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PMID: 20668244 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 107 ·No. 33 ·2010-08-17 ·Pages 14679-84

Cuvelier ML, Allen AE, Monier A, McCrow JP, Messié M, Tringe SG, Woyke T, Welsh RM, Ishoey T, Lee JH, Binder BJ, DuPont CL, Latasa M, Guigand C, Buck KR, Hilton J, Thiagarajan M, Caler E, Read B, Lasken RS, Chavez FP, Worden AZ

Abstract

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.

MeSH Terms

Amino Acid Sequence Biomass Ecosystem Eukaryota/classification,genetics,growth & development Evolution, Molecular Florida Geography Metagenome/genetics Metagenomics/methods Molecular Sequence Data Oceans and Seas Phylogeny Phytoplankton/classification,genetics,growth & development RNA, Ribosomal, 16S/genetics RNA, Ribosomal, 18S/genetics Seasons Sequence Homology, Amino Acid Temperature

Chemicals

RNA, Ribosomal, 16S RNA, Ribosomal, 18S

Authors & Affiliations

22 authors, click to expand affiliations / ORCID

Cuvelier Marie L

Monterey Bay Aquarium Research Institute, Moss Landing, CA 95039, USA.

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

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Article Info

Journal

Proceedings of the National Academy of Sciences of the United States of America

Abbr.

Proc Natl Acad Sci U S A

ISSN

1091-6490

DOI

10.1073/pnas.1001665107

Published

2010-08-17

Epub

2010-00-28

Pages

14679-84

Language

English

Region

United States

NLM ID

7505876

PMCID

PMC2930470

Subset

Databases

GENBANK

HM565909, HM565910, HM565911, HM565912, HM565913, HM565914, HM581528, HM581529, HM581530, HM581531, HM581532, HM581533, HM581534, HM581535, HM581536, HM581537, HM581538, HM581539, HM581540, HM581541, HM581542, HM581543, HM581544, HM581545, HM581546, HM581547, HM581548, HM581549, HM581550, HM581551, HM581552, HM581553, HM581554, HM581555, HM581556, HM581557, HM581558, HM581559, HM581560, HM581561, HM581562, HM581563, HM581564, HM581565, HM581566, HM581567, HM581568, HM581569, HM581570, HM581571, HM581572, HM581573, HM581574, HM581575, HM581576, HM581577, HM581578, HM581579, HM581580, HM581581, HM581582, HM581583, HM581584, HM581585, HM581586, HM581587, HM581588, HM581589, HM581590, HM581591, HM581592, HM581593, HM581594, HM581595, HM581596, HM581597, HM581598, HM581599, HM581600, HM581601, HM581602, HM581603, HM581604, HM581605, HM581606, HM581607, HM581608, HM581609, HM581610, HM581611, HM581612, HM581613, HM581614, HM581615, HM581616, HM581617, HM581618, HM581619, HM581620, HM581621, HM581622, HM581623, HM581624, HM581625, HM581626, HM581627, HM581628, HM581629, HM581630, HM581631, HM581632, HM581633, HM581634, HM581635, HM581636, HM581637, HM581638

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PubMed source DOI: 10.1073/pnas.1001665107 PMC Full Text View journal details

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