• A Corrigendum to this article was published on 24 August 2016

Abstract

Microbial viruses can control host abundances via density-dependent lytic predator–prey dynamics. Less clear is how temperate viruses, which coexist and replicate with their host, influence microbial communities. Here we show that virus-like particles are relatively less abundant at high host densities. This suggests suppressed lysis where established models predict lytic dynamics are favoured. Meta-analysis of published viral and microbial densities showed that this trend was widespread in diverse ecosystems ranging from soil to freshwater to human lungs. Experimental manipulations showed viral densities more consistent with temperate than lytic life cycles at increasing microbial abundance. An analysis of 24 coral reef viromes showed a relative increase in the abundance of hallmark genes encoded by temperate viruses with increased microbial abundance. Based on these four lines of evidence, we propose the Piggyback-the-Winner model wherein temperate dynamics become increasingly important in ecosystems with high microbial densities; thus ‘more microbes, fewer viruses’.

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Accessions

Data deposits

The viromes and microbiomes used in this paper are accessible at MG-RAST (http://metagenomics.anl.gov/) under the Piggyback-the-Winner project. Virome accession numbers: 4683670.3, 4683674.3, 4683677.3, 4683680.3, 4683683.3, 4683684.3, 4683686.3, 4683690.3, 4683702.3, 4683703.3, 4683704.3, 4683706.3, 4683712.3, 4683720.3, 4683739.3, 4683744.3, 4683745.3, 4683746.3, 4683747.3, 4683731.3, 4683733.3, 4683734.3, 4683718.3, 4684617.3. Microbiome accession numbers: 4683666.3, 4683667.3, 4683668.3, 4683669.3, 4683671.3, 4683672.3, 4683673.3, 4683675.3, 4683676.3, 4683678.3, 4683679.3, 4683681.3, 4683682.3, 4683685.3, 4683687.3, 4683688.3, 4683689.3, 4683691.3, 4683692.3, 4683693.3, 4683694.3, 4683695.3, 4683696.3, 4683697.3, 4683698.3, 4683699.3, 4683700.3, 4683701.3, 4683705.3, 4683707.3, 4683708.3, 4683709.3, 4683710.3, 4683711.3, 4683713.3, 4683714.3, 4683715.3, 4683716.3, 4683717.3, 4683719.3, 4683721.3, 4683722.3, 4683723.3, 4683724.3, 4683725.3, 4683726.3, 4683727.3, 4683728.3, 4683729.3, 4683732.3, 4683735.3, 4683736.3, 4683737.3, 4683738.3, 4683740.3, 4683741.3, 4683742.3, 4683743.3, 4683748.3, 4683749.3, 4683750.3, 4683751.3, 4683752.3, 4683753.3, 4683754.3, 4684616.3.

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Acknowledgements

This paper is dedicated to the memory of Mike Furlan, mentor, friend, and colleague. We are grateful to the National Oceanographic and Atmospheric Administration Coral Reef Ecosystem Division for supporting this research, and to the captains and crews of the NOAA ship Hi’ialakai and the Hanse Explorer. Thanks to J. Payet for providing viral and microbial abundance data. Sampling was carried out under research permits from the US Fish and Wildlife Service, Palmyra Atoll National Wildlife Refuge, the Environment and Conservation Division of the Republic of Kiribati (n. 021/13) and ICMBio, Brazil (n. 27147-2). This work was funded by the Canadian Institute for Advanced Research Integrated Microbial Biodiversity Program Fellowship Award 141679 (to F.R.) and National Science Foundation grants OISE-1243541 and DEB-1046413 (to F.R.), CNS-1305112 and MCB-1330800 (to R.A.E.), DUE-1323809 (to E.A.D.), Gordon and Betty Moore Foundation Investigator Award GBMF-3781 (to F.R.), and the Brazilian National Research Council (CNPq; to F.T.) and Brazilian National Research Council Science Without Borders Program (CNPq/CAPES; to C.B.S.).

Author information

Author notes

    • B. Knowles
    •  & C. B. Silveira

    These authors contributed equally to this work.

