting an important role in the regulation of mRNA processing and function including alternative splicing and gene expression. Very little is known about the effect of environmental chemical exposure on m6A modifications. As many of the commonly occurring environmental contaminants alter gene expression profiles and have detrimental effects on physiological processes, it is important to understand the effects of exposure on this important layer of gene regulation. Hence, the objective of this study was to characterize the acute effects of developmental exposure to PCB126, an environmentally relevant dioxin-like PCB, on m6A methylation patterns. We exposed zebrafish embryos to PCB126 for 6 h starting from 72 h post fertilization and profiled m6A RNA using methylated RNA immunoprecipitation followed by sequencing (MeRIP-seq). Our analysis revealed 117 and 217 m6A peaks in the DMSO and PCB126 samples (false discovery rate 5%), respectively. The majority of the peaks were preferentially located around the 3′ UTR and stop codons. Statistical analysis revealed 15 m6A marked transcripts to be differentially methylated by PCB126 exposure. These include transcripts that are known to be activated by AHR agonists (eg, ahrra, tiparp, nfe2l2b) as well as others that are important for normal development (vgf, cebpd, sned1). These results suggest that environmental chemicals such as dioxin-like PCBs could affect developmental gene expression patterns by altering m6A levels. Further studies are necessary to understand the functional consequences of exposure-associated alterations in m6A levels.
    Description: National Institute of Health National Institute of Environmental Health Sciences Outstanding New Environmental Scientist (NIH R01ES024915 to N.A.); Woods Hole Center for Oceans and Human Health [National Institutes of Health (NIH) (Grant P01ES028938); National Science Foundation (Grant OCE-1840381) to M. E. Hahn, J. J. Stegeman, N.A., and S.K.].
    Description: 2021-10-16
    Keywords: dioxin-like PCBs ; development ; zebrafish ; epitranscriptomics ; m6A ; MeRIP
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  • 28
    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 Lamb, D. C., Hargrove, T. Y., Zhao, B., Wawrzak, Z., Goldstone, J. V., Nes, W. D., Kelly, S. L., Waterman, M. R., Stegeman, J. J., & Lepesheva, G. I. Concerning P450 evolution: structural analyses support bacterial origin of sterol 14α-demethylases. Molecular Biology and Evolution, (2020): msaa260, doi:10.1093/molbev/msaa260.
    Description: Sterol biosynthesis, primarily associated with eukaryotic kingdoms of life, occurs as an abbreviated pathway in the bacterium Methylococcus capsulatus. Sterol 14α-demethylation is an essential step in this pathway and is catalyzed by cytochrome P450 51 (CYP51). In M. capsulatus, the enzyme consists of the P450 domain naturally fused to a ferredoxin domain at the C-terminus (CYP51fx). The structure of M. capsulatus CYP51fx was solved to 2.7 Å resolution and is the first structure of a bacterial sterol biosynthetic enzyme. The structure contained one P450 molecule per asymmetric unit with no electron density seen for ferredoxin. We connect this with the requirement of P450 substrate binding in order to activate productive ferredoxin binding. Further, the structure of the P450 domain with bound detergent (which replaced the substrate upon crystallization) was solved to 2.4 Å resolution. Comparison of these two structures to the CYP51s from human, fungi, and protozoa reveals strict conservation of the overall protein architecture. However, the structure of an “orphan” P450 from nonsterol-producing Mycobacterium tuberculosis that also has CYP51 activity reveals marked differences, suggesting that loss of function in vivo might have led to alterations in the structural constraints. Our results are consistent with the idea that eukaryotic and bacterial CYP51s evolved from a common cenancestor and that early eukaryotes may have recruited CYP51 from a bacterial source. The idea is supported by bioinformatic analysis, revealing the presence of CYP51 genes in 〉1,000 bacteria from nine different phyla, 〉50 of them being natural CYP51fx fusion proteins.
    Description: The study was supported by National Institutes of Health (Grant No. R01 GM067871 to G.I.L.) and by a UK-USA Fulbright Scholarship and the Royal Society (to D.C.L.).
