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Abundant SAR11 viruses in the ocean

Abstract

Several reports proposed that the extraordinary dominance of the SAR11 bacterial clade in ocean ecosystems could be a consequence of unusual mechanisms of resistance to bacteriophage infection, including ‘cryptic escape’ through reduced cell size1 and/or K-strategist defence specialism2. Alternatively, the evolution of high surface-to-volume ratios coupled with minimal genomes containing high-affinity transporters enables unusually efficient metabolism for oxidizing dissolved organic matter in the world’s oceans that could support vast population sizes despite phage susceptibility. These ideas are important for understanding plankton ecology because they emphasize the potentially important role of top-down mechanisms in predation, thus determining the size of SAR11 populations and their concomitant role in biogeochemical cycling. Here we report the isolation of diverse SAR11 viruses belonging to two virus families in culture, for which we propose the name ‘pelagiphage’, after their host. Notably, the pelagiphage genomes were highly represented in marine viral metagenomes, demonstrating their importance in nature. One of the new phages, HTVC010P, represents a new podovirus subfamily more abundant than any seen previously, in all data sets tested, and may represent one of the most abundant virus subfamilies in the biosphere. This discovery disproves the theory that SAR11 cells are immune to viral predation and is consistent with the interpretation that the success of this highly abundant microbial clade is the result of successfully evolved adaptation to resource competition.

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Figure 1: Transmission electron microscopy images of isolated pelagiphages.
Figure 2: Phylogenetic analysis of the pelagiphages.
Figure 3: Abundance of pelagiphage relative to representative cyanophages and roseophage SIO1.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Viral genome sequences and annotations have been deposited at GenBank/EMBL/DDBJ under accession codes: KC465898 (HTVC10P), KC465899 (HTVC008M), KC465900 (HTVC011P) and KC465901 (HTVC019P). Scripts and data used to generate the figures in this manuscript are available at http://giovannonilab.science.oregonstate.edu/publications.

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Acknowledgements

We thank the Tucson Marine Phage Lab and B. Hurwitz for early access to the Pacific Ocean virome datasets and J. Yan for her assistance in isolating HTVC011P. This work was supported by an investigator award to S.J.G. from the Gordon and Betty Moore Foundation Marine Microbiology Initiative.

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Affiliations

Authors

Contributions

Y.Z. isolated phages and performed genome sequencing and annotation; B.T. designed and implemented metagenomic bioinformatic analyses and prepared the manuscript; J.C.T. performed phylogenetic and metagenomic analyses; M.S.S. began the project and isolated the first virus, HTVC011P; Y.Z., M.E. and T.D. performed transmission electron microscopy; K.L.V. sequenced the HTVC011P genome; Z.C.L. assembled and annotated the viral genomes. M.B.S. and S.J.G. gave technical support and conceptual advice. S.J.G. assisted in writing the manuscript.

Corresponding author

Correspondence to Stephen J. Giovannoni.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-11, Supplementary Methods, Supplementary Tables 1-3 and Supplementary References. (PDF 6255 kb)

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Zhao, Y., Temperton, B., Thrash, J. et al. Abundant SAR11 viruses in the ocean. Nature 494, 357–360 (2013). https://doi.org/10.1038/nature11921

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