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The elemental composition of virus particles: implications for marine biogeochemical cycles

Key Points

  • Virus-mediated lysis of host cells results in the generation of dissolved organic carbon (DOC), dissolved organic nitrogen (DON) and dissolved organic phosphorus (DOP) via a process that is known as the 'viral shunt'.

  • Previous quantitative estimates of the contribution of the viral shunt to biogeochemical cycles focused on host cellular constituents and overlooked the contribution of virus particles.

  • In this Analysis article, we develop a biophysical scaling model that predicts the elemental contents and compositions of virus particles.

  • This scaling model was validated using detailed sequence and structural contents of intact bacteriophage particles.

  • Viruses are predicted to be enriched in phosphorus, so much so that the total phosphorus content in a burst of released viruses may approach that of the phosphorus content in an uninfected host.

  • As a consequence, cellular debris may be depleted in phosphorus compared with the stoichiometry of hosts.

  • Furthermore, by extrapolating the model to the ecosystem scale, marine viruses are predicted to contain an important fraction (for example, >5%) of the total DOP pool in some systems (for example, in surface waters, when virus density exceeds 3.5 × 1010 and the DOP concentration is approximately 100 nM).

Abstract

In marine environments, virus-mediated lysis of host cells leads to the release of cellular carbon and nutrients and is hypothesized to be a major driver of carbon recycling on a global scale. However, efforts to characterize the effects of viruses on nutrient cycles have overlooked the geochemical potential of the virus particles themselves, particularly with respect to their phosphorus content. In this Analysis article, we use a biophysical scaling model of intact virus particles that has been validated using sequence and structural information to quantify differences in the elemental stoichiometry of marine viruses compared with their microbial hosts. By extrapolating particle-scale estimates to the ecosystem scale, we propose that, under certain circumstances, marine virus populations could make an important contribution to the reservoir and cycling of oceanic phosphorus.

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Figure 1: Schematic of the viral shunt.
Figure 2: Model of the elemental stoichiometry of virus particles.
Figure 3: Theoretical prediction of elemental stoichiometry for viruses.
Figure 4: Virus-induced transformation of elemental content in cellular debris following lysis.
Figure 5: Predicted DOP concentration in viral populations as a function of viral density and virus size.

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Accessions

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Acknowledgements

This work was supported by US National Science Foundation (NSF) grants OCE-1233760 (to J.S.W.) and OCE-1061352 (to A.B. and S.W.W.). This work was assisted by attendance as a short-term visitor (J.S.W.) and participation (A.B., S.W.W. and J.S.W.) in the Ocean Viral Dynamics working group at the US National Institute for Mathematical and Biological Synthesis — an Institute that is sponsored by the NSF, the US Department of Homeland Security and the US Department of Agriculture through NSF Award EF-0832858, with additional support from The University of Tennessee, Knoxville, USA. J.S.W. holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. The authors thank participants of the Ocean Viral Dynamics working group, M. Sullivan, J. Brum and three anonymous referees for their feedback and suggestions.

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Correspondence to Joshua S. Weitz.

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Supplementary information

Supplementary information S1 (box)

Parameters and ranges used in the theory of viral elemental stoichoimetry (PDF 1733 kb)

Supplementary information S2 (table)

Phage capsid size and genome length calibration data set (XLSX 12 kb)

Supplementary information S3 (table)

Phage genome length data set (XLSX 49 kb)

Supplementary information S4 (table)

Viral protein data set (XLSX 660 kb)

Glossary

Dissolved organic matter

(DOM). Operationally defined as marine organic matter that passes through a filter with pores of 0.22 μm to 0.45 μm in diameter. DOM can be further classified on the basis of biological availability.

Particulate organic matter

(POM). Operationally defined as the material in a marine environment that is retained by a filter with pores of 0.22 μm to 0.45 μm in diameter.

Heterotrophic bacteria

Bacteria that use organic carbon compounds to satisfy nutritional requirements.

Cyanobacteria

Ubiquitous marine bacteria that fix inorganic carbon compounds into organic carbon compounds.

Quantitative transmission electron microscopy

(qTEM). Method to quantitatively estimate viral morphological characteristics (such as morphotype, capsid diameter and tail length) using transmission electron microscopy.

Oligotrophic

A term used to describe an aquatic environment that has low levels of nutrients and photosynthetic production (for example, the open ocean).

Spring blooms

Annual increases in phytoplankton abundance in response to seasonal changes, such as increased temperature and higher nutrient levels.

Gene-transfer agents

Phage-like particles that encapsulate cellular DNA that can be transferred to another bacterium.

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Jover, L., Effler, T., Buchan, A. et al. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat Rev Microbiol 12, 519–528 (2014). https://doi.org/10.1038/nrmicro3289

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