    Keywords: sterol biosynthesis ; evolution ; cytochrome P450 ; CYP51 redox partner ; crystallography
    Repository Name: Woods Hole Open Access Server
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  • 29
    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 Zemeckis, D. R., Dean, M. J., DeAngelis, A. I., Van Parijs, S. M., Hoffman, W. S., Baumgartner, M. F., Hatch, L. T., Cadrin, S. X., & McGuire, C. H. Identifying the distribution of Atlantic cod spawning using multiple fixed and glider-mounted acoustic technologies. ICES Journal of Marine Science, 76(6), (2019): 1610-1625, doi: 10.1093/icesjms/fsz064.
    Description: Effective fishery management measures to protect fish spawning aggregations require reliable information on the spatio-temporal distribution of spawning. Spawning closures have been part of a suite of fishery management actions to rebuild the Gulf of Maine stock of Atlantic cod (Gadus morhua), but difficulties remain with managing rebuilding. The objective of this study was to identify the spatial and temporal distribution of cod spawning during winter in Massachusetts Bay to improve our understanding of cod spawning dynamics and inform fisheries management. Spawning was investigated in collaboration with commercial fishermen during three winter spawning seasons (October 2013–March 2016) using acoustic telemetry and passive acoustic monitoring equipment deployed in fixed-station arrays and mounted on mobile autonomous gliders. Tagged cod exhibited spawning site fidelity and spawning primarily occurred from early November through January with a mid-December peak and some inter-annual variability. The spatial distribution of spawning was generally consistent among years with multiple hotspots in areas 〉50 m depth. Current closures encompass most of spawning, but important areas are recommended for potential modifications. Utilizing multiple complementary technologies and deployment strategies in collaboration with commercial fishermen enabled a comprehensive description of spawning and provides a valuable model for future studies.
    Description: Year 1 was jointly funded by The Nature Conservancy and Massachusetts Division of Marine Fisheries. The remainder of this research was funded through the 2013–2014 NOAA Saltonstall Kennedy grant program (Award No. NA14NMF4270027) with additional support from the Nature Conservancy and Cabot Family Charitable Foundation.
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  • 30
    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 Dong, E., Zhang, Y., Song, Z., Zhang, T., Cai, C., & Fang, N. X. Physical modeling and validation of porpoises' directional emission via hybrid metamaterials. National Science Review, 6(5), (2019): 921-928, doi:10.1093/nsr/nwz085.
    Description: In wave physics and engineering, directional emission sets a fundamental limitation on conventional simple sources as their sizes should be sufficiently larger than their wavelength. Artificial metamaterial and animal biosonar both show potential in overcoming this limitation. Existing metamaterials arranged in periodic microstructures face great challenges in realizing complex and multiphase biosonar structures. Here, we proposed a physical directional emission model to bridge the gap between porpoises’ biosonar and artificial metamaterial. Inspired by the anatomical and physical properties of the porpoise's biosonar transmission system, we fabricated a hybrid metamaterial system composed of multiple composite structures. We validated that the hybrid metamaterial significantly increased directivity and main lobe energy over a broad bandwidth both numerically and experimentally. The device displayed efficiency in detecting underwater target and suppressing false target jamming. The metamaterial-based physical model may be helpful to achieve the physical mechanisms of porpoise biosonar detection and has diverse applications in underwater acoustic sensing, ultrasound scanning, and medical ultrasonography.
    Description: E.D., Y.Z., Z.S., T.Z. and C.C. acknowledge the financial support in part by the National Key Research and Development Program of China (2018YFC1407504), the National Natural Science Foundation of China (41676023, 41276040 and 41422604). N.X.F. acknowledges the support from the MIT Energy Initiative grant. Z.S. thanks the China Scholarship Council for the financial support of his oversea study in Woods Hole Oceanographic Institution.
    Keywords: porpoise's physical model ; metamaterials ; biosonar ; directional emission
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  • 31
    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 Lin, J., Xu, Y., Sun, Z., & Zhou, Z. Mantle upwelling beneath the South China Sea and links to surrounding subduction systems. National Science Review, 6(5), (2019): 877-881, doi:10.1093/nsr/nwz123.
