Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Cuvelier, Marie L.; Allen, Andrew E.; Monier, Adam; McCrow, John P.; Messié, Monique; Tringe, Susannah G.; Woyke, Tanja; Welsh, Rory M.; Ishoey, Thomas; Lee, Jae-Hyeok; Binder, Brian J.; DuPont, Chris L.; Latasa, Mikel; Guigand, Cédric; Buck, Kurt R.; Hilton, Jason; Thiagarajan, Mathangi; Caler, Elisabet; Read, Betsy; Lasken, Roger S.; Chavez, Francisco P.; Worden, Alexandra Z.

doi:10.1073/pnas.1001665107

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Journal Article · Wed Jul 28 00:00:00 EDT 2010 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1001665107· OSTI ID:1051835

Cuvelier, Marie L. ^[1]; Allen, Andrew E. ^[2]; Monier, Adam ^[3]; McCrow, John P. ^[2]; Messié, Monique ^[3]; Tringe, Susannah G. ^[4]; Woyke, Tanja ^[4]; Welsh, Rory M. ^[3]; Ishoey, Thomas ^[2]; Lee, Jae-Hyeok ^[5]; Binder, Brian J. ^[6]; DuPont, Chris L. ^[2]; Latasa, Mikel ^[7]; Guigand, Cédric ^[8]; Buck, Kurt R. ^[3]; Hilton, Jason ^[8]; Thiagarajan, Mathangi ^[2]; Caler, Elisabet ^[2]; Read, Betsy ^[9]; Lasken, Roger S. ^[2] more »

Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039; Rosenstiel School of Marine and Atmospheric Science, Miami, FL 33149
J. Craig Venter Institute, San Diego, CA 92121
Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039
US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598
Department of Biology, Washington University, St. Louis, MO 63130
Department of Marine Sciences, University of Georgia, Athens, GA 36072
Institut de Ciències del Mar (CSIC), E-08003 Barcelona, Spain; and
Rosenstiel School of Marine and Atmospheric Science, Miami, FL 33149
Department of Biological Sciences, California State University, San Marcos, CA 92096

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 from only 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 pico-prymnesiophytes 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.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1051835

Alternate ID(s):: OSTI ID: 1153668

Report Number(s):: LBNL-5175E

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 33 Vol. 107; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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