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Re-examination of the relationship between marine virus and microbial cell abundances

Nature Microbiology volume 1, Article number: 15024 (2016) Cite this article

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An Author Correction to this article was published on 03 October 2017

This article has been updated

Abstract

Marine viruses are critical drivers of ocean biogeochemistry, and their abundances vary spatiotemporally in the global oceans, with upper estimates exceeding 108 per ml. Over many years, a consensus has emerged that virus abundances are typically tenfold higher than microbial cell abundances. However, the true explanatory power of a linear relationship and its robustness across diverse ocean environments is unclear. Here, we compile 5,508 microbial cell and virus abundance estimates from 22 distinct marine surveys and find substantial variation in the virus-to-microbial cell ratio, in which a 10:1 model has either limited or no explanatory power. Instead, virus abundances are better described as nonlinear, power-law functions of microbial cell abundances. The fitted scaling exponents are typically less than 1, implying that the virus-to-microbial cell ratio decreases with microbial cell density, rather than remaining fixed. The observed scaling also implies that viral effect sizes derived from ‘representative’ abundances require substantial refinement to be extrapolated to regional or global scales.

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Figure 1: Global distribution and information regarding sample sites.
Figure 2: Variation in virus and microbial abundances and the VMR.
Figure 3: Virus abundance is poorly fit by a model of a tenfold increase relative to microbial abundance.
Figure 4: Virus–microbial relationships given the variable slope and intercept mixed-effects model.
Figure 5: Study-specific 95% confidence intervals of power-law exponents for relationships between virus and microbial abundances in the surface.

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Change history

  • 03 October 2017

    The original publication of this Article included analysis of virus and microbial cell abundances and virus-to-microbial cell ratios. Data in the Article came from 25 studies intended to be exclusively from marine sites. However, 3 of the studies included in the original unified dataset were erroneously classified as marine sites during compilation. The records with mis-recorded longitude and latitude values were, in fact, taken from inland, freshwater sources. The three inland, freshwater datasets are ELA, TROUT and SWAT. The data from these three studies represent 163 of the 5,671 records in the original publication. In the updated version of the Article, all analyses have been recalculated using the same statistical analysis pipeline released via GitHub as part of the original publication. Removal of the three studies reduces the unified dataset to 5,508 records. Analyses involving all grouped datasets have been updated with changes noted in each figure. All key results remain qualitatively unchanged. All data and scripts used in this correction have been made available as a new, updated GitHub release to reflect the updated dataset and figures.

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Acknowledgements

This work was supported by National Science Foundation (NSF) grants OCE-1233760 (to J.S.W.) and OCE-1061352 (to A.B. and S.W.W.), a Career Award at the Scientific Interface from the Burroughs Wellcome Fund (to J.S.W.) and a Simons Foundation SCOPE grant (to J.S.W.). This work was conducted as part of the Ocean Viral Dynamics Working Group at the National Institute for Mathematical and Biological Synthesis, sponsored by the National Science Foundation through NSF Award DBI-1300426, with additional support from The University of Tennessee, Knoxville.

Author information

Authors and Affiliations

  1. School of Biology, Georgia Institute of Technology, Atlanta, 30332, Georgia, USA

    Charles H. Wigington & Joshua S. Weitz

  2. Department of Mathematics and Statistics, Northern Arizona University, Flagstaff, 86011, Arizona, USA

    Derek Sonderegger

  3. Department of Biological Oceanography, Royal Netherlands Institute for Sea Research (NIOZ), 1790 AB Den Burg, Texel, The Netherlands

    Corina P. D. Brussaard

  4. Department of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, 1090 GE, Amsterdam, The Netherlands

    Corina P. D. Brussaard

  5. Department of Microbiology, The University of Tennessee, Knoxville, 37996, Tennessee, USA

    Alison Buchan & Steven W. Wilhelm

  6. Department of Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Jan F. Finke & Curtis A. Suttle

  7. Department of Biological Sciences, University of Southern California, Los Angeles, 90089, California, USA

    Jed A. Fuhrman

  8. Department of Biology, Indiana University, Bloomington, 47405, Indiana, USA

    Jay T. Lennon

  9. Department of Biology, Marine Biological Section, University of Copenhagen, DK-3000, Helsingør, Denmark

    Mathias Middelboe

  10. Department of Microbiology and Immunology, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Curtis A. Suttle

  11. Department of Botany, University of British Columbia, Vancouver, V6T 1Z4, British Columbia, Canada

    Curtis A. Suttle

  12. Program in Integrated Microbial Diversity, Canadian Institute for Advanced Research, Toronto, M5G 1Z8, Ontario, Canada

    Curtis A. Suttle

  13. Geophysical Fluid Dynamics Laboratory, Princeton, 08540, New Jersey, USA

    Charles Stock

  14. Sir Alister Hardy Foundation for Ocean Science, The Laboratory, Citadel Hill, PL1 2PB, Plymouth, UK

    William H. Wilson

  15. Plant and Soil Sciences, Delaware Biotechnology Institute, Delaware Technology Park, Newark, 19711, Delaware, USA

    K. Eric Wommack

  16. School of Physics, Georgia Institute of Technology, Atlanta, 30332, Georgia, USA

    Joshua S. Weitz

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  1. Charles H. Wigington
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Contributions

C.H.W. developed the code and implemented all scripts, analysed data, performed statistical analysis and contributed to writing the manuscript. D.S. developed and reviewed the code, analysed data, performed statistical analysis and provided feedback on the manuscript. A.B., J.F., J.T.L., M.M., C.A.S., C.S., W.H.W. and K.E.W. contributed to the design and implementation of the study, the assessment and collection of data sets, and provided feedback on the manuscript. C.P.D.B. and J.F.F. contributed to the assessment and collection of data sets and provided feedback on the manuscript. S.W.W. co-led the design of the study, led the data collection and assessment component, and contributed to writing the manuscript. J.S.W. co-led the design of the study, led the code and statistical analysis component, and wrote the manuscript.

Corresponding authors

Correspondence to Steven W. Wilhelm or Joshua S. Weitz.

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Wigington, C., Sonderegger, D., Brussaard, C. et al. Re-examination of the relationship between marine virus and microbial cell abundances. Nat Microbiol 1, 15024 (2016). https://doi.org/10.1038/nmicrobiol.2015.24

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