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).
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.
Subscribe to Journal
Get full journal access for 1 year
only $22.08 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788 (1999). This report estimates the contribution of virus-mediated lysis of marine bacteria and algae to the biogeochemical cycling of carbon, in the process of defining the 'viral shunt'.
Brussaard, C. P. D. et al. Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J. 2, 575–578 (2008).
Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999). This paper gives a foundational perspective on the roles of viruses in ecosystems and proposes estimates for the changes in carbon fluxes between ecosystem pools in aquatic food webs owing to virus-mediated lysis.
Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Rev. Microbiol. 8, 593–599 (2010). This review discusses the production of recalcitrant carbon in marine systems and includes the viral shunt as a central component of the hypothesized production process.
Suttle, C. A. Marine viruses — major players in the global ecosystem. Nature Rev. Microbiol. 5, 801–812 (2007).
Gobler, C. J. et al. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine Chrysophyte. Limnol. Oceanogr. 42, 1492–1504 (1997).
Middelboe, M., Jørgensen, N. O. G. & Kroer, N. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl. Environ. Microbiol. 62, 1991–1997 (1996).
Noble, R. T., Middelboe, M. & Fuhrman, J. A. The effects of viral enrichment on the mortality and growth of heterotrophic bacterioplankton. Aquat. Microb. Ecol. 18, 1–13 (1999).
Suttle, C. A. Viruses in the Sea. Nature 437, 356–361 (2005). This paper provides the first global-scale diagram of the carbon cycle that includes marine viruses as an important component.
Steward, G. F. et al. Microbial biomass and viral infections of heterotrophic prokaryotes in the sub-surface layer of the central Arctic Ocean. Deep-Sea Res. I 54, 1744–1757 (2007).
Steward, G. F., Montiel, J. L. & Azam, F. Genome size distributions indicate variability and similarities among marine viral assemblages from diverse environments. Limnol. Oceanogr. 45, 1697–1706 (2000).
Bertilsson, S. et al. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003). This paper describes how phosphorus limitation shifts the subsequent elemental composition of marine cyanobacteria grown in culture.
Simon, M. & Azam, F. Protein content and protein synthesis rates of planktonic marine bacteria. Mar. Ecol. Prog. Ser. 51, 201–213 (1989). This paper shows that viruses in nutrient-limited environments are predominantly synthesized from elemental pools that are already available in host cells (for example, recycled nucleotides).
Redfield, A. C. Ketchum, B. H., & Richards, F. A. in The composition of seawater. Comparative and descriptive oceanography. The sea: ideas and observations on progress in the study of the seas. (Ed. Hill, M. N.) Vol. 2, 26–77 (Interscience Publishers, 1963).
Jiao, N. et al. The microbial carbon pump and the oceanic recalcitrant dissolved organic matter pool. Nature Rev. Microbiol. 9, 555 (2011).
Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. (Princeton University Press, 2002).
Iyer, L. M., Aravind, L. & Koonin, E. V. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75, 11720–11734 (2001).
Espejo, R. T. & Canelo, E. S. Properties of bacteriophage PM2: a lipid-containing bacterial virus. Virology 34, 738–747 (1968).
Bamford, D. H. et al. Constituents of SH1, a novel lipid-containing virus infecting the halophilic euryarchaeon Haloarcula hispanica. J. Virol. 79, 9097–9107 (2005).
Clasen, J. L. & Elser, J. J. The effect of host Chlorella NC64A carbon: phosphorus ratio on the production of Paramecium bursaria Chlorella Virus 1. Freshw. Biol. 52, 112–122 (2008). This study shows how virus productivity during infections decreases with decreasing host quality, and tabulates the total elemental content of a single algal virus.
Calendar, R. & Abedon S. T. The Bacteriophages (Oxford University Press, 2005).
Weitz, J. S. & Wilhelm, S. W. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol. Rep. 4, 17 (2012).
Scanlan, D. J. et al. An immunological approach to detect phosphate stress in populations and single cells of photosynthetic picoplankton. Appl. Environ. Microbiol. 63, 2411–2420 (1997).
Sullivan, M. B. et al. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biology 3, e144 (2005).
Sullivan, M. B. et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4 like myoviruses from diverse hosts and environments. Environ. Microbiol. 12, 3035–3056 (2010).
Zeng, Q. & Chisholm, S. W. Marine viruses exploit their host's two-component regulatory system in response to resource limitation. Curr. Biol. 22, 124–128 (2012).
Wikner, J. et al. Nucleic acids from the host bacterium as a major source of nucleotides for three marine bacteriophages. FEMS Microbiol. Ecol. 12, 237–248 (1993).
Wilson, W. H., Carr, N. G. & Mann, N. H. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. Wh78031. J. Phycol. 32, 506–516 (1996).
Cohen, S. S. The synthesis of nucleic acid by virus-infected bacteria. Bacteriol. Rev. 15, 131–146 (1951).
