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Major viral impact on the functioning of benthic deep-sea ecosystems

Nature volume 454, pages 1084–1087 (2008)Cite this article

Abstract

Viruses are the most abundant biological organisms of the world’s oceans. Viral infections are a substantial source of mortality in a range of organisms—including autotrophic and heterotrophic plankton—but their impact on the deep ocean and benthic biosphere is completely unknown. Here we report that viral production in deep-sea benthic ecosystems worldwide is extremely high, and that viral infections are responsible for the abatement of 80% of prokaryotic heterotrophic production. Virus-induced prokaryotic mortality increases with increasing water depth, and beneath a depth of 1,000 m nearly all of the prokaryotic heterotrophic production is transformed into organic detritus. The viral shunt, releasing on a global scale ∼0.37–0.63 gigatonnes of carbon per year, is an essential source of labile organic detritus in the deep-sea ecosystems. This process sustains a high prokaryotic biomass and provides an important contribution to prokaryotic metabolism, allowing the system to cope with the severe organic resource limitation of deep-sea ecosystems. Our results indicate that viruses have an important role in global biogeochemical cycles, in deep-sea metabolism and the overall functioning of the largest ecosystem of our biosphere.

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Figure 1: Bathymetric patterns of viruses and prokaryotes in deep-sea sediments worldwide.
Figure 2: Relationships between viruses and prokaryotes in deep-sea sediments worldwide.
Figure 3: Bathymetric patterns of virus-induced prokaryotic mortality.
Figure 4: Relationship between carbon released by viral lysis of prokaryotic biomass (viral shunt) and by prokaryotic turnover.

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Acknowledgements

This work was financially supported by the EU within the framework of the project HERMES. C.T. was supported by the ANR POTES.

Author Contributions R.D. performed the project planning; A.D., C.C., M.M. and C.T. performed the experimental work; R.D., A.D., C.C., M.M., R.N., C.T. and M.W. performed the data analysis; R.D., A.D., C.C., M.M., R.N., C.T. and M.W. wrote the manuscript.

Author information

Authors and Affiliations

  1. Department of Marine Science, Faculty of Science, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy,

    Roberto Danovaro, Antonio Dell’Anno, Cinzia Corinaldesi & Mirko Magagnini

  2. Institute of Marine Sciences, The University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, North Carolina 28557, USA ,

    Rachel Noble

  3. Université de la Méditerranée, Centre d'Océanologie de Marseille, UMR 6117–CNRS, Campus de Luminy, Case 901, 163 Avenue de Luminy, 13288 Marseille, Cedex 9, France,

    Christian Tamburini

  4. CNRS,

    Markus Weinbauer

  5. Microbial Ecology & Biogeochemistry Group, Laboratoire d’Océanographie de Villefranche, 06234 Villefranche-sur-Mer, France, Université Pierre et Marie Curie-Paris 6, Laboratoire d’Océanographie de Villefranche, 06234 Villefranche-sur-Mer, France

    Markus Weinbauer

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  1. Roberto Danovaro
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Corresponding author

Correspondence to Roberto Danovaro.

Supplementary information

Supplementary Information

The file contains Supplementary Methods; Supplementary Tables 1-4; Supplementary Figures 1-7; Supplementary Notes. The Supplementary Figure 1 provides information on sampling sites where sediments for microbiological determinations were collected. Supplementary figures 2-7 provide additional information on viral production estimated by using different methodologies, on the effect of mitomycin C on viral production and on the effect of pressure on viral and prokaryotic C production. (PDF 655 kb)

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Danovaro, R., Dell’Anno, A., Corinaldesi, C. et al. Major viral impact on the functioning of benthic deep-sea ecosystems. Nature 454, 1084–1087 (2008). https://doi.org/10.1038/nature07268

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