Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton.

Cuvelier, M. L., Allen, A. E., Monier, A., McCrow, J. P., Messié, M., Tringe, S. G., Woyke, T., Welsh, R. M., Ishoey, T., Lee, J.-H., Binder, B. J., DuPont, C. L., Latasa, M., Guigand, C., Buck, K. R., Hilton, J., Thiagarajan, M., Caler, E., Read, B., Lasken, R. S., Chavez, F. P. and Worden, Alexandra Z. (2010) Targeted metagenomics and ecology of globally important uncultured eukaryotic phytoplankton. Open Access Proceedings of the National Academy of Sciences of the United States of America (PNAS), 107 (33). pp. 14679-14684. DOI 10.1073/pnas.1001665107.

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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, 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.

Document Type: Article
Keywords: iron; nickel; RNA 18S; superoxide dismutase; RNA 16S, article; biogeographic region; biomass; ecology; eukaryotic spore; flow cytometry; genetic analysis; growth rate; Haptophyta; metagenomics; nonhuman; North Atlantic deep water; nucleotide sequence; nutrient uptake; phytoplankton; plastid genome; Prasinophyceae; priority journal; Prochlorococcus; stramenopile; amino acid sequence; classification; ecosystem; eukaryote; genetics; geography; growth, development and aging; metagenome; methodology; molecular evolution; molecular genetics; phylogeny; sea; season; sequence homology; temperature; United States, Alveolata; Eukaryota; Haptophyceae; Prasinophyceae; Prochlorococcus; stramenopiles, Amino Acid Sequence; Biomass; Ecosystem; Eukaryota; Evolution, Molecular; Florida; Geography; Metagenome; Metagenomics; Molecular Sequence Data; Oceans and Seas; Phylogeny; Phytoplankton; RNA, Ribosomal, 16S; RNA, Ribosomal, 18S; Seasons; Sequence Homology, Amino Acid; Temperature
Research affiliation: OceanRep > GEOMAR > FB3 Marine Ecology > FB3-EOE-N Experimental Ecology - Food Webs
Refereed: Yes
Open Access Journal?: No
DOI etc.: 10.1073/pnas.1001665107
ISSN: 0027-8424
Date Deposited: 06 Mar 2019 11:11
Last Modified: 06 Mar 2019 11:11
URI: http://oceanrep.geomar.de/id/eprint/46045

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