Past Research
Protistan metabolism along a coastal-offshore transition zone revealed through autonomous underwater profiling
Using WHOI’s newest AUV Clio, high resolution vertical sampling was achieved along a BATS-WHOI transect in June 2019, capturing metabolic signatures of protists from oligotrophic, continental margin, and productive coastal ecosystems. Taxonomy and functional composition was examined using a paired metatranscriptomic and metaproteomic approach. A diverse community consisting of haptophytes, stramenopiles, dinoflagellates and ciliates were represented in both the transcript and protein fractions, with foraminifera proteins enriched >200 m, and fungi proteins emerging in waters >3,000 m, coinciding with a nepheloid layer on the continental shelf. In the broad protistan community, indications of nitrogen stress were detected at coastal sites, and phosphorus stress in transitionary waters. Dissolved and particulate trace metal distributions were compared to metal-dependent metabolic processes, and suggest a vertical delineation of key metalloproteins dependent on availability of metal cofactor. This multi-omics dataset broadens our understanding of how marine microbial taxonomy and functional diversity is structured along environmental gradients of macronutrients, trace metals, light, and temperature.
Cohen, NR, Krinos AI, Kell RM, Chmiel RJ, Moran DM, McIlvin MR, Lopez PZ, Barth A, Stone J, Alanis BA, Chan EW, Breier JA, Jakuba MV, Johnson R, Alexander H, Saito MA (2023) Microeukaryote metabolism across the western North Atlantic Ocean revealed through autonomous underwater profiling. Preprint: biorxiv.org/content/10.1101/2023.11.20.567900v1.full
Hydrothermal metal input near the Tongan plateau of the tropical South Pacific
In addition to exploring protistan ecology in the surface and mesopelagic of the central Pacific, we are also investigating the influence of hydrothermal metal release on deep sea communities. Low continentally-derived bioactive trace metal supplies limits microbial growth in the tropical South Pacific Ocean, inhibiting primary production and the biological transformation of carbon. Subsurface hydrothermal vents may serve as important sources of iron and other trace metals to microorganisms living in metal-deplete seawater ecosystems. Off the Somoan Islands in the Northeast Lau Basin, hydrothermal activity (3He/4He) has been measured at approximately 1,700 and 2,500 m, with the shallow helium plume hypothesized to be derived locally and the deeper signature advected from the East Pacific Rise (Lupton et al. 2004). Using seawater samples collected during the original cruise, dissolved metals were quantified along the meridionial transect. Acidified seawater was previously preconcentrated using the magnesium hydroxide precipitation method, and we confirmed dissolved metal distributions using the seaFAST preconcentration system and ICPMS. Results indicate elevated iron and manganese concentrations consistent with hydrothermal sources, and an associated hydrothermal signal in particle-associated bacterial proteins in the distal plume influenced-site compared to deep background locations.
Cohen NR, Noble AE, Moran DM, McIlvin MR, Goeptfert TJ, Hawco NJ, German CR, Horner TJ, Lamborg CH, McCrow JP, Allen AE, Saito MA. Hydrothermal trace metal release and microbial metabolism in the Northeast Lau Basin of the south Pacific Ocean (2021) Biogeosciences https://bg.copernicus.org/articles/18/5397/2021/bg-18-5397-2021.html
Dinoflagellates alter carbon and nutrient metabolism across biogeochemical gradients
A natural geochemical gradient exists in the central Pacific Ocean in which tropical, oligotrophic regions are low in nitrogen (N), while the equatorial upwelling region is N-rich and comparatively low in dissolved iron (Fe). It is unknown how unicellular eukaryotes (protists) across this transition zone differ in nutrient utilization, growth strategies, and contributions to carbon export. Using a combined ‘omic set including metatranscriptomes, metaproteomes, and 18S metabarcoding data along with geochemical measurements, we have characterized metabolic profiles spanning the euphotic to mesopelagic zones. Our findings suggest that dinoflagellates are relatively abundant throughout the water column (to ~800m) and demonstrate a tremendous amount of plasticity when adapting to various chemical environments. Although diatoms are typically regarded as key eukaryotes driving the biological carbon pump in the equatorial Pacific, our results suggest that the dinoflagellates play a previously unrecognized role in the ecosystem due to their broad extent and diverse metabolic strategies.
Cohen NR, McIlvin MR, Moran DM, Hawco NJ, Held NA, Saunders JK, Brosnahan M, DiTullio G, Lamborg C, McCrow J, Dupont C, Allen A, Saito MA. Dinoflagellates alter their carbon and nutrient metabolic strategies across environmental gradients in the central Pacific Ocean (2021) Nature Microbiology https://www.nature.com/articles/s41564-020-00814-7
Molecular ecophysiology of Pseudo-nitzschia granii
Members of the diatom genus Pseudo-nitzschia are ecologically important diatoms within iron-limited regions of the ocean, able to subsist during long periods of chronic iron limitation and quickly form dense blooms following iron fertilization events. The cellular strategies within diatoms from these regions that orchestrate these physiological responses to variable iron concentrations remain largely uncharacterized. We explore the exceptional ability of a diatom isolated from iron-limited waters of the Northeast Pacific Ocean to reorganize intracellular processes as a function of iron by examining its transcriptome and proteome under iron limitation. We conclude that P. granii is rather unique amongst studied diatoms in its iron physiology stemming from its distinctive cellular responses, which may underly its ability to subsist in low iron regions and rapidly bloom and outcompete other diatom taxa following iron enrichment.
