Dupont Christopher L.
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ArticleThaumarchaeal ecotype distributions across the equatorial Pacific Ocean and their potential roles in nitrification and sinking flux attenuation(John Wiley & Sons, 2017-04-05) Santoro, Alyson E. ; Saito, Mak A. ; Goepfert, Tyler J. ; Lamborg, Carl H. ; Dupont, Christopher L. ; DiTullio, Giacomo R.Thaumarchaea are among the most abundant microbial groups in the ocean, but controls on their abundance and the distribution and metabolic potential of different subpopulations are poorly constrained. Here, two ecotypes of ammonia-oxidizing thaumarchaea were quantified using ammonia monooxygenase (amoA) genes across the equatorial Pacific Ocean. The shallow, or water column “A” (WCA), ecotype was the most abundant ecotype at the depths of maximum nitrification rates, and its abundance correlated with other biogeochemical indicators of remineralization such as NO3 : Si and total Hg. Metagenomes contained thaumarchaeal genes encoding for the catalytic subunit of the urease enzyme (ureC) at all depths, suggesting that members of both WCA and the deep, water column “B” (WCB) ecotypes may contain ureC. Coupled urea hydrolysis-ammonia oxidation rates were similar to ammonia oxidation rates alone, suggesting that urea could be an important source of ammonia for mesopelagic ammonia oxidizers. Potential inducement of metal limitation of both ammonia oxidation and urea hydrolysis was demonstrated via additions of a strong metal chelator. The water column inventory of WCA was correlated with the depth-integrated abundance of WCB, with both likely controlled by the flux of sinking particulate organic matter, providing strong evidence of vertical connectivity between the ecotypes. Further, depth-integrated amoA gene abundance and nitrification rates were correlated with particulate organic nitrogen flux measured by contemporaneously deployed sediment traps. Together, the results refine our understanding of the controls on thaumarchaeal distributions in the ocean, and provide new insights on the relationship between material flux and microbial communities in the mesopelagic.
PreprintTrace elements at the intersection of marine biological and geochemical evolution( 2016-10) Robbins, Leslie J. ; Lalonde, Stefan V. ; Planavsky, Noah J. ; Partin, Camille A. ; Reinhard, Christopher T. ; Kendall, Brian ; Scott, Clint ; Hardisty, Dalton S. ; Gill, Benjamin C. ; Alessi, Daniel S. ; Dupont, Christopher L. ; Saito, Mak A. ; Crowe, Sean A. ; Poulton, Simon W. ; Bekker, Andrey ; Lyons, Timothy W. ; Konhauser, Kurt O.Life requires a wide variety of bioessential trace elements to act as structural components and reactive centers in metalloenzymes. These requirements differ between organisms and have evolved over geological time, likely guided in some part by environmental conditions. Until recently, most of what was understood regarding trace element concentrations in the Precambrian oceans was inferred by extrapolation, geochemical modeling, and/or genomic studies. However, in the past decade, the increasing availability of trace element and isotopic data for sedimentary rocks of all ages have yielded new, and potentially more direct, insights into secular changes in seawater composition – and ultimately the evolution of the marine biosphere. Compiled records of many bioessential trace elements (including Ni, Mo, P, Zn, Co, Cr, Se, and I) provide new insight into how trace element abundance in Earth’s ancient oceans may have been linked to biological evolution. Several of these trace elements display redox-sensitive behavior, while others are redox-sensitive but not bioessential (e.g., Cr, U). Their temporal trends in sedimentary archives provide useful constraints on changes in atmosphere-ocean redox conditions that are linked to biological evolution, for example, the activity of oxygen-producing, photosynthetic cyanobacteria. In this review, we summarize available Precambrian trace element proxy data, and discuss how temporal trends in the seawater concentrations of specific trace elements may be linked to the evolution of both simple and complex life. We also examine several biologically relevant and/or redox-sensitive trace elements that have yet to be fully examined in the sedimentary rock record (e.g., Cu, Cd, W) and suggest several directions for future studies.