    Description: The evolution of the South China Sea (SCS) is directly linked to the complex subduction systems of the surrounding Pacific, Philippine Sea and Indo-Australian Plates (Fig. 1a). Major advances in the last several years are providing new insights into the SCS-mantle dynamics, through regional seismic imaging of the upper mantle [1,2], unprecedented IODP drilling expeditions (349/367/368/368X) [3–5] that obtained the oceanic basement basalt samples for the first time, geochemical analyses of the SCS-mantle source compositions [6–8] and geodynamic modeling [9,10]. Furthermore, new geological mapping, seismic imaging [11,12] and IODP drilling [13,14] have revealed evidence for significantly greater magma production at the northern SCS rifted margin, in comparison to the magma-poor end-member of the Atlantic rifted margins. This paper provides a new perspective of the SCS-mantle dynamics inspired by new observations and geodynamic modeling. We first highlight new geophysical evidence for a broad region of low-seismic-velocity anomalies in the upper mantle beneath the northern SCS, abundant magmatism during continental breakup and post-seafloor spreading, and geochemical evidence for recycled oceanic components beneath the SCS. We then present new models of layered flows in the mantle beneath the SCS, revealing two modes of plate- and subduction-driven mantle upwelling, including (i) narrow centers of mantle upwelling at shallow depths induced by divergent plate motion at seafloor-spreading centers and (ii) broad zones of mantle upwelling as a result of subduction-induced mantle-return flows at greater depths. These new observations and geodynamic studies suggest strong links between mantle upwelling beneath the SCS and surrounding subducting plates.
    Description: This work was supported by the National Natural Science Foundation of China (41890813, 91628301, U1606401, 41976066, 91858207 and 41706056), the Chinese Academy of Sciences (Y4SL021001, QYZDY-SSW-DQC005 and 133244KYSB20180029), the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou, GML2019ZD0205), the National Key R&D Program of China (2018YFC0309800 and 2018YFC0310100), the State Oceanic Administration (GASI-GEOGE-02) and China Ocean Mineral Resources R&D Association (DY135-S2–1-04).
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  • 32
    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 Sun, Z., Lin, J., Qiu, N., Jian, Z., Wang, P., Pang, X., Zheng, J., & Zhu, B. The role of magmatism in the thinning and breakup of the South China Sea continental margin: Special Topic: the South China Sea Ocean Drilling. National Science Review, 6(5), (2019): 871-876, doi:10.1093/nsr/nwz116.
    Description: Magmatism plays a key role in the process of continental margin breakup and ocean formation. Even in the extremely magma-poor Iberia and Newfoundland margin, studies of field outcrops have shown that syn-rift magmatism had participated in rifting from a very early stage and contributed directly to the rifting process. The final transition from exhumed continental mantle to the ocean formation is also triggered by the accumulation and eruption of magma [1]. Therefore, Atlantic-type passive continental margins are classified into two end-members: magma-poor (non-volcanic) and magma-rich (volcanic). The differences between them lie in whether a large amount of intrusive and extrusive magmatism from the mantle plume/hotspot is involved in the syn-rift and breakup stages. A magma-rich margin [2] should include the following characteristics: (i) a high-velocity lower crust (HVLC) caused by syn-rift mafic magma underplating; (ii) continental crust intruded by abundant sills and dikes; (iii) a large volume of seaward-dipping reflectors (SDRs) caused by flood basalt eruption or tuffs. All other margins are classified as magma-poor margins.
    Description: We thank the research team project of Guangdong Natural Science Foundation (2017A030312002), IODP-China and South China Sea Deep Project (91628301) and K.C. Wong Education Foundation (GJTD-2018-13) for providing support for the research. This research was also supported by the China National Science and Technology Major Project (2016ZX05026–003), the joint foundation of the National Natural Science Foundation of China and Guangdong province (U1301233), as well as the National Natural Science Foundation of China (41576070 and 41890813).
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