Edited by James L. Van Etten, University of Nebraska-Lincoln, Lincoln, NE, and approved March 16, 2015 (received for review November 21, 2014)
Viruses proliferate at the expense of their hosts. After cell death the released viruses can infect other hosts or undergo decomposition processes. Here we show, for the first time to our knowledge, that in deep-sea ecosystems, the largest biome of the biosphere, approximately 25% of viruses released by lysed prokaryotic cells are decomposed at fast rates. We show that, given the huge viral biomass of the ocean seafloor and the high rates of this process, virus decomposition provides a major source of labile organic compounds able to sustain the microbial food webs and nutrient cycling at a global scale. These findings provide new insights that will enable a better understanding of the functioning of the global oceans.
Viruses are key biological agents of prokaryotic mortality in the world oceans, particularly in deep-sea ecosystems where nearly all of the prokaryotic C production is transformed into organic detritus. However, the extent to which the decomposition of viral particles (i.e., organic material of viral origin) influences the functioning of benthic deep-sea ecosystems remains completely unknown. Here, using various independent approaches, we show that in deep-sea sediments an important fraction of viruses, once they are released by cell lysis, undergo fast decomposition. Virus decomposition rates in deep-sea sediments are high even at abyssal depths and are controlled primarily by the extracellular enzymatic activities that hydrolyze the proteins of the viral capsids. We estimate that on a global scale the decomposition of benthic viruses releases ∼37–50 megatons of C per year and thus represents an important source of labile organic compounds in deep-sea ecosystems. Organic material released from decomposed viruses is equivalent to 3 ± 1%, 6 ± 2%, and 12 ± 3% of the input of photosynthetically produced C, N, and P supplied through particles sinking to bathyal/abyssal sediments. Our data indicate that the decomposition of viruses provides an important, previously ignored contribution to deep-sea ecosystem functioning and has an important role in nutrient cycling within the largest ecosystem of the biosphere.
Author contributions: A.D., C.C., and R.D. designed research, performed research, analyzed data, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in MetaVir, metavir-meb.univ-bpclermont.fr, within the project EXPLODIVE.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1422234112/-/DCSupplemental.
Freely available online through the PNAS open access option.