Kozloff, L. M. & Putnam, F. W. Biochemical studies of virus reproduction: III. The origin of virus phosphorus in the Eschericia coli T6 bacteriophage system. J. Biol. Chem. 182, 229–243 (1950).
Middelboe, M. et al. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat. Microb. Ecol. 33, 1–10 (2003).
Shelford, E. J. et al. Virus-driven nitrogen cycling enhances phytoplankton growth. Aquat. Microb. Ecol. 66, 41–46 (2012).
Poorvin, L. et al. Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr. 49, 1734–1741 (2004).
Zhao, Y. et al. Abundant SAR11 viruses in the ocean. Nature 494, 357–360 (2013). This paper provides the first description of viruses that infect pelagibacteria spp., which are the most abundant heterotrophic bacterium in the oceans.
Clasen, J. L. et al. Evidence that viral abundance across oceans and lakes is driven by different biological factors. Freshw. Biol. 53, 1090–1100 (2008).
Wilhelm, S. W. & Matteson, A. R. Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshw. Biol. 53, 1076–1089 (2008).
Danovaro, R. et al. Marine viruses and global climate change. FEMS Microbiol. Rev. 35, 993–1034 (2011).
Brum, J. R., Schenck, R. O. & Sullivan, M. B. Global morphological analysis of marine viruses shows minimal regional variation and dominance of non-tailed viruses. ISME J. 7, 1738–1751 (2013). This study provides quantitative estimates of the size and morphology of virus particles in seawater and provides constraints on the probable ranges of marine virus sizes.
Ridal, J. J. & Moore, R. M. Dissolved organic phosphorus concentrations in the northeast subarctic Pacific Ocean. Limnol. Oceanogr. 37, 1067–1075 (1992).
Clark, L. L., Ingall, E. D. & Benner, R. Marine phosphorus is selectively remineralized. Nature 393, 426–426 (1998).
Ammerman, J. W. et al. Phosphorus deficiency in the Atlantic: an emerging paradigm in oceanography. Eos 84, 165–170 (2003).
Loh, A. N. & Bauer, J. E. Distribution, partitioning and fluxes of dissolved and particulate organic C, N and P in the eastern North Pacific and Southern Oceans. Deep Sea Res. I 47, 2287–2316 (2000).
Lomas, M. W. et al. Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP). Biogeosciences 7, 695–710 (2010). This study shows the importance of organic, rather than inorganic, forms of phosphorus in supporting primary production in some oceanic realms (for example, in the Sargasso Sea).
Nausch, M. & Nausch, G. Bioavailability of dissolved organic phosphorus in the Baltic Sea. Mar. Ecol. Prog. Ser. 321, 9–17 (2006).
Nishimura, Y., Kim, C. & Nagata, T. Vertical and seasonal variations of bacterioplankton subgroups with different nucleic acid contents: possible regulation by phosphorus. Appl. Environ. Microbiol. 71, 5828–5836 (2005).
Raimbault, P., Garcia, N. & Cerutti, F. Distribution of inorganic and organic nutrients in the South Pacific Ocean — evidence for long-term accumulation of organic matter in nitrogen-depleted waters. Biogeosciences 5, 281–298 (2008).
van der Zee, C. & Chou, L. Seasonal cycling of phosphorus in the southern bight of the North Sea. Biogeosciences Discussions 1, 681–707 (2004).
Yoshimura, T. et al. Distributions of particulate and dissolved organic and inorganic phosphorus in North Pacific surface waters. Marine Chem. 103, 112–121 (2007).
Kolowith, L. C., Ingall, E. D. & Benner, R. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46, 309–320 (2001).
Bermuda Institue of Ocean Sciences. Bermuda Atlantic Time-Series Study [online]
Parsons, R. J. et al. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273–284 (2011).
Fujieki, L. A. Hawaii Ocean Time Series Data Organization and Graphical System (HOT-DOGS) [online]
Culley, A. I. & Welschmeyer, N. A. The abundance, distribution, and correlation of viruses, phytoplankton, and prokaryotes along a Pacific Ocean transect. Limnol. Oceanogr. 47, 1508–1513 (2002).
Brum, J. R. Concentration, production and turnover of viruses and dissolved DNA pools at Stn ALOHA, North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 41, 103–113 (2005).
Matteson, A. R. et al. High abundances of cyanomyoviruses in marine ecosystems demonstrate ecological relevance. FEMS Microbiol. Ecol. 84, 223–234 (2013).
Strzepek, R. F. et al. Spinning the 'ferrous wheel': the importance of the microbial community in an iron budget during the FeCycle experiment. Global Biogeochem. Cycles 19, GB4S26 (2005).
Evans, C. & Brussaard, C. P. D. Regional variation in lytic and lysogenic viral infection in the Southern Ocean and its contribution to biogeochemical cycling. Appl. Environ. Microbiol. 78, 6741–6748 (2012).