ArticleMicrobial functional diversity across biogeochemical provinces in the central Pacific Ocean(National Academy of Sciences, 2022-09-13) Saunders, Jaclyn K. ; McIlvin, Matthew R. ; Dupont, Christopher L. ; Kaul, Drishti ; Moran, Dawn M. ; Horner, Tristan J. ; Laperriere, Sarah ; Webb, Eric A. ; Bosak, Tanja ; Santoro, Alyson E. ; Saito, Mak A.Enzymes catalyze key reactions within Earth’s life-sustaining biogeochemical cycles. Here, we use metaproteomics to examine the enzymatic capabilities of the microbial community (0.2 to 3 µm) along a 5,000-km-long, 1-km-deep transect in the central Pacific Ocean. Eighty-five percent of total protein abundance was of bacterial origin, with Archaea contributing 1.6%. Over 2,000 functional KEGG Ontology (KO) groups were identified, yet only 25 KO groups contributed over half of the protein abundance, simultaneously indicating abundant key functions and a long tail of diverse functions. Vertical attenuation of individual proteins displayed stratification of nutrient transport, carbon utilization, and environmental stress. The microbial community also varied along horizontal scales, shaped by environmental features specific to the oligotrophic North Pacific Subtropical Gyre, the oxygen-depleted Eastern Tropical North Pacific, and nutrient-rich equatorial upwelling. Some of the most abundant proteins were associated with nitrification and C1 metabolisms, with observed interactions between these pathways. The oxidoreductases nitrite oxidoreductase (NxrAB), nitrite reductase (NirK), ammonia monooxygenase (AmoABC), manganese oxidase (MnxG), formate dehydrogenase (FdoGH and FDH), and carbon monoxide dehydrogenase (CoxLM) displayed distributions indicative of biogeochemical status such as oxidative or nutritional stress, with the potential to be more sensitive than chemical sensors. Enzymes that mediate transformations of atmospheric gases like CO, CO2, NO, methanethiol, and methylamines were most abundant in the upwelling region. We identified hot spots of biochemical transformation in the central Pacific Ocean, highlighted previously understudied metabolic pathways in the environment, and provided rich empirical data for biogeochemical models critical for forecasting ecosystem response to climate change.
ArticleMetabolic versatility of the nitrite-oxidizing bacterium Nitrospira marina and its proteomic response to oxygen-limited conditions(Springer Nature, 2020-11-23) Bayer, Barbara ; Saito, Mak A. ; McIlvin, Matthew R. ; Lücker, Sebastian ; Moran, Dawn M. ; Lankiewicz, Thomas S. ; Dupont, Christopher L. ; Santoro, Alyson E.The genus Nitrospira is the most widespread group of nitrite-oxidizing bacteria and thrives in diverse natural and engineered ecosystems. Nitrospira marina Nb-295T was isolated from the ocean over 30 years ago; however, its genome has not yet been analyzed. Here, we investigated the metabolic potential of N. marina based on its complete genome sequence and performed physiological experiments to test genome-derived hypotheses. Our data confirm that N. marina benefits from additions of undefined organic carbon substrates, has adaptations to resist oxidative, osmotic, and UV light-induced stress and low dissolved pCO2, and requires exogenous vitamin B12. In addition, N. marina is able to grow chemoorganotrophically on formate, and is thus not an obligate chemolithoautotroph. We further investigated the proteomic response of N. marina to low (∼5.6 µM) O2 concentrations. The abundance of a potentially more efficient CO2-fixing pyruvate:ferredoxin oxidoreductase (POR) complex and a high-affinity cbb3-type terminal oxidase increased under O2 limitation, suggesting a role in sustaining nitrite oxidation-driven autotrophy. This putatively more O2-sensitive POR complex might be protected from oxidative damage by Cu/Zn-binding superoxide dismutase, which also increased in abundance under low O2 conditions. Furthermore, the upregulation of proteins involved in alternative energy metabolisms, including Group 3b [NiFe] hydrogenase and formate dehydrogenase, indicate a high metabolic versatility to survive conditions unfavorable for aerobic nitrite oxidation. In summary, the genome and proteome of the first marine Nitrospira isolate identifies adaptations to life in the oxic ocean and provides insights into the metabolic diversity and niche differentiation of NOB in marine environments.
