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PNAS
Vol. 107, No. 33, 2010, Pages: 14679–14684


Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton

Marie L. Cuveliera,b, Andrew E. Allenc,1, Adam Moniera,1, John P. McCrowc, Monique Messiéa, Susannah G. Tringed,
Tanja Woyked, Rory M. Welsha, Thomas Ishoeyc, Jae-Hyeok Leee, Brian J. Binderf, Chris L. DuPontc, Mikel Latasag,
Cédric Guigandb, Kurt R. Bucka, Jason Hiltonb, Mathangi Thiagarajanc, Elisabet Calerc, Betsy Readh, Roger S. Laskenc, Francisco P. Chaveza, and Alexandra Z. Wordena,b,2

1Departamento de Ingeniería y Ciencia de los Materiales, Escuela Técnica Superior de Ingenieros Industriales, Universidad Politécnica de Madrid (UPM), José Gutiérrez Abascal 2, 28006 Madrid, Spain.

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
fromonly 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 picoprymnesiophytes 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, picoprymnesiophytes 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.

Keywords:comparative genomics, primary production, prymnesiophytes, marine photosynthesis, haptophytes,taxonomy.


Corresponding author:

E-mail: azworden@mbari.org

 

 
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