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Abundant SAR11 viruses in the ocean


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


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


  1. 1

    Yooseph, S. et al. Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468, 60–66 (2010)

    CAS  ADS  Article  Google Scholar 

  2. 2

    Suttle, C. A. Marine viruses — major players in the global ecosystem. Nature Rev. Microbiol. 5, 801–812 (2007)

    CAS  Article  Google Scholar 

  3. 3

    Nagasaki, K. & Bratbak, G. In Manual of Aquatic Viral Ecology Limnol . Oceanogr. 92–101 (2010)

  4. 4

    Lavigne, R., Seto, D., Mahadevan, P., Ackermann, H.-W. & Kropinski, A. M. Unifying classical and molecular taxonomic classification: analysis of the Podoviridae using BLASTP-based tools. Res. Microbiol. 159, 406–414 (2008)

    CAS  Article  Google Scholar 

  5. 5

    Ignacio-Espinoza, J. C. & Sullivan, M. B. Phylogenomics of T4 cyanophages: lateral gene transfer in the ‘core’ and origins of host genes. Environ. Microbiol. 14, 2113–2126 (2012)

    CAS  Article  Google Scholar 

  6. 6

    Hurwitz, B. L. & Sullivan, M. B. The Pacific Ocean virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS ONE (in the press). (2013)

  7. 7

    Duhaime, M. B., Deng, L., Poulos, B. T. & Sullivan, M. B. Towards quantitative metagenomics of wild viruses and other ultra-low concentration DNA samples: a rigorous assessment and optimization of the linker amplification method. Environ. Microbiol. 14, 2526–2537 (2012)

    CAS  Article  Google Scholar 

  8. 8

    Angly, F. E. et al. The marine viromes of four oceanic regions. PLoS Biol. 4, e368 (2006)

    Article  Google Scholar 

  9. 9

    López-Bueno, A. et al. High diversity of the viral community from an Antarctic lake. Science 326, 858–861 (2009)

    ADS  Article  Google Scholar 

  10. 10

    Ghai, R. et al. Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing. ISME J. 4, 1154–1166 (2010)

    CAS  Article  Google Scholar 

  11. 11

    Wilhelm, L. J., Tripp, H. J., Givan, S. A., Smith, D. P. & Giovannoni, S. J. Natural variation in SAR11 marine bacterioplankton genomes inferred from metagenomic data. Biol. Direct 2, 27 (2007)

    Article  Google Scholar 

  12. 12

    Grote, J. et al. Streamlining and core genome conservation among highly divergent members of the SAR11 clade. mBio 3, (2012)

  13. 13

    Rodriguez-Valera, F. et al. Explaining microbial population genomics through phage predation. Nature Rev. Microbiol. 7, 828–836 (2009)

    CAS  Article  Google Scholar 

  14. 14

    Avrani, S., Wurtzel, O., Sharon, I., Sorek, R. & Lindell, D. Genomic island variability facilitates Prochlorococcus–virus coexistence. Nature 474, 604–608 (2011)

    CAS  Article  Google Scholar 

  15. 15

    Wang, L. et al. DNA phosphorothioation is widespread and quantized in bacterial genomes. Proc. Natl Acad. Sci. USA 108, 2963–2968 (2011)

    CAS  ADS  Article  Google Scholar 

  16. 16

    Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997)

    Article  Google Scholar 

  17. 17

    Chow, C.-E. T. & Fuhrman, J. A. Seasonality and monthly dynamics of marine myovirus communities. Environ. Microbiol. 14, 2171–2183 (2012)

    Article  Google Scholar 

  18. 18

    Marston, M. F. et al. Rapid diversification of coevolving marine Synechococcus and a virus. Proc. Natl Acad. Sci. USA 109, 4544–4549 (2012)

    CAS  ADS  Article  Google Scholar 

  19. 19

    Fuhrman, J. A. & Schwalbach, M. Viral influence on aquatic bacterial communities. Biol. Bull. 204, 192–195 (2003)

    CAS  Article  Google Scholar 

  20. 20

    Parsons, R. J., Breitbart, M., Lomas, M. W. & Carlson, C. A. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273–284 (2012)

    CAS  Article  Google Scholar 

  21. 21

    Rappé, M. S., Connon, S. A., Vergin, K. L. & Giovannoni, S. J. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418, 630–633 (2002)

    ADS  Article  Google Scholar 

  22. 22

    Sullivan, M. B., Waterbury, J. B. & Chisholm, S. W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus . Nature 424, 1047–1051 (2003)

    CAS  ADS  Article  Google Scholar 

  23. 23

    Sullivan, M. B., Coleman, M., Weigele, P., Rohwer, F. & Chisholm, S. W. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 3, e144 (2005)

    Article  Google Scholar 

  24. 24

    Sullivan, M. B. et al. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. Environ. Microbiol. 11, 2935–2951 (2009)

    CAS  Article  Google Scholar 

  25. 25

    Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010)

    CAS  Article  Google Scholar 

  26. 26

    Malmstrom, R. R., Cottrell, M. T., Elifantz, H. & Kirchman, D. L. Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean. Appl. Environ. Microbiol. 71, 2979–2986 (2005)

    CAS  Article  Google Scholar 

  27. 27

    Kunin, V. et al. A bacterial metapopulation adapts locally to phage predation despite global dispersal. Genome Res. 18, 293–297 (2008)

    CAS  Article  Google Scholar 

  28. 28

    Vergin, K. L. et al. High intraspecific recombination rate in a native population of Candidatus Pelagibacter ubique (SAR11). Environ. Microbiol. 9, 2430–2440 (2007)

    CAS  Article  Google Scholar 

  29. 29

    Vos, M. & Didelot, X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3, 199–208 (2009)

    CAS  Article  Google Scholar 

  30. 30

    Van Valen, L. A new evolutionary law. Evol. Theory 1, 1–30 (1973)

    Google Scholar 

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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.

Author information




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).

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