Becker
Kevin W.
Becker
Kevin W.
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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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PreprintUnusual butane- and pentanetriol-based tetraether lipids in Methanomassiliicoccus luminyensis, a representative of the seventh order of methanogens( 2016-05) Becker, Kevin W. ; Elling, Felix J. ; Yoshinaga, Marcos Y. ; Sollinger, Andrea ; Urich, Tim ; Hinrichs, Kai-UweA new clade of archaea has recently been proposed to constitute the seventh methanogenic order, the Methanomassiliicoccales, which is related to the Thermoplasmatales and the uncultivated archaeal clades deep-sea hydrothermal vent Euryarchaeota group 2 and marine group II Euryarchaeota but only distantly related to other methanogens. In this study, we investigated the membrane lipid composition of Methanomassiliicoccus luminyensis, the sole cultured representative of this seventh order. The lipid inventory of M. luminyensis comprises a unique assemblage of novel lipids as well as lipids otherwise typical for thermophilic, methanogenic, or halophilic archaea. For instance, glycerol sesterpanyl-phytanyl diether core lipids found mainly in halophilic archaea were detected, and so were compounds bearing either heptose or methoxylated glycosidic head groups, neither of which have been reported so far for other archaea. The absence of quinones or methanophenazines is consistent with a biochemistry of methanogenesis different from that of the methanophenazine-containing methylotrophic methanogens. The most distinctive characteristic of the membrane lipid composition of M. luminyensis, however, is the presence of tetraether lipids in which one glycerol backbone is replaced by either butane- or pentanetriol, i.e., lipids recently discovered in marine sediments. Butanetriol dibiphytanyl glycerol tetraether (BDGT) constitutes the most abundant core lipid type (>50% relative abundance) in M. luminyensis. We have thus identified a source for these unusual orphan lipids. The complementary analysis of diverse marine sediment samples showed that BDGTs are widespread in anoxic layers, suggesting an environmental significance of Methanomassiliicoccales and/or related BDGT producers beyond gastrointestinal tracts.
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ArticleParticulate organic carbon deconstructed: molecular and chemical composition of particulate organic carbon in the ocean(Frontiers Media, 2020-06-26) Kharbush, Jenan J. ; Close, Hilary G. ; Van Mooy, Benjamin A. S. ; Arnosti, Carol ; Smittenberg, Rienk H. ; Le Moigne, Frederic A. C. ; Mollenhauer, Gesine ; Scholz-Böttcher, Barbara ; Obreht, Igor ; Koch, Boris P. ; Becker, Kevin W. ; Iversen, Morten H. ; Mohr, WiebkeThe dynamics of the particulate organic carbon (POC) pool in the ocean are central to the marine carbon cycle. POC is the link between surface primary production, the deep ocean, and sediments. The rate at which POC is degraded in the dark ocean can impact atmospheric CO2 concentration. Therefore, a central focus of marine organic geochemistry studies is to improve our understanding of POC distribution, composition, and cycling. The last few decades have seen improvements in analytical techniques that have greatly expanded what we can measure, both in terms of organic compound structural diversity and isotopic composition, and complementary molecular omics studies. Here we provide a brief overview of the autochthonous, allochthonous, and anthropogenic components comprising POC in the ocean. In addition, we highlight key needs for future research that will enable us to more effectively connect diverse data sources and link the identity and structural diversity of POC to its sources and transformation processes.
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ArticleTargeted metabolomics reveals proline as a major osmolyte in the chemolithoautotroph Sulfurimonas denitrificans(John Wiley & Sons, 2018-02-09) Götz, Florian ; Longnecker, Krista ; Kido Soule, Melissa C. ; Becker, Kevin W. ; McNichol, Jesse C. ; Kujawinski, Elizabeth B. ; Sievert, Stefan M.Chemoautotrophic bacteria belonging to the genus Sulfurimonas in the class Campylobacteria are widespread in many marine environments characterized by redox interfaces, yet little is known about their physiological adaptations to different environmental conditions. Here, we used liquid chromatography coupled with tandem mass spectrometry (LC-MS/ MS) in a targeted metabolomics approach to study the adaptations of Sulfurimonas denitrificans to varying salt concentrations that are found in its natural habitat of tidal mudflats. Proline was identified as one of the most abundant internal metabolites and its concentration showed a strong positive correlation with ionic strength, suggesting that it acts as an important osmolyte in S. denitrificans. 2,3-dihydroxypropane- 1- sulfonate was also positively correlated with ionic strength, indicating it might play a previously unrecognized role in osmoregulation. Furthermore, the detection of metabolites from the reductive tricarboxylic acid cycle at high internal concentrations reinforces the importance of this pathway for carbon fixation in Campylobacteria and as a hub for biosynthesis. As the first report of metabolomic data for an campylobacterial chemolithoautotroph, this study provides data that will be useful to understand the adaptations of Campylobacteria to their natural habitat at redox interfaces.
