Armbrust
E. Virginia
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E. Virginia
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ArticleDaily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean(Nature Publishing Group, 2018-12-05) Becker, Kevin W. ; Collins, James R. ; Durham, Bryndan P. ; Groussman, Ryan D. ; White, Angelicque E. ; Fredricks, Helen F. ; Ossolinski, Justin E. ; Repeta, Daniel J. ; Carini, Paul ; Armbrust, E. Virginia ; Van Mooy, Benjamin A. S.Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr−1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.
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ArticleThe Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP) : illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing(Public Library of Science, 2014-06-24) Keeling, Patrick J. ; Burki, Fabien ; Wilcox, Heather M. ; Allam, Bassem ; Allen, Eric E. ; Amaral-Zettler, Linda A. ; Armbrust, E. Virginia ; Archibald, John M. ; Bharti, Arvind K. ; Bell, Callum J. ; Beszteri, Bank ; Bidle, Kay D. ; Cameron, Connor T. ; Campbell, Lisa ; Caron, David A. ; Cattolico, Rose Ann ; Collier, Jackie L. ; Coyne, Kathryn J. ; Davy, Simon K. ; Deschamps, Phillipe ; Dyhrman, Sonya T. ; Edvardsen, Bente ; Gates, Ruth D. ; Gobler, Christopher J. ; Greenwood, Spencer J. ; Guida, Stephanie M. ; Jacobi, Jennifer L. ; Jakobsen, Kjetill S. ; James, Erick R. ; Jenkins, Bethany D. ; John, Uwe ; Johnson, Matthew D. ; Juhl, Andrew R. ; Kamp, Anja ; Katz, Laura A. ; Kiene, Ronald P. ; Kudryavtsev, Alexander N. ; Leander, Brian S. ; Lin, Senjie ; Lovejoy, Connie ; Lynn, Denis ; Marchetti, Adrian ; McManus, George ; Nedelcu, Aurora M. ; Menden-Deuer, Susanne ; Miceli, Cristina ; Mock, Thomas ; Montresor, Marina ; Moran, Mary Ann ; Murray, Shauna A. ; Nadathur, Govind ; Nagai, Satoshi ; Ngam, Peter B. ; Palenik, Brian ; Pawlowski, Jan ; Petroni, Giulio ; Piganeau, Gwenael ; Posewitz, Matthew C. ; Rengefors, Karin ; Romano, Giovanna ; Rumpho, Mary E. ; Rynearson, Tatiana A. ; Schilling, Kelly B. ; Schroeder, Declan C. ; Simpson, Alastair G. B. ; Slamovits, Claudio H. ; Smith, David R. ; Smith, G. Jason ; Smith, Sarah R. ; Sosik, Heidi M. ; Stief, Peter ; Theriot, Edward ; Twary, Scott N. ; Umale, Pooja E. ; Vaulot, Daniel ; Wawrik, Boris ; Wheeler, Glen L. ; Wilson, William H. ; Xu, Yan ; Zingone, Adriana ; Worden, Alexandra Z.Microbial ecology is plagued by problems of an abstract nature. Cell sizes are so small and population sizes so large that both are virtually incomprehensible. Niches are so far from our everyday experience as to make their very definition elusive. Organisms that may be abundant and critical to our survival are little understood, seldom described and/or cultured, and sometimes yet to be even seen. One way to confront these problems is to use data of an even more abstract nature: molecular sequence data. Massive environmental nucleic acid sequencing, such as metagenomics or metatranscriptomics, promises functional analysis of microbial communities as a whole, without prior knowledge of which organisms are in the environment or exactly how they are interacting. But sequence-based ecological studies nearly always use a comparative approach, and that requires relevant reference sequences, which are an extremely limited resource when it comes to microbial eukaryotes. In practice, this means sequence databases need to be populated with enormous quantities of data for which we have some certainties about the source. Most important is the taxonomic identity of the organism from which a sequence is derived and as much functional identification of the encoded proteins as possible. In an ideal world, such information would be available as a large set of complete, well-curated, and annotated genomes for all the major organisms from the environment in question. Reality substantially diverges from this ideal, but at least for bacterial molecular ecology, there is a database consisting of thousands of complete genomes from a wide range of taxa, supplemented by a phylogeny-driven approach to diversifying genomics. For eukaryotes, the number of available genomes is far, far fewer, and we have relied much more heavily on random growth of sequence databases, raising the question as to whether this is fit for purpose.
