Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Viruses in the sea

Nature volume 437, pages 356–361 (2005)Cite this article

Abstract

Viruses exist wherever life is found. They are a major cause of mortality, a driver of global geochemical cycles and a reservoir of the greatest genetic diversity on Earth. In the oceans, viruses probably infect all living things, from bacteria to whales. They affect the form of available nutrients and the termination of algal blooms. Viruses can move between marine and terrestrial reservoirs, raising the spectre of emerging pathogens. Our understanding of the effect of viruses on global systems and processes continues to unfold, overthrowing the idea that viruses and virus-mediated processes are sidebars to global processes.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The three families of tailed dsDNA viruses (phages) that infect bacteria.
Figure 2: The nuclear inclusion virus of Heterosigma akashiwo.
Figure 3: Viruses are catalysts for biogeochemical cycling.
Figure 4: Viruses can affect the efficiency of the biological pump.

Similar content being viewed by others

References

  1. Bergh, O., Børsheim, K. Y., Bratbak, G. & Heldal, M. High abundance of viruses found in aquatic environments. Nature 340, 467–468 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Proctor, L. M. & Fuhrman, J. A. Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60–62 (1990).

    Article  ADS  Google Scholar 

  3. Suttle, C. A., Chan, A. M. & Cottrell, M. T. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347, 467–469 (1990).

    Article  ADS  Google Scholar 

  4. Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea. Bioscience 49, 781–788 (1999).

    Article  Google Scholar 

  5. Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  8. Weinbauer, M. G. & Rassoulzadegan, F. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6, 1–11 (2004).

    Article  PubMed  Google Scholar 

  9. Cochlan, W. P., Wikner, J., Steward, G. F., Smith, D. C. & Azam, F. Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments. Mar. Ecol. Prog. Ser. 92, 77–87 (1993).

    Article  ADS  Google Scholar 

  10. Paul, J. H., Rose, J. B., Jiang, S. C., Kellogg, C. A. & Dickson, L. Distribution of viral abundance in the reef environment of Key Largo, Florida. Appl. Environ. Microbiol. 59, 718–724 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Boehme, J. et al. Viruses, bacterioplankton, and phytoplankton in the southeastern Gulf of Mexico: distribution and contribution to oceanic DNA pools. Mar. Ecol. Prog. Ser. 97, 1–10 (1993).

    Article  ADS  Google Scholar 

  12. Maranger, R. & Bird, D. F. Viral abundances in aquatic systems: a comparison between marine and fresh waters. Mar. Ecol. Prog. Ser. 121, 217–226 (1995).

    Article  ADS  Google Scholar 

  13. Hewson, I., O'Neil, J. M., Fuhrman, J. A. & Dennison, W. C. Virus-Like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol. Oceanogr. 46, 1734–1746 (2001).

    Article  ADS  Google Scholar 

  14. Middelboe, M., Glud, R. N. & Finster, K. Distribution of viruses and bacteria in relation to diagenetic activity in an estuarine sediment. Limnol. Oceanogr. 48, 1447–1456 (2003).

    Article  ADS  Google Scholar 

  15. Bird, D. F. et al. Subsurface viruses and bacteria in Holocene/Late Pleistocene sediments of Saanich Inlet, BC: ODP holes 1033b and 1034b, Leg 169s. Mar. Geol. 174, 227–239 (2001).

    Article  ADS  CAS  Google Scholar 

  16. Danovaro, R., Corinaldesi, C., Dell'anno, A., Fabiano, M. & Corselli, C. Viruses, prokaryotes and DNA in the sediments of a deep-hypersaline anoxic basin (DHAB) of the Mediterranean Sea. Environ. Microbiol. 7, 586–592 (2005).

    Article  CAS  PubMed  Google Scholar 

  17. Hennes, K. P. & Suttle, C. A. Direct counts of viruses in natural waters and laboratory cultures by epifluorescence microscopy. Limnol. Oceanogr. 40, 1050–1055 (1995).