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ArticleMethane- and dissolved organic carbon-fueled microbial loop supports a tropical subterranean estuary ecosystem(Nature Publishing Group, 2017-11-28) Brankovits, David ; Pohlman, John W. ; Niemann, Helge ; Leigh, Mary Beth ; Leewis, Mary-Cathrine ; Becker, Kevin W. ; Iliffe, Thomas ; Alvarez, Fernando ; Lehmann, Moritz F. ; Phillips, BilSubterranean estuaries extend inland into density-stratified coastal carbonate aquifers containing a surprising diversity of endemic animals (mostly crustaceans) within a highly oligotrophic habitat. How complex ecosystems (termed anchialine) thrive in this globally distributed, cryptic environment is poorly understood. Here, we demonstrate that a microbial loop shuttles methane and dissolved organic carbon (DOC) to higher trophic levels of the anchialine food web in the Yucatan Peninsula (Mexico). Methane and DOC production and consumption within the coastal groundwater correspond with a microbial community capable of methanotrophy, heterotrophy, and chemoautotrophy, based on characterization by 16S rRNA gene amplicon sequencing and respiratory quinone composition. Fatty acid and bulk stable carbon isotope values of cave-adapted shrimp suggest that carbon from methanotrophic bacteria comprises 21% of their diet, on average. These findings reveal a heretofore unrecognized subterranean methane sink and contribute to our understanding of the carbon cycle and ecosystem function of karst subterranean estuaries.
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ArticleLinking diatom-diazotroph symbioses to nitrogen cycle perturbations and deep-water anoxia: insights from Mediterranean sapropel events(Elsevier, 2021-07-30) Elling, Felix J. ; Hemingway, Jordon D. ; Kharbush, Jenan J. ; Becker, Kevin W. ; Polik, Catherine A. ; Pearson, AnnElevated organic matter (OM) export flux promotes marine anoxia, thus increasing carbon sequestration efficiency and decreasing atmospheric carbon dioxide levels. However, the mechanisms that trigger and sustain anoxic events—particularly those associated with nutrient-poor, oligotrophic surface waters—remain poorly constrained. Mediterranean Sea sapropels are well-preserved sediments deposited during episodic anoxic events throughout the Plio-Pleistocene; as such, they may provide unique insight into the biogeochemical and ecological drivers of—and responses to—marine anoxia. Using biomarker distributions, we demonstrate that anaerobic ammonium oxidizing (anammox) bacteria and diazotrophic endosymbionts of mat- and/or raft-forming diatoms were both abundant during sapropel events, particularly in the Ionian and Libyan seas. In these sapropels, the carbon isotope compositions of anammox biomarkers directly capture progressive 13C-depletion in deep-water dissolved inorganic carbon, indicating sustained carbon sequestration. To explain these observations, we propose a reinforcing feedback whereby initial nutrient and/or circulation perturbations promote fixed nitrogen loss via intensified anammox and heterotrophic denitrification, which in turn favors proliferation of rapidly sinking diatom-diazotroph symbiotic consortia, increases OM burial flux, and sustains anoxia. This mechanism resolves the long-standing conundrum that small and buoyant diazotrophs are apparently associated with high OM export during periods of marine anoxia and oligotrophy.
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ArticleProchlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes(Society for Applied Microbiology, 2021-11-12) Biller, Steven J. ; Lundeen, Rachel A. ; Hmelo, Laura R. ; Becker, Kevin W. ; Arellano, Aldo A. ; Dooley, Keven ; Heal, Katherine R. ; Carlson, Laura Truxal ; Van Mooy, Benjamin A. S. ; Ingalls, Anitra ; Chisholm, Sallie W.Extracellular vesicles are small (~50–200 nm diameter) membrane-bound structures released by cells from all domains of life. While vesicles are abundant in the oceans, their functions, both for cells themselves and the emergent ecosystem, remain a mystery. To better characterize these particles – a prerequisite for determining function – we analysed the lipid, protein, and metabolite content of vesicles produced by the marine cyanobacterium Prochlorococcus. We show that Prochlorococcus exports a diverse array of cellular compounds into the surrounding seawater enclosed within discrete vesicles. Vesicles produced by two different strains contain some materials in common, but also display numerous strain-specific differences, reflecting functional complexity within vesicle populations. The vesicles contain active enzymes, indicating that they can mediate extracellular biogeochemical reactions in the ocean. We further demonstrate that vesicles from Prochlorococcus and other bacteria associate with diverse microbes including the most abundant marine bacterium, Pelagibacter. Together, our data point toward hypotheses concerning the functional roles of vesicles in marine ecosystems including, but not limited to, possibly mediating energy and nutrient transfers, catalysing extracellular biochemical reactions, and mitigating toxicity of reactive oxygen species.
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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.