ArticleGenetic tool development in marine protists: emerging model organisms for experimental cell biology(Nature Research, 2020-04-06) Faktorová, Drahomíra ; Nisbet, R. Ellen R. ; Fernández Robledo, José A. ; Casacuberta, Elena ; Sudek, Lisa ; Allen, Andrew E. ; Ares, Manuel, Jr. ; Aresté, Cristina ; Balestreri, Cecilia ; Barbrook, Adrian C. ; Beardslee, Patrick ; Bender, Sara J. ; Booth, David S. ; Bouget, François-Yves ; Bowler, Chris ; Breglia, Susana A. ; Brownlee, Colin ; Burger, Gertraud ; Cerutti, Heriberto ; Cesaroni, Rachele ; Chiurillo, Miguel A. ; Clemente, Thomas ; Coles, Duncan B. ; Collier, Jackie L. ; Cooney, Elizabeth C. ; Coyne, Kathryn J. ; Docampo, Roberto ; Dupont, Christopher L. ; Edgcomb, Virginia P. ; Einarsso, Elin ; Elustondo, Pía A. ; Federici, Fernan ; Freire-Beneitez, Veronica ; Freyria, Nastasia J. ; Fukuda, Kodai ; García, Paulo A. ; Girguis, Peter R. ; Gomaa, Fatma ; Gornik, Sebastian G. ; Guo, Jian ; Hampl, Vladimír ; Hanawa, Yutaka ; Haro-Contreras, Esteban R. ; Hehenberger, Elisabeth ; Highfield, Andrea ; Hirakawa, Yoshihisa ; Hopes, Amanda ; Howe, Christopher J. ; Hu, Ian ; Ibañez, Jorge ; Irwin, Nicholas A. T. ; Ishii, Yuu ; Janowicz, Natalia Ewa ; Jones, Adam C. ; Kachale, Ambar ; Fujimura-Kamada, Konomi ; Kaur, Binnypreet ; Kaye, Jonathan Z. ; Kazana, Eleanna ; Keeling, Patrick J. ; King, Nicole ; Klobutcher, Lawrence A. ; Lander, Noelia ; Lassadi, Imen ; Li, Zhuhong ; Lin, Senjie ; Lozano, Jean-Claude ; Luan, Fulei ; Maruyama, Shinichiro ; Matute, Tamara ; Miceli, Cristina ; Minagawa, Jun ; Moosburner, Mark ; Najle, Sebastián R. ; Nanjappa, Deepak ; Nimmo, Isabel C. ; Noble, Luke ; Novák Vanclová, Anna M. G. ; Nowacki, Mariusz ; Nuñez, Isaac ; Pain, Arnab ; Piersanti, Angela ; Pucciarelli, Sandra ; Pyrih, Jan ; Rest, Joshua S. ; Rius, Mariana ; Robertson, Deborah ; Ruaud, Albane ; Ruiz-Trillo, Iñaki ; Sigg, Monika A. ; Silver, Pamela A. ; Slamovits, Claudio H. ; Smith, G. Jason ; Sprecher, Brittany N. ; Stern, Rowena ; Swart, Estienne C. ; Tsaousis, Anastasios D. ; Tsypin, Lev ; Turkewitz, Aaron ; Turnšek, Jernej ; Valach, Matus ; Vergé, Valérie ; von Dassow, Peter ; von der Haar, Tobias ; Waller, Ross F. ; Wang, Lu ; Wen, Xiaoxue ; Wheeler, Glen L. ; Woods, April ; Zhang, Huan ; Mock, Thomas ; Worden, Alexandra Z. ; Lukes, JuliusDiverse microbial ecosystems underpin life in the sea. Among these microbes are many unicellular eukaryotes that span the diversity of the eukaryotic tree of life. However, genetic tractability has been limited to a few species, which do not represent eukaryotic diversity or environmentally relevant taxa. Here, we report on the development of genetic tools in a range of protists primarily from marine environments. We present evidence for foreign DNA delivery and expression in 13 species never before transformed and for advancement of tools for eight other species, as well as potential reasons for why transformation of yet another 17 species tested was not achieved. Our resource in genetic manipulation will provide insights into the ancestral eukaryotic lifeforms, general eukaryote cell biology, protein diversification and the evolution of cellular pathways.