The fate and biogeochemical cycling of viral elements

In a recent Analysis article (The elemental composition of virus particles: implications for marine biogeochemical cycles. Nature Rev. Microbiol. 12, 519–528 (2014))1, Jover et al. highlight the generally overlooked potential biogeochemical importance of the elements that are bound in virus particles. Here, we wish to discuss the fate of marine virioplankton (that is, free virus particles in the water column), which further extends our knowledge of the biogeochemical cycling of the elements that are present in viral particles in the ocean.

After being released into seawater, virus particles face complex environmental conditions before they successfully encounter their specific hosts and start a new life cycle2,3,4. Most viruses are impeded from establishing a new infection and, in natural seawater, a major loss of infectivity and decay of viral particles is observed over periods of hours and days2,3,4. This rapid turnover rate of marine virioplankton suggests that the chemical elements within these particles also undergo fast and active cycling. Jover et al. suggest that these elements, particularly phosphorus, could make a considerable contribution to marine elemental reservoirs1. In fact, the direction of flow and biogeochemical cycling of these elements depends on the fate of the virioplankton (Fig. 1), which is determined by different biological, chemical and physical factors.

Figure 1: Schematic illustration of the fate of viral particles in the upper ocean.
figure1

Elements that are present in viral particles will enter the microbial loop via degradation, classical marine food webs via grazing and the deep ocean via adsorption. DOM, dissolved organic matter; C,N,P, carbon, nitrogen, phosphorus; HNF, heterotrophic nanoflagellate; POM, particulate organic matter.

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UV irradiation (especially UV-B irradiation) has been considered to be one of the main causative factors responsible for the presence of defective viruses in surface marine environments5,6. An average loss of viral infectivity of 0.2 per hour has been observed under full sunlight for a diverse range of marine virus isolates4. Although solar radiation mainly decreases viral infectivity, extracellular enzymes produced by bacterioplankton and other microorganisms degrade viral particles, and the viral components therein (mainly protein and nucleic acid) are released into the marine dissolved organic matter (DOM) pool and can be utilized by bacterioplankton and cycled within the microbial loop7 (Fig. 1). It is evident that direct or indirect grazing by protists (for example, phagotrophic flagellates) contributes to the removal of viruses8,9, which acts as top-down control for virioplankton and transfers the viral component to higher trophic levels of the marine food web (Fig. 1). The effects of grazing on the removal of viral particles are more significant in eutrophic than in oligotrophic waters and depend on the abundance of both viruses and protists8,9. The viral components and elements that are transferred into the microbial loop and food web are mainly cycled locally. However, viral particles will also be absorbed onto particles (for example, particular organic matter or transparent exopolymeric particles) and then vertically settle down to the deep ocean2,3,4 (Fig. 1) or are transported laterally with the water mass. This accounts for the removal of a substantial proportion (up to 34% in the coastal Mediterranean Sea) of free-living viral particles from the water column6,9 and should drive a large amount of viral materials away from local biogeochemical cycling.

Although several studies have shown that viral particles are abundant in bathypelagic waters10,11,12, the source and fate of these deep sea viruses are unclear. Compared with surface waters, the decay rate of virioplankton in the deep sea is decreased by two to three orders of magnitude, which might contribute — at least partially — to the high number of viruses in the deep sea10,13. Very limited measurements of viral production and the decay rate have suggested allochthonous inputs of viruses, on sedimentation particles, to the deep sea9,10,11,12,13. Nevertheless, as an organic form, the elemental constituents of viruses should be more important in the deep sea than in the upper ocean as most DOM in the deep sea is refractory14. In this sense, unlike their generally recognized top-down role in microbial ecosystems, in oligotrophic deep seas viral particles can be regarded as 'bottom-up' agents, partially fertilizing the microbial loop. More investigations are urged to elucidate the biogeochemical role of viruses in the deep ocean.

References

  1. 1

    Jover, L. F., Effler, T. C., Buchan, A., Wilhelm, S. W. & Weitz, J. S. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nature Rev. Microbiol. 12, 519–528 (2014).

    CAS  Article  Google Scholar 

  2. 2

    Weinbauer, M. G. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28, 127–181 (2004).

    CAS  Article  Google Scholar 

  3. 3

    Wommack, K. E. & Colwell, R. R. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64, 69–114 (2000).

    CAS  Article  Google Scholar 

  4. 4

    Mojica, K. D. & Brussaard, C. P. Factors affecting virus dynamics and microbial host–virus interactions in marine environments. FEMS Microbiol. Ecol. 89, 495–515 (2014).

    CAS  Article  Google Scholar 

  5. 5

    Suttle, C. A. & Chen, F. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721–3729 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Noble, R. T. & Fuhrman, J. A. Virus decay and its causes in coastal waters. Appl. Environ. Microbiol. 63, 77–83 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Noble, R. T. & Fuhrman, J. A. Breakdown and microbial uptake of marine viruses and other lysis products. Aquat. Microb. Ecol. 20, 1–11 (1999).

    Article  Google Scholar 

  8. 8

    Gonzalez, J. & Suttle, C. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94, 1–10 (1993).

    Article  Google Scholar 

  9. 9

    Bongiorni, L., Magagnini, M., Armeni, M., Noble, R. & Danovaro, R. Viral production, decay rates, and life strategies along a trophic gradient in the North Adriatic Sea. Appl. Environ. Microbiol. 71, 6644–6650 (2005).

    CAS  Article  Google Scholar 

  10. 10

    Arístegui, J., Gasol, J. M., Duarte, C. M. & Herndl, G. Microbial oceanography of the dark ocean's pelagic realm. Limnol. Oceanogr. 54, 1501–1529 (2009).

    Article  Google Scholar 

  11. 11

    de Corte, D., Sintes, E., Yokokawa, T., Reinthaler, T. & Herndl, G. J. Links between viruses and prokaryotes throughout the water column along a North Atlantic latitudinal transect. ISME J. 6, 1566–1577 (2012).

    CAS  Article  Google Scholar 

  12. 12

    Li, Y. et al. Examination of the role of the microbial loop in regulating lake nutrient stoichiometry and phytoplankton dynamics. Biogeosciences 11, 2939–2960 (2014).

    CAS  Article  Google Scholar 

  13. 13

    Parada, V., Sintes, E. & van Aken, H. M. Viral abundance, decay, and diversity in the meso-and bathypelagic waters of the North Atlantic. Appl. Environ. Microbiol. 73, 4429–4438 (2007).

    CAS  Article  Google Scholar 

  14. 14

    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).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Comments from Feng Chen were appreciated. Financial support is provided by the 973 program (2013CB955700) and NSFC (41376132.) to R.Z.

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Zhang, R., Wei, W. & Cai, L. The fate and biogeochemical cycling of viral elements. Nat Rev Microbiol 12, 850–851 (2014). https://doi.org/10.1038/nrmicro3384

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