Cohen NR, Gong W, Moran DM, McIlvin MR, Saito MA, Marchetti A. Transcriptomic and proteomic responses of the oceanic diatom Pseudo-nitzschia granii to iron limitation. (2018) Environmental Microbiology 20(8): 3109–3126 doi:10.1111/1462-2920.14386
Comparison of iron-related metabolic strategies between diatom taxa and across ocean provinces
Iron-limited diatom growth has been characterized in both oceanic and coastal waters of the North Pacific Ocean, however the strategies diatoms utilize to cope with iron limitation and iron resupply events may differ between the two systems. We investigated the responses of diatom communities to variable iron conditions through mesocosm incubation experiments performed in the sporadically iron-limited coastal California Upwelling Zone and the chronically iron-limited subarctic Northeast Pacific Ocean. In particular, we examined iron-related metabolic processes in two ecologically dominant diatom genera: Pseudo-nitzschia and Thalassiosira, via metatranscriptomic sequencing and physiological approaches. We observed several strategies for dealing with iron stress and responding to iron enrichment that were distinct among regions and between diatom genera, suggesting geographically- and taxonomically-diverse diatoms have evolved iron metabolisms optimized for different purposes.
Cohen NR, Ellis KA, Lampe RH, McNair H, Twining BS, Maldonado MT, Brzezinksi MA, Kuzminov FI, Thamatrakoln K, Till CP, Bruland KW, Sunda WG, Bargu S, Marchetti A. Diatom transcriptional and physiological responses to changes in iron bioavailability across ocean provinces (2017) Frontiers in Marine Science 4:360. doi:10.3389/fmars.2017.00360
Ferritin functional roles in diatoms
A large amount of genetic diversity is contained within the group of phytoplankton that responds to iron addition events very quickly in the surface ocean: the diatoms. Diatom species often vary in their physiological response to iron, with large blooms of primarily pennate diatoms blooming when iron is added to previously iron-limited waters. The ability of pennate diatoms to proliferate following iron addition has been partly attributed to their ability to store iron through the iron storage protein, ferritin. However, transcriptomic sequencing of diatoms indicates that some centric diatoms also possess ferritin proteins. Using a combination of physiological and targeted gene expression approaches, we examined the iron storage capacities and associated ferritin gene expression among diverse diatoms grown under a range of iron levels. This work explores how a single protein may be used for multiple purposes among diatoms, likely depending on the environment in which each taxon is adapted.
Cohen NR, Mann, E, Stemple B, Raushenberg S, Jacquot J, Moreno C, Sunda W.G, Twining B.S, Marchetti A. Iron storage capacities and associated ferritin gene expression among marine diatoms. (2018) Limnology & Oceanography 63: 1677-1691 doi:10.1002/lno.10800
Iron and vitamin interactions in diatoms
Trace metals (such as iron) and biologically-synthesized compounds (such as B-vitamins) play critical roles in regulating marine microorganism growth and composition. Unfortunately, only some microorganisms in the surface ocean are capable of producing these important B-vitamins, while others cannot and depend on others for their supply. Therefore the external factors influencing B-vitamin production, such as iron status, alter the extent to which B-vitamins are available in surface waters. Laboratory culture experiments with targeted gene expression analyses in diatoms indicate changes in iron bioavailability influence B7 (biotin) synthesis, but not B12 (cobalamin)-sensitive machinery. However, molecular indications of B12 stress are observed in certain members of natural diatom assemblages in the Northeast Pacific Ocean following iron enrichment, as determined through community-wide bioinformatic analyses. This is likely a result of B12 consumption by blooming taxa offsetting microbial B12 production. As a result of altered vitamin levels following natural or artificial iron fertilization, phytoplankton may experience changes in community composition, potentially causing shifts in biogeochemical cycling patterns. This is important because a seemingly minor physiological characteristic, such as the thickness of a diatom’s silica shell, can substantially influence the efficiency of the biological carbon pump, with heavier, thicker cells transporting more carbon to the deep ocean!
Cohen NR, Ellis KA, Burns W, Lampe RH, Schuback N, Johnson Z, Sa˜nudo-Wilhelmy S, Marchetti A. Iron and vitamin interactions in marine diatom isolates and natural assemblages of the Northeast Pacific Ocean (2017) Limnology & Oceanography aslopubs.onlinelibrary.wiley.com/doi/abs/10. 1002/lno.10552
Ellis KA, Cohen NR, Moreno CM, Marchetti A. Cobalamin-independent Methionine synthase distribution and Influence on Vitamin B12 Growth Requirements in Marine Diatoms (2017) Protist www.sciencedirect.com/science/article/abs/pii/S1434461016300682
