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Nature Reviews Microbiology
  • Review Article
  • Published:

Marine viruses — major players in the global ecosystem

Nature Reviews Microbiologyvolume 5, pages801–812 (2007)Cite this article

Key Points

  • Viruses can be found in every environment on the Earth, but their importance is perhaps most evident in the oceans, where they are known to be the reservoir of most of the genetic diversity. Viruses kill approximately 20% of the oceanic microbial biomass daily, which has a significant impact on nutrient and energy cycles. This Review highlights areas in which marine virology is advancing quickly or seems to be poised for paradigm-shifting discoveries.

  • Developing the necessary techniques to obtain accurate and reproducible estimates of the distribution and abundance of marine viruses has been a challenge for researchers. Sub-populations of both viruses and host cells can now be discriminated using flow cytometry. Viral abundance generally co-varies with prokaryotic abundance and productivity, but marked differences in this relationship have been reported in different marine environments.

  • Quantifying the effects of viruses on marine prokaryotic and eukaryotic heterotrophic and autotrophic communities is also a challenging area, and remains one of the biggest obstacles to incorporating viral-mediated processes into global models of nutrient and energy cycling.

  • Our knowledge of the diversity of viruses in marine environments has increased greatly with the development of metagenomic approaches. The interactions between viruses and the organisms they infect ultimately control the genetic diversity of viruses and potentially influence the composition of microbial communities. However, the experimental evidence that supports the hypothesis that viruses regulate microbial diversity in nature is ambiguous. This is perhaps not surprising as the effects of viruses on their host cells depend on transient associations, which might lead us to expect that the influences of viruses on host populations will also be spatially and temporally variable.

Abstract

Viruses are by far the most abundant 'lifeforms' in the oceans and are the reservoir of most of the genetic diversity in the sea. The estimated 1030 viruses in the ocean, if stretched end to end, would span farther than the nearest 60 galaxies. Every second, approximately 1023 viral infections occur in the ocean. These infections are a major source of mortality, and cause disease in a range of organisms, from shrimp to whales. As a result, viruses influence the composition of marine communities and are a major force behind biogeochemical cycles. Each infection has the potential to introduce new genetic information into an organism or progeny virus, thereby driving the evolution of both host and viral assemblages. Probing this vast reservoir of genetic and biological diversity continues to yield exciting discoveries.

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Figure 1: Relative biomass and abundances of prokaryotes, protists and viruses.
Figure 2: Shunt and pump.
Figure 3: The distribution of, and selective influences operating on, marine prokaryotes, eukaryotes and viruses.
Figure 4: The distribution of marine viruses and their hosts along anr- and K-selection continuum.

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References

  1. Bergh, O., Børsheim, K. Y., Bratbak, G. & Heldal, M. High abundance of viruses found in aquatic environments.Nature340, 467–468 (1989).

    CAS PubMed  Google Scholar 

  2. Proctor, L. M. & Fuhrman, J. A. Viral mortality of marine bacteria and cyanobacteria.Nature343, 60–62 (1990).

    Google Scholar 

  3. Suttle, C. A., Chan, A. M. & Cottrell, M. T. Infection of phytoplankton by viruses and reduction of primary productivity.Nature347, 467–469 (1990).

    Google Scholar 

  4. Wilhelm, S. W. & Suttle, C. A. Viruses and nutrient cycles in the sea.Bioscience49, 781–788 (1999).

    Google Scholar 

  5. Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects.Nature399, 541–548 (1999).

    CAS PubMed  Google Scholar 

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

    CAS PubMed PubMed Central  Google Scholar 

  7. Suttle, C. A. Viruses in the sea.Nature437, 356–361 (2005).

    Article CAS PubMed  Google Scholar 

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

    Article CAS PubMed  Google Scholar 

  9. Torrella, F. & Morita, R. Y. Evidence by electron micrographs for a high incidence of bacteriophage particles in the waters of Yaquina Bay, Oregon: ecological and taxonomical implications.Appl. Environ. Microbiol.37, 774–778 (1979).

    CAS PubMed PubMed Central  Google Scholar 

  10. Hara, S., Terauchi, K. & Koike, I. Abundance of viruses in marine waters: assessment by epifluorescence and transmission electron microscopy.Appl. Environ. Microbiol.57, 2731–2734 (1991).

    CAS PubMed PubMed Central  Google Scholar 

  11. 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 CAS  Google Scholar 

  12. 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 

  13. 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 

  14. 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. I52, 1515–1527 (2005).

    Article  Google Scholar 

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

    Article CAS PubMed PubMed Central  Google Scholar 

  16. Danovaro, R., Dell'anno, A., Trucco, A., Serresi, M. & Vanucci, S. Determination of virus abundance in marine sediments.Appl. Environ. Microbiol.67, 1384–1387 (2001).

    Article CAS PubMed PubMed Central  Google Scholar 

  17. Helton, R. R., Liu, L. & Wommack, K. E. Assessment of factors influencing direct enumeration of viruses within estuarine sediments.Appl. Environ. Microbiol.72, 4767–4774 (2006).

