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

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.

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Correspondence to Roberto Danovaro.

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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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