    Article  ADS  CAS  Google Scholar 

  18. Noble, R. T. & Fuhrman, J. A. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14, 113–118 (1998).

    Article  Google Scholar 

  19. Brussaard, C. P. D. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol. 70, 1506–1513 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bettarel, Y., Sime-Ngando, T., Amblard, C. & Laveran, H. A comparison of methods for counting viruses in aquatic systems. Appl. Environ. Microbiol. 66, 2283–2289 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wen, K., Ortmann, A. C. & Suttle, C. A. Accurate estimation of viral abundance by epifluorescence microscopy. Appl. Environ. Microbiol. 70, 3862–3867 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Guixa-Boixereu, N., Vaque, D., Gasol, J. M., Sanchez-Camara, J. & Pedros-Alio, C. Viral distribution and activity in Antarctic waters. Deep-Sea Res. II 49, 827–845 (2002).

    Article  ADS  Google Scholar 

  23. Ortmann, A. C. & Suttle, C. A. High abundances of viruses in a deep-sea hydrothermal vent system indicates viral mediated microbial mortality. Deep-Sea Res. I 52, 1515–1527 (2005).

    Article  ADS  Google Scholar 

  24. Jelmert, A. & Oppen-Berntsen, D. O. Whaling and deep-sea biodiversity. Conserv. Biol. 10, 653–654 (1996).

    Article  Google Scholar 

  25. Wilhelm, S. W., Weinbauer, M. G., Suttle, C. A., Pledger, R. J. & Mitchell, D. L. Measurements of DNA damage and photoreactivation imply that most viruses in marine surface waters are infective. Aquat. Microb. Ecol. 14, 215–222 (1998).

    Article  Google Scholar 

  26. Suttle, C. A. in Viral Ecology (ed. Hurst, C. J.) 248–286 (Academic, New York, 2000).

    Google Scholar 

  27. Lawrence, J. E., Chan, A. M. & Suttle, C. A. Viruses causing lysis of the toxic bloom-forming alga, Heterosigma akashiwo (Raphidophyceae), are widespread in coastal sediments of British Columbia, Canada. Limnol. Oceanogr. 47, 545–550 (2002).

    Article  ADS  Google Scholar 

  28. Suttle, C. A. & Chan, A. M. Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol. 60, 3167–3174 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Cottrell, M. T. & Suttle, C. A. Dynamics of a lytic virus infecting the photosynthetic marine picoflagellate, Micromonas pusilla. Limnol. Oceanogr. 40, 730–739 (1995).

    Article  ADS  Google Scholar 

  30. Frank, H. & Moebus, K. An electron microscopic study of bacteriophages from marine waters. Helgolander Meeresunters 41, 385–414 (1987).

    Article  Google Scholar 

  31. Moebus, K. & Nattkemper, H. Bacteriophage sensitivity patterns among bacteria isolated from marine waters. Helgolander Meeresunters 34, 375–385 (1981).

    Article  Google Scholar 

  32. Kellogg, C. A., Rose, J. B., Jiang, S. C., Thurmond, J. & Paul, J. H. Genetic diversity of related vibriophages isolated from marine environments around Florida and Hawaii, USA. Mar. Ecol. Prog. Ser. 120, 89–98 (1995).

    Article  ADS  Google Scholar 

  33. Wichels, A. et al. Bacteriophage diversity in the North Sea. Appl. Environ. Microbiol. 64, 4128–4133 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Sullivan, M. B., Waterbury, J. B. & Chisholm, S. W. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 424, 1047–1051 (2003).