Affiliations

  1. Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, California 92182, USA

    • B. Knowles
    • , C. B. Silveira
    • , A. G. Cobián-Güemes
    • , E. A. Dinsdale
    • , E. E. George
    • , K. T. Green
    • , A. F. Haas
    • , J. M. Haggerty
    • , E. R. Hester
    • , N. Hisakawa
    • , L. W. Kelly
    • , Y. W. Lim
    • , M. Little
    • , S. D. Quistad
    • , N. L. Robinett
    • , S. E. Sanchez
    •  & F. Rohwer
  2. Biology Institute, Rio de Janeiro Federal University, Av. Carlos Chagas Filho 373, Rio de Janeiro, Rio de Janeiro 21941-599, Brazil

    • C. B. Silveira
    • , F. H. Coutinho
    • , L. S. de Oliveira
    • , C. Thompson
    •  & F. Thompson
  3. Department of Mathematics and Statistics, San Diego State University, 5500 Campanile Drive, San Diego, California 92182, USA

    • B. A. Bailey
    • , B. Felts
    • , A. Luque
    • , P. Salamon
    •  & J. Nulton
  4. Hawaii Institute of Marine Biology, University of Hawaii at Manoa, 46-007 Lilipuna Road, Kaneohe, Hawaii 96744, USA

    • K. Barott
  5. Computational Science Research Center, San Diego State University, 5500 Campanile Drive, San Diego, California 92182, USA

    • V. A. Cantu
    • , A. Luque
    • , K. McNair
    • , G. G. Z. Silva
    •  & R. A. Edwards
  6. Radboud University Medical Centre, Radboud Institute for Molecular Life Sciences, Centre for Molecular and Biomolecular Informatics, 6525HP Nijmegen, The Netherlands

    • K. A. Furby
    • , T. McDole-Somera
    • , S. Sandin
    • , J. Smith
    •  & B. Zgliczynski
  7. Viral Information Institute, San Diego State University, 5500 Campanile Drive, San Diego, California 92182, USA

    • G. B. Gregoracci
  8. Scripps Institution of Oceanography, 8622 Kennel Way, La Jolla, California 92037, USA

    • E. Sala
  9. Marine Sciences Department, Sao Paulo Federal University - Baixada Santista, Av. Alm. Saldanha da Gama, 89, Santos, São Paulo 11030-400, Brazil

    • C. Sullivan
  10. National Geographic Society, 1145 17th St NW, Washington D.C. 20036, USA

    • M. J. A. Vermeij
  11. Department of Biology, University of California San Diego, 9500 Gilman Drive, La Jolla, California 92093, USA

    • P. Salamon
    • , M. J. A. Vermeij
    •  & F. Rohwer
  12. CARMABI Foundation, Piscaderabaai z/n, Willemstad, Curacao, Netherlands Antilles

    • M. Youle
  13. Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1098XH Amsterdam, The Netherlands

    • C. Young
    •  & R. Brainard
  14. Rainbow Rock, Ocean View, Hawaii 96737, USA

    • F. H. Coutinho
    • , E. A. Dinsdale
    •  & R. A. Edwards
  15. Coral Reef Ecosystem Division-PIFSC-NOAA, 1845 Wasp Blvd, Honolulu, Hawaii 96818, USA

  16. Department of Computer Science, San Diego State University, 5500 Campanile Drive, San Diego, California 92182, USA

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Contributions

F.R., B.K., C.B.S., and F.T. conceptualized the project; B.K., F.R., C.B.S., and M.Y. wrote the manuscript; B.K., C.B.S., V.A.C., A.G.C.-G., K.T.G, K.M., G.G.Z.S., S.D.Q., Y.W.L., S.E.S., F.H.C., E.R.H. , N.L.R., B.A.B., B.F., A.L., P.S., J.N., C.Y., E.E.G., M.L., K.A.F., L.S.O., T.M.-S., J.M.H., B.Z., A.F.H., M.J.A.V., K.B., C.S., R.A.E., and F.R. performed sample collection, processing, experiments, and analysis; N.H. provided graphics and GIS analysis; E.A.D., L.W.K., S.S., J.S., R.B., C.T., G.B.G., J.N., E.S., R.A.E., F.T., and F.R. provided intellectual guidance and funding during the development of the research.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to B. Knowles or F. Rohwer.

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https://doi.org/10.1038/nature17193

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