    Article CAS PubMed PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  19. Jiang, S. C. & Paul, J. H. Seasonal and diel abundance of viruses and occurrence of lysogeny/bacteriocinogeny in the marine environment.Mar. Ecol. Prog. Ser.104, 163–172 (1994).

    Article  Google Scholar 

  20. 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  Google Scholar 

  21. Clasen, J. L., Brigden, S. M., Payet, J. P. & Suttle, C. A. Viral abundance across marine and freshwater systems is driven by different biological factors.Freshwater Biol. (in the press).

  22. Waterbury, J. B. & Valois, F. W. Resistance to co-occurring phages enables marineSynechococcus communities to coexist with cyanophages abundant in seawater.Appl. Environ. Microbiol.59, 3393–3399 (1993).

    CAS PubMed PubMed Central  Google Scholar 

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

    CAS PubMed PubMed Central  Google Scholar 

  24. Hara, S., Koike, I., Terauchi, K., Kamiya, H. & Tanoue, E. Abundance of viruses in deep oceanic waters.Mar. Ecol. Prog. Ser.145, 269–277 (1996).

    Article  Google Scholar 

  25. Proctor, L. M. & Fuhrman, J. A. Roles of viral infection in organic particle flux.Mar. Ecol. Prog. Ser.69, 133–142 (1991).

    Article  Google Scholar 

  26. Seymour, J. R., Seuront, L., Doubell, M., Waters, R. L. & Mitchell, J. G. Microscale patchiness of virioplankton.J. Mar. Biolog. Assoc. UK86, 551–561 (2006).

    Article  Google Scholar 

  27. Marie, D., Brussaard, C. P. D., Thyrhaug, R., Bratbak, G. & Vaulot, D. Enumeration of marine viruses in culture and natural samples by flow cytometry.Appl. Environ. Microbiol.65, 45–52 (1999).

    CAS PubMed PubMed Central  Google Scholar 

  28. 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 

  29. Li, W. K. W. & Dickie, P. M. Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal inlet (Bedford Basin) by flow cytometry.Cytometry44, 236–246 (2001).

    Article CAS PubMed  Google Scholar 

  30. Chen, F., Lu, J. R., Binder, B. J., Liu, Y. C. & Hodson, R. E. Application of digital image analysis and flow cytometry to enumerate marine viruses stained with SYBR Gold.Appl. Environ. Microbiol.67, 539–545 (2001).

    Article CAS PubMed PubMed Central  Google Scholar 

  31. Lebaron, P., Servais, P., Agogue, H., Courties, C. & Joux, F. Does the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems?Appl. Environ. Microbiol.67, 1775–1782 (2001).

    Article CAS PubMed PubMed Central  Google Scholar 

  32. Lebaron, P. et al. Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry.Aquat. Microb. Ecol.28, 131–140 (2002).

    Article  Google Scholar 

  33. Longnecker, K., Sherr, B. F. & Sherr, E. B. Variation in cell-specific rates of leucine and thymidine incorporation by marine bacteria with high and with low nucleic acid content off the Oregon coast.Aquat. Microb. Ecol.43, 113–125 (2006).

    Article  Google Scholar 

  34. Sherr, E. B., Sherr, B. F. & Longnecker, K. Distribution of bacterial abundance and cell-specific nucleic acid content in the Northeast Pacific Ocean.Deep-Sea Res. I53, 713–725 (2006).

    Article CAS  Google Scholar 

  35. Moran, X. A. G., Bode, A., Suarez, L. A. & Nogueira, E. Assessing the relevance of nucleic acid content as an indicator of marine bacterial activity.Aquat. Microb. Ecol.46, 141–152 (2007).

    Article  Google Scholar 

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

    Article CAS PubMed  Google Scholar 

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

    Article  Google Scholar 

  38. 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 

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

    Article  Google Scholar 

  40. Helton, R. R., Cottrell, M. T., Kirchman, D. L. & Wommack, K. E. Evaluation of incubation-based methods for estimating virioplankton production in estuaries.Aquat. Microb. Ecol.41, 209–219 (2005).

    Article  Google Scholar 

  41. Weinbauer, M. G., Winter, C. & Hofle, M. G. Reconsidering transmission electron microscopy based estimates of viral infection of bacterio-plankton using conversion factors derived from natural communities.Aquat. Microb. Ecol.27, 103–110 (2002).

    Article  Google Scholar 

  42. Middelboe, M. & Glud, R. N. Viral activity along a trophic gradient in continental margin sediments off central Chile.Mar. Biol. Res.2, 41–51 (2006).

    Article  Google Scholar 

  43. Bratbak, G., Egge, J. K. & Heldal, M. Viral mortality of the marine algaEmiliania huxleyi (Haptophyceae) and termination of algal blooms.Mar. Ecol. Prog. Ser.93, 39–48 (1993).

    Article  Google Scholar 

  44. Tarutani, K., Nagasaki, K. & Yamaguchi, M. Viral impacts on total abundance and clonal composition of the harmful bloom-forming phytoplanktonHeterosigma akashiwo.Appl. Environ. Microbiol.66, 4916–4920 (2000).

    Article CAS PubMed