    Article  ADS  CAS  PubMed  Google Scholar 

  35. Van Etten, J. L., Graves, M. V., Muller, D. G., Boland, W. & Delaroque, N. Phycodnaviridae — Large DNA algal viruses. Arch. Virol. 147, 1479–1516 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Lang, A. S., Culley, A. I. & Suttle, C. A. Genome sequence and characterization of a virus (HaRNAV) related to picorna-like viruses that infects the marine toxic bloom-forming alga Heterosigma akashiwo. Virology 320, 206–217 (2004).

    Article  CAS  PubMed  Google Scholar 

  37. Brussaard, C. P. D., Noordeloos, A. A. M., Sandaa, R. A., Heldal, M. & Bratbak, G. Discovery of a dsRNA virus infecting the marine photosynthetic protist Micromonas pusilla. Virology 319, 280–291 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. Takao, Y., Nagasaki, K., Mise, K., Okuno, T. & Honda, D. Isolation and characterization of a novel single-stranded RNA virus infectious to a marine fungoid protist, Schizochytrium sp. (Thraustochytriaceae, Labyrinthulea). Appl. Environ. Microbiol. 71, 4516–4522 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nagasaki, K. et al. Previously unknown virus infects marine diatom. Appl. Environ. Microbiol. 71, 3528–3535 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lawrence, J. E., Chan, A. M. & Suttle, C. A. A novel virus (HaNIV) causes lysis of the toxic bloom-forming alga Heterosigma akashiwo (Raphidophyceae). J. Phycol. 37, 216–222 (2001).

    Article  Google Scholar 

  41. Bettarel, Y. et al. Isolation and characterisation of a small nuclear inclusion virus infecting the diatom Chaetoceros c.f. gracilis. Aquat. Microb. Ecol. (in the press).

  42. Garza, D. R. & Suttle, C. A. Large double-stranded DNA viruses which cause the lysis of marine heterotrophic nanoflagellates (Bodo sp.) occur in natural marine virus communities. Aquat. Microb. Ecol. 9, 203–210 (1995).

    Article  Google Scholar 

  43. Raoult, D. et al. The 1.2-megabase genome sequence of mimivirus. Science 306, 1344–1350 (2004).

    Article  ADS  CAS  PubMed  Google Scholar 

  44. Van Hulten, M. C. W. et al. The White Spot Syndrome Virus DNA genome sequence. Virology 286, 7–22 (2001).

    Article  CAS  PubMed  Google Scholar 

  45. Zhang, S., Shi, Z., Zhang, J. & Bonami, J. R. Purification and characterization of a new reovirus from the Chinese Mitten Crab, Eriocheir sinensis. J. Fish Dis. 27, 687–692 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Chen, F., Suttle, C. A. & Short, S. M. Genetic diversity in marine algal virus communities as revealed by sequence analysis of DNA polymerase genes. Appl. Environ. Microbiol. 62, 2869–2874 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Short, S. M. & Suttle, C. A. Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 68, 1290–1296 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Wilson, W. H., Fuller, N. J., Joint, I. R. & Mann, N. H. Analysis of cyanophage diversity and population structure in a south-north transect of the Atlantic Ocean. Bull. Inst. Oceanogr. 19, 209–216 (1999).

    Google Scholar 

  49. Frederickson, C. M., Short, S. M. & Suttle, C. A. The physical environment affects cyanophage communities in British Columbia inlets. Microb. Ecol. 46, 348–357 (2003).

    Article  CAS  PubMed  Google Scholar 

  50. Zhong, Y., Chen, F., Wilhelm, S. W., Poorvin, L. & Hodson, R. E. Phylogenetic diversity of marine cyanophage isolates and natural virus communities as revealed by sequences of viral capsid assembly protein gene G20. Appl. Environ. Microbiol. 68, 1576–1584 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Short, C. M. & Suttle, C. A. Nearly identical bacteriophage structural gene sequences are widely distributed in both marine and freshwater environments. Appl. Environ. Microbiol. 71, 480–486 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Breitbart, M., Miyake, J. H. & Rohwer, F. Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol. Lett. 236, 249–256 (2004).