Evans, C., Pearce, I. & Brussaard, C. P. D. Viral-mediated lysis of microbes and carbon release in the sub-Antarctic and Polar Frontal zones of the Australian Southern Ocean. Environ. Microbiol. 11, 2924–2934 (2009).
Hansell, D. A. et al. Dissolved organic matter in the ocean: new insights stimulated by a controversy. Oceanography 22, 202–211 (2009).
Letscher, R. T. et al. Dissolved organic nitrogen in the global surface ocean: distribution and fate. Global Biogeochem. Cycles 27, 141–153 (2013).
Winget, D. M. et al. Repeating patterns of virioplankton production within an estuarine ecosystem. Proc. Natl Acad. Sci. USA 108, 11506–11511 (2011).
Winter, C. et al. Linking bacterial richness with viral abundance and prokaryotic activity. Limnol. Oceanogr. 50, 968–977 (2005).
Matteson, A. R. et al. Production of viruses during a spring phytoplankton bloom in the South Pacific Ocean near of New Zealand. FEMS Microbiol. Ecol. 79, 709–719 (2012).
Suttle, C. A., Chan, A. M. & Chen, F. Cyanophages and Sunlight: a Paradox. (eds. Guerrero, R. & Pedros-Alio, C.) 303–307 (Spanish Society for Microbiology, 1993).
Bjorkman, K., Thomson-Bulldis, A. L. & Karl, D. M. Phosphorus dynamics in the North Pacific subtropical gyre. Aquat. Microb. Ecol. 22, 185–198 (2000).
Gonzalez, J. M. & Suttle, C. A. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Marine Ecol. Prog. Ser. 94, 1–10 (1993). This study shows the ecological potential for viruses to be targets of grazing.
Fischer, M. G. et al. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl Acad. Sci. USA 107, 19508–19513 (2010).
La Scola, B. et al. The virophage as a unique parasite of the giant mimivirus. Nature 455, 100–104 (2008).
Steward, G. F. et al. Are we missing half of the viruses in the ocean? ISME J. 7, 672–679 (2013).
Forterre, P. et al. Fake virus particles generated by fluorescence microscopy. Trends Microbiol. 21, 1–5 (2012).
Dyhrman, S. T., Ammerman, J. W. & Van Mooy, B. A. S. Microbes and the marine phosphorus cycle. Oceanography 20, 110–116 (2007).
Lindell, D. et al. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005). This study shows that host-derived, viral-encoded protein expression during infection boosts host metabolism during viral progeny production.
Frank, H. & Moebus, K. An electron microscopic study of bacteriophages from marine waters. Helgol. Mar. Res. 41, 385–414 (1987).
Ackermann, H.-W. & Heldal, M. in Manual of Aquatic Viral Ecology. (eds Wilhelm, S., Weinbauer, M. & Suttle C.) 182–192 (American Society of Limnology and Oceanography, 2010).
Angly, F. E. et al. The marine viromes of four oceanic regions. PLoS Biol. 4, 2121–2131 (2006).
Williamson, S. J. et al. The Sorcerer II Global Ocean Sampling Expedition: metagenomic characterization of viruses within aquatic microbial samples. PLoS ONE 3, e1456 (2008).
Deng, L. et al. Contrasting life strategies of viruses that infect photo- and heterotrophic bacteria, as revealed by viral tagging. mBio 3, e00373-12 (2012).
De Paepe, M. & Taddei, F. Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol. 4, e193 (2006).
Choi, K. H. et al. Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4. J. Mol. Biol. 378, 726–736 (2008).
Pope, W. H. et al. Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: a 'horned' bacteriophage of marine Synechococcus. J. Mol. Biol. 368, 966–981 (2007).
Wikoff, W. R. et al. Topologically linked protein rings in the bacteriophage HK97 capsid. Science 289, 2129–2133 (2000).
Ionel, A. et al. Molecular rearrangements involved in the capsid shell maturation of bacteriophage T7. J. Biol. Chem. 286, 234–242 (2011).
Tao, Y. et al. Assembly of a tailed bacterial virus and its genome release studied in three dimensions. Cell 95, 431–437 (1998).
Leiman, P. G. et al. Structure and morphogenesis of bacteriophage T4. Cell. Mol. Life Sci. 60, 2356–2370 (2003).
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.
The authors declare no competing financial interests.
Parameters and ranges used in the theory of viral elemental stoichoimetry (PDF 1733 kb)
Phage capsid size and genome length calibration data set (XLSX 12 kb)
Phage genome length data set (XLSX 49 kb)
Viral protein data set (XLSX 660 kb)
- 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.
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.
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.
About this article
Cite this article
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
The ISME Journal (2020)
Nature Reviews Microbiology (2020)
Proceedings of the National Academy of Sciences (2019)
Systematic Variation in Marine Dissolved Organic Matter Stoichiometry and Remineralization Ratios as a Function of Lability
Global Biogeochemical Cycles (2019)