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ArticleThe evolution of silicon transporters in diatoms(John Wiley & Sons, 2016-08-31) Durkin, Colleen A. ; Koester, Julie ; Bender, Sara J. ; Armbrust, E. VirginiaDiatoms are highly productive single-celled algae that form an intricately patterned silica cell wall after every cell division. They take up and utilize silicic acid from seawater via silicon transporter (SIT) proteins. This study examined the evolution of the SIT gene family to identify potential genetic adaptations that enable diatoms to thrive in the modern ocean. By searching for sequence homologs in available databases, the diversity of organisms found to encode SITs increased substantially and included all major diatom lineages and other algal protists. A bacterial-encoded gene with homology to SIT sequences was also identified, suggesting that a lateral gene transfer event occurred between bacterial and protist lineages. In diatoms, the SIT genes diverged and diversified to produce five distinct clades. The most basal SIT clades were widely distributed across diatom lineages, while the more derived clades were lineage-specific, which together produced a distinct repertoire of SIT types among major diatom lineages. Differences in the predicted protein functional domains encoded among SIT clades suggest that the divergence of clades resulted in functional diversification among SITs. Both laboratory cultures and natural communities changed transcription of each SIT clade in response to experimental or environmental growth conditions, with distinct transcriptional patterns observed among clades. Together, these data suggest that the diversification of SITs within diatoms led to specialized adaptations among diatoms lineages, and perhaps their dominant ability to take up silicic acid from seawater in diverse environmental conditions.
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PreprintCryptic carbon and sulfur cycling between surface ocean plankton( 2014-12) Durham, Bryndan P. ; Sharma, Shalabh ; Luo, Haiwei ; Smith, Christa B. ; Amin, Shady A. ; Bender, Sara J. ; Dearth, Stephen P. ; Van Mooy, Benjamin A. S. ; Campagna, Shawn R. ; Kujawinski, Elizabeth B. ; Armbrust, E. Virginia ; Moran, Mary AnnAbout half the carbon fixed by phytoplankton in the ocean is taken up and metabolized by marine bacteria, a transfer that is mediated through the seawater dissolved organic carbon (DOC) pool. The chemical complexity of marine DOC, along with a poor understanding of which compounds form the basis of trophic interactions between bacteria and phytoplankton, have impeded efforts to identify key currencies of this carbon cycle link. Here, we used transcriptional patterns in a bacterial-diatom model system based on vitamin B12 auxotrophy as a sensitive assay for metabolite exchange between marine plankton. The most highly upregulated genes (up to 374-fold) by a marine Roseobacter clade bacterium when co-cultured with the diatom Thalassiosira pseudonana were those encoding the transport and catabolism of 2,3- dihydroxypropane-1-sulfonate (DHPS). This compound has no currently recognized role in the marine microbial food web. As the genes for DHPS catabolism have limited distribution among bacterial taxa, T. pseudonana may use this novel sulfonate for targeted feeding of beneficial associates. Indeed, DHPS was both a major component of the T. pseudonana cytosol and an abundant microbial metabolite in a diatom bloom in the eastern North Pacific Ocean. Moreover, transcript analysis of the North Pacific samples provided evidence of DHPS catabolism by Roseobacter populations. Other such biogeochemically important metabolites may be common in the ocean but difficult to discriminate against the complex chemical background of seawater. Bacterial transformation of this diatom-derived sulfonate represents a new and likely sizeable link in both the marine carbon and sulfur cycles.
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ArticleDiel transcriptional oscillations of light-sensitive regulatory elements in open-ocean eukaryotic plankton communities(National Academy of Sciences, 2021-02-09) Coesel, Sacha N. ; Durham, Bryndan P. ; Groussman, Ryan D. ; Hu, Sarah K. ; Caron, David A. ; Morales, Rhonda L. ; Ribalet, François ; Armbrust, E. VirginiaThe 24-h cycle of light and darkness governs daily rhythms of complex behaviors across all domains of life. Intracellular photoreceptors sense specific wavelengths of light that can reset the internal circadian clock and/or elicit distinct phenotypic responses. In the surface ocean, microbial communities additionally modulate nonrhythmic changes in light quality and quantity as they are mixed to different depths. Here, we show that eukaryotic plankton in the North Pacific Subtropical Gyre transcribe genes encoding light-sensitive proteins that may serve as light-activated transcription factors, elicit light-driven electrical/chemical cascades, or initiate secondary messenger-signaling cascades. Overall, the protistan community relies on blue light-sensitive photoreceptors of the cryptochrome/photolyase family, and proteins containing the Light-Oxygen-Voltage (LOV) domain. The greatest diversification occurred within Haptophyta and photosynthetic stramenopiles where the LOV domain was combined with different DNA-binding domains and secondary signal-transduction motifs. Flagellated protists utilize green-light sensory rhodopsins and blue-light helmchromes, potentially underlying phototactic/photophobic and other behaviors toward specific wavelengths of light. Photoreceptors such as phytochromes appear to play minor roles in the North Pacific Subtropical Gyre. Transcript abundance of environmental light-sensitive protein-encoding genes that display diel patterns are found to primarily peak at dawn. The exceptions are the LOV-domain transcription factors with peaks in transcript abundances at different times and putative phototaxis photoreceptors transcribed throughout the day. Together, these data illustrate the diversity of light-sensitive proteins that may allow disparate groups of protists to respond to light and potentially synchronize patterns of growth, division, and mortality within the dynamic ocean environment.
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ArticleDisentangling top-down drivers of mortality underlying diel population dynamics of Prochlorococcus in the North Pacific Subtropical Gyre(Nature Research, 2024-03-07) Beckett, Stephen J. ; Demory, David ; Coenen, Ashley R. ; Casey, John R. ; Dugenne, Mathilde ; Follett, Christopher L. ; Connell, Paige ; Carlson, Michael C. G. ; Hu, Sarah K. ; Wilson, Samuel T. ; Muratore, Daniel ; Rodriguez-Gonzalez, Rogelio A. ; Peng, Shengyun ; Becker, Kevin W. ; Mende, Daniel R. ; Armbrust, E. Virginia ; Caron, David A. ; Lindell, Debbie ; White, Angelicque E. ; Ribalet, Francois ; Weitz, Joshua S.Photosynthesis fuels primary production at the base of marine food webs. Yet, in many surface ocean ecosystems, diel-driven primary production is tightly coupled to daily loss. This tight coupling raises the question: which top-down drivers predominate in maintaining persistently stable picocyanobacterial populations over longer time scales? Motivated by high-frequency surface water measurements taken in the North Pacific Subtropical Gyre (NPSG), we developed multitrophic models to investigate bottom-up and top-down mechanisms underlying the balanced control of Prochlorococcus populations. We find that incorporating photosynthetic growth with viral- and predator-induced mortality is sufficient to recapitulate daily oscillations of Prochlorococcus abundances with baseline community abundances. In doing so, we infer that grazers in this environment function as the predominant top-down factor despite high standing viral particle densities. The model-data fits also reveal the ecological relevance of light-dependent viral traits and non-canonical factors to cellular loss. Finally, we leverage sensitivity analyses to demonstrate how variation in life history traits across distinct oceanic contexts, including variation in viral adsorption and grazer clearance rates, can transform the quantitative and even qualitative importance of top-down controls in shaping Prochlorococcus population dynamics.