ALBERT

Description: Among eukaryotes, four major phytoplankton lineages are responsible for marine photosynthesis; prymnesiophytes, alveolates, stramenopiles, and prasinophytes. Contributions by individual taxa, however, are not well known, and genomes have been analyzed fromonly the latter two lineages. Tiny "picoplanktonic" members of the prymnesiophyte lineage have long been inferred to be ecologically important but remain poorly characterized. Here, we examine pico-prymnesiophyte evolutionary history and ecology using cultivation-independent methods. 18S rRNA gene analysis showed picoprymnesiophytes belonged to broadly distributed uncultivated taxa. Therefore, we used targeted metagenomics to analyze uncultured pico-prymnesiophytes sorted by flow cytometry from subtropical North Atlantic waters. The data reveal a composite nuclear-encoded gene repertoire with strong green-lineage affiliations, which contrasts with the evolutionary history indicated by the plastid genome. Measured pico-prymnesiophyte growth rates were rapid in this region, resulting in primary production contributions similar to the cyanobacterium Prochlorococcus. On average, pico-prymnesiophytes formed 25 of global picophytoplankton biomass, with differing contributions in five biogeographical provinces spanning tropical to subpolar systems. Elements likely contributing to success include high gene density and genes potentially involved in defense and nutrient uptake. Our findings have implications reaching beyond pico-prymnesiophytes, to the prasinophytes and stramenopiles. For example, prevalence of putative Ni-containing superoxide dismutases (SODs), instead of Fe-containing SODs, seems to be a common adaptation among eukaryotic phytoplankton for reducing Fe quotas in low-Fe modern oceans. Moreover, highly mosaic gene repertoires, although compositionally distinct for each major eukaryotic lineage, now seem to be an underlying facet of successful marine phytoplankton.

Description: Significance: Cold and dry glacial-state climate conditions persisted in the Southern Hemisphere until approximately 17.7 ka, when paleoclimate records show a largely unexplained sharp, nearly synchronous acceleration in deglaciation. Detailed measurements in Antarctic ice cores document exactly at that time a unique, ∼192-y series of massive halogen-rich volcanic eruptions geochemically attributed to Mount Takahe in West Antarctica. Rather than a coincidence, we postulate that halogen-catalyzed stratospheric ozone depletion over Antarctica triggered large-scale atmospheric circulation and hydroclimate changes similar to the modern Antarctic ozone hole, explaining the synchronicity and abruptness of accelerated Southern Hemisphere deglaciation. Abstract: Glacial-state greenhouse gas concentrations and Southern Hemisphere climate conditions persisted until ∼17.7 ka, when a nearly synchronous acceleration in deglaciation was recorded in paleoclimate proxies in large parts of the Southern Hemisphere, with many changes ascribed to a sudden poleward shift in the Southern Hemisphere westerlies and subsequent climate impacts. We used high-resolution chemical measurements in the West Antarctic Ice Sheet Divide, Byrd, and other ice cores to document a unique, ∼192-y series of halogen-rich volcanic eruptions exactly at the start of accelerated deglaciation, with tephra identifying the nearby Mount Takahe volcano as the source. Extensive fallout from these massive eruptions has been found 〉2,800 km from Mount Takahe. Sulfur isotope anomalies and marked decreases in ice core bromine consistent with increased surface UV radiation indicate that the eruptions led to stratospheric ozone depletion. Rather than a highly improbable coincidence, circulation and climate changes extending from the Antarctic Peninsula to the subtropics—similar to those associated with modern stratospheric ozone depletion over Antarctica—plausibly link the Mount Takahe eruptions to the onset of accelerated Southern Hemisphere deglaciation ∼17.7 ka.

Description: Coccolithophores are an important component of the Earth system, and, as calcifiers, their possible susceptibility to ocean acidification is of major concern. Laboratory studies at enhanced pCO2 levels have produced divergent results without overall consensus. However, it has been predicted from these studies that, although calcification may not be depressed in all species, acidification will produce "a transition in dominance from more to less heavily calcified coccolithophores"Ridgwell A, et al., (2009) Biogeosciences 6:2611-2623. A recent observational study Beaufort L, et al., (2011) Nature 476:80-83 also suggested that coccolithophores are less calcified in more acidic conditions.We present the results of a large observational study of coccolithophore morphology in the Bay of Biscay. Samples were collected once a month for over a year, along a 1,000-km-long transect. Our data clearly show that there is a pronounced seasonality in the morphotypes of Emiliania huxleyi, the most abundant coccolithophore species. Whereas pH and CaCO 3saturation are lowest in winter, the E. huxleyi population shifts from 〈10% (summer) to >90% (winter) of the heavily calcified form. However, it is unlikely that the shifts in carbonate chemistry alone caused the morphotype shift. Our finding that the most heavily calcified morphotype dominates when conditions are most acidic is contrary to the earlier predictions and raises further questions about the fate of coccolithophores in a high-CO2 world.

Description: Inorganic nitrogen depletion restricts productivity in much of the low-latitude oceans, generating a selective advantage for diazotrophic organisms capable of fixing atmospheric dinitrogen (N2). However, the abundance and activity of diazotrophs can in turn be controlled by the availability of other potentially limiting nutrients, including phosphorus (P) and iron (Fe). Here we present high-resolution data (∼0.3°) for dissolved iron, aluminum, and inorganic phosphorus that confirm the existence of a sharp north–south biogeochemical boundary in the surface nutrient concentrations of the (sub)tropical Atlantic Ocean. Combining satellite-based precipitation data with results from a previous study, we here demonstrate that wet deposition in the region of the intertropical convergence zone acts as the major dissolved iron source to surface waters. Moreover, corresponding observations of N2 fixation and the distribution of diazotrophic Trichodesmium spp. indicate that movement in the region of elevated dissolved iron as a result of the seasonal migration of the intertropical convergence zone drives a shift in the latitudinal distribution of diazotrophy and corresponding dissolved inorganic phosphorus depletion. These conclusions are consistent with the results of an idealized numerical model of the system. The boundary between the distinct biogeochemical systems of the (sub)tropical Atlantic thus appears to be defined by the diazotrophic response to spatial–temporal variability in external Fe inputs. Consequently, in addition to demonstrating a unique seasonal cycle forced by atmospheric nutrient inputs, we suggest that the underlying biogeochemical mechanisms would likely characterize the response of oligotrophic systems to altered environmental forcing over longer timescales.

Description: Diatoms of the iron-replete continental margins and North Atlantic are key exporters of organic carbon. In contrast, diatoms of the iron-limited Antarctic Circumpolar Current sequester silicon, but comparatively little carbon, in the underlying deep ocean and sediments. Because the Southern Ocean is the major hub of oceanic nutrient distribution, selective silicon sequestration there limits diatom blooms elsewhere and consequently the biotic carbon sequestration potential of the entire ocean. We investigated this paradox in an in situ iron fertilization experiment by comparing accumulation and sinking of diatom populations inside and outside the iron-fertilized patch over 5 wk. A bloom comprising various thin- and thick-shelled diatom species developed inside the patch despite the presence of large grazer populations. After the third week, most of the thinner-shelled diatom species underwent mass mortality, formed large, mucous aggregates, and sank out en masse (carbon sinkers). In contrast, thicker-shelled species, in particular Fragilariopsis kerguelensis, persisted in the surface layers, sank mainly empty shells continuously, and reduced silicate concentrations to similar levels both inside and outside the patch (silica sinkers). These patterns imply that thick-shelled, hence grazer-protected, diatom species evolved in response to heavy copepod grazing pressure in the presence of an abundant silicate supply. The ecology of these silica-sinking species decouples silicon and carbon cycles in the iron-limited Southern Ocean, whereas carbon-sinking species, when stimulated by iron fertilization, export more carbon per silicon. Our results suggest that large-scale iron fertilization of the silicate-rich Southern Ocean will not change silicon sequestration but will add carbon to the sinking silica flux.

Description: A major percentage of fixed nitrogen (N) loss in the oceans occurs within nitrite-rich oxygen minimum zones (OMZs) via denitrification and anammox. It remains unclear to what extent ammonium and nitrite oxidation co-occur, either supplying or competing for substrates involved in nitrogen loss in the OMZ core. Assessment of the oxygen (O2) sensitivity of these processes down to the O2 concentrations present in the OMZ core (〈10 nmol⋅L−1) is therefore essential for understanding and modeling nitrogen loss in OMZs. We determined rates of ammonium and nitrite oxidation in the seasonal OMZ off Concepcion, Chile at manipulated O2 levels between 5 nmol⋅L−1 and 20 μmol⋅L−1. Rates of both processes were detectable in the low nanomolar range (5–33 nmol⋅L−1 O2), but demonstrated a strong dependence on O2 concentrations with apparent half-saturation constants (Kms) of 333 ± 130 nmol⋅L−1 O2 for ammonium oxidation and 778 ± 168 nmol⋅L−1 O2 for nitrite oxidation assuming one-component Michaelis–Menten kinetics. Nitrite oxidation rates, however, were better described with a two-component Michaelis–Menten model, indicating a high-affinity component with a Km of just a few nanomolar. As the communities of ammonium and nitrite oxidizers were similar to other OMZs, these kinetics should apply across OMZ systems. The high O2 affinities imply that ammonium and nitrite oxidation can occur within the OMZ core whenever O2 is supplied, for example, by episodic intrusions. These processes therefore compete with anammox and denitrification for ammonium and nitrite, thereby exerting an important control over nitrogen loss.

Description: Long-term observations of the reactive chemical composition of the tropical marine boundary layer (MBL) are rare, despite its crucial role for the chemical stability of the atmosphere. Recent observations of reactive bromine species in the tropical MBL showed unexpectedly high levels that could potentially have an impact on the ozone budget. Uncertainties in the ozone budget are amplified by our poor understanding of the fate of NOx (= NO + NO2), particularly the importance of nighttime chemical NOx sinks. Here, we present year-round observations of the multiisotopic composition of atmospheric nitrate in the tropical MBL at the Cape Verde Atmospheric Observatory. We show that the observed oxygen isotope ratios of nitrate are compatible with nitrate formation chemistry, which includes the BrNO3 sink at a level of ca. 20 ± 10% of nitrate formation pathways. The results also suggest that the N2O5 pathway is a negligible NOx sink in this environment. Observations further indicate a possible link between the NO2/NOx ratio and the nitrogen isotopic content of nitrate in this low NOx environment, possibly reflecting the seasonal change in the photochemical equilibrium among NOx species. This study demonstrates the relevance of using the stable isotopes of oxygen and nitrogen of atmospheric nitrate in association with concentration measurements to identify and constrain chemical processes occurring in the MBL.

Description: The use of molecular methods is altering our understanding of the microbial biosphere and the complexity of the tree of life. Here, we report a newly discovered uncultured plastid-bearing eukaryotic lineage named the rappemonads. Phylogenies using near-complete plastid ribosomal DNA (rDNA) operons demonstrate that this group represents an evolutionarily distinct lineage branching with haptophyte and cryptophyte algae. Environmental DNA sequencing revealed extensive diversity at North Atlantic, North Pacific, and European freshwater sites, suggesting a broad ecophysiology and wide habitat distribution. Quantitative PCR analyses demonstrate that the rappemonads are often rare but can form transient blooms in the Sargasso Sea, where high 16S rRNA gene copies mL-1 were detected in late winter. This pattern is consistent with these microbes being a member of the rare biosphere, whose constituents have been proposed to play important roles under ecosystem change. Fluorescence in situ hybridization revealed that cells from this unique lineage were 6.6 ± 1.2 x 5.7 ± 1.0 μm, larger than numerically dominant open-ocean phytoplankton, and appear to contain two to four plastids. The rappemonads are unique, widespread, putatively photosynthetic algae that are absent from present-day ecosystem models and current versions of the tree of life.

Description: Phytochrome photosensors control a vast gene network in streptophyte plants, acting as master regulators of diverse growth and developmental processes throughout the life cycle. In contrast with their absence in known chlorophyte algal genomes and most sequenced prasinophyte algal genomes, a phytochrome is found in Micromonas pusilla , a widely distributed marine picoprasinophyte (〈2 μm cell diameter). Together with phytochromes identified from other prasinophyte lineages, we establish that prasinophyte and streptophyte phytochromes share core lightinput and signaling-output domain architectures except for the loss of C-terminal response regulator receiver domains in the streptophyte phytochrome lineage. Phylogenetic reconstructions robustly support the presence of phytochrome in the common progenitor of green algae and land plants. These analyses reveal a monophyletic clade containing streptophyte, prasinophyte, cryptophyte, and glaucophyte phytochromes implying an origin in the eukaryotic ancestor of the Archaeplastida. Transcriptomic measurements reveal diurnal regulation of phytochrome and bilin chromophore biosynthetic genes in Micromonas. Expression of these genes precedes both light-mediated phytochrome redistribution from the cytoplasm to the nucleus and increased expression of photo-synthesis-associated genes. Prasinophyte phytochromes perceive wavelengths of light transmitted farther through seawater than the red/far-red light sensed by land plant phytochromes. Prasinophyte phytochromes also retain light-regulated histidine kinase activity lost in the streptophyte phytochrome lineage. Our studies demonstrate that light-mediated nuclear translocation of phytochrome predates the emergence of land plants and likely represents a widespread signaling mechanism in unicellular algae.

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.