    Article  CAS  PubMed  Google Scholar 

  53. Culley, A. I., Lang, A. S. & Suttle, C. A. High diversity of unknown picorna-like viruses in the sea. Nature 424, 1054–1057 (2003).

    Article  ADS  CAS  PubMed  Google Scholar 

  54. Breitbart, M. et al. Genomic analysis of uncultured marine viral communities. Proc. Natl Acad. Sci. USA 99, 14250–14255 (2002).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  55. Breitbart, M. et al. Diversity and population structure of a near-shore marine-sediment viral community. Proc. R. Soc. Lond. B 271, 565–574 (2004).

    Article  Google Scholar 

  56. Breitbart, M. & Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284 (2005).

    Article  CAS  PubMed  Google Scholar 

  57. Edwards, R. A. & Rohwer, F. Viral metagenomics. Nature Rev. Microbiol. 3, 504–510 (2005).

    Article  CAS  Google Scholar 

  58. Rohwer, F. et al. The complete genomic sequence of the marine phage Roseophage SIO1 shares homology with nonmarine phages. Limnol. Oceanogr. 45, 408–418 (2000).

    Article  ADS  CAS  Google Scholar 

  59. Hardies, S. C., Comeau, A. M., Serwer, P. & Suttle, C. A. The complete sequence of marine bacteriophage VpV262 infecting Vibrio parahaemolyticus indicates that an ancestral component of a T7 viral supergroup is widespread in the marine environment. Virology 310, 359–371 (2003).

    Article  CAS  PubMed  Google Scholar 

  60. Chen, F. & Lu, J. R. Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl. Environ. Microbiol. 68, 2589–2594 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Paul, J. H. et al. Complete genome sequence of fHSIC, a pseudotemperate marine phage of Listonella pelagia. Appl. Environ. Microbiol. 71, 3311–3320 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Sullivan, M. B., Coleman, M. L., Weigele, P., Rohwer, F. & Chisholm, S. W. Three Prochlorococcus cyanophage genomes: Signature features and ecological interpretations. PLoS Biol. 3, 790–806 (2005).

    Article  CAS  Google Scholar 

  63. Wilson, W. H. et al. Complete genome sequence and lytic phase transcription profile of a Coccolithovirus. Science 309, 1090–1092 (2005).

    Article  ADS  CAS  PubMed  Google Scholar 

  64. Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 424, 741 (2003).

    Article  ADS  CAS  PubMed  Google Scholar 

  65. Millard, A., Clokie, M. R. J., Shub, D. A. & Mann, N. H. Genetic organization of the psbAD region in phages infecting marine Synechococcus strains. Proc. Natl Acad. Sci. USA 101, 11007–11012 (2004).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  66. Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl Acad. Sci. USA 101, 11013–11018 (2004).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zeidner, G. et al. Potential photosynthesis gene swapping between Prochlorococcus and Synechococcus via viral intermediates. Environ. Microbiol. published online 23 June 2005 (doi: 10.1111/j.1462-2920.2005.00833.x).

  68. Hambly, E. & Suttle, C. A. The viriosphere, diversity and genetic exchange within phage communities. Curr. Opin. Microbiol. 8, 444–450 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Heldal, M. & Bratbak, G. Production and decay of viruses in aquatic environments. Mar. Ecol. Prog. Ser. 72, 205–212 (1991).

    Article  ADS  Google Scholar 

  70. 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 

  71. Noble, R. T. & Fuhrman, J. A. Rapid virus production and removal as measured with fluorescently labeled viruses as tracers. Appl. Environ. Microbiol. 66, 3790–3797 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Steward, G. F., Wikner, J., Cochlan, W. P., Smith, D. C. & Azam, F. Estimation of virus production in the sea: 2. Field results. Mar. Microb. Food Webs 6, 79–90 (1992).

    Google Scholar 

  73. Wilhelm, S. W., Brigden, S. M. & Suttle, C. A. A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters. Microb. Ecol. 43, 168–173 (2002).

    Article  CAS  PubMed  Google Scholar 

  74. Evans, C., Archer, S. D., Jacquet, S. & Wilson, W. H. Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a Micromonas spp. population. Aquat. Microb. Ecol. 30, 207–219 (2003).

    Article  Google Scholar 

  75. Suttle, C. A. The significance of viruses to mortality in aquatic microbial communities. Microb. Ecol. 28, 237–243 (1994).

    Article  CAS  PubMed  Google Scholar 

  76. Fuhrman, J. A. & Noble, R. T. Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol. Oceanogr. 40, 1236–1242 (1996).

    Article  ADS  Google Scholar 

  77. Middelboe, M., Riemann, L., Steward, G. F., Hansen, V. & Nybroe, O. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat. Microb. Ecol. 33, 1–10 (2003).

    Article  Google Scholar 

  78. Lawrence, J. E. & Suttle, C. A. Effect of viral infection on sinking rates of Heterosigma akashiwo and its implications for bloom termination. Aquat. Microb. Ecol. 37, 1–7 (2004).

    Article  Google Scholar 

  79. Gobler, C. J., Hutchins, D. A., Fisher, N. S., Cosper, E. M. & Sanudo-Wilhelmy, S. Release and bioavailability of C,N, P, Se, and Fe following viral lysis of a marine Chrysophyte. Limnol. Oceanogr. 42, 1492–1504 (1997).

    Article  ADS  CAS  Google Scholar 

  80. Poorvin, L., Rinta-Kanto, J. M., Hutchins, D. A. & Wilhelm, S. W. Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr. 49, 1734–1741 (2004).

    Article  ADS  CAS  Google Scholar 

  81. Daughney, C. J. et al. Adsorption and precipitation of iron from seawater on a marine bacteriophage (PWH3a-P1). Mar. Chem. 91, 101–115 (2004).

    Article  CAS  Google Scholar 

  82. Smith, A. W. et al. Antisense treatment of Caliciviridae: an emerging disease agent of animals and humans. Curr. Opin. Mol. Ther. 4, 177–184 (2002).

    CAS  PubMed  Google Scholar 

  83. Philippa, J. D. W. et al. Antibodies to selected pathogens in free-ranging terrestrial carnivores and marine mammals in Canada. Vet. Rec. 155, 135–140 (2004).

    Article  CAS  PubMed  Google Scholar 

  84. Li, K. S. et al. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209–213 (2004).

    Article  ADS  CAS  PubMed  Google Scholar 

  85. Delaroque, N. et al. The complete DNA sequence of the Ectocarpus siliculosus Virus EsV-1 genome. Virology 287, 112–132 (2001).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I have an unrepayable debt of gratitude to L. M. Proctor and J. A. Fuhrman for introducing me to the world of viruses in the ocean and how to study them, and to A. M. Chan for her critical attention to detail and scientific excellence. In addition, I have been fortunate to have been continuously educated by the many scientific colleagues that have chosen to work in my laboratory over the years, and contributed to a rich and stimulating environment. I thank R. G. Hendrix of PBI for the idea of scaling viral abundance to planetary proportions, and giving permission to use the idea in this paper. Finally, I apologize for all the excellent scientific contributions that I have been unable to include in this abbreviated format.

Author information

Authors and Affiliations

  1. Department of Chemistry, University of California, Berkeley and the Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, 94720, California, USA

    Curtis A. Suttle

Authors
  1. Curtis A. Suttle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Curtis A. Suttle.

Ethics declarations

Competing interests

The author declares no competing financial interests.

Additional information

Author Information Reprints and permissions information is available at npg.nature.com/reprintsandpermissions.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suttle, C. Viruses in the sea. Nature 437, 356–361 (2005). https://doi.org/10.1038/nature04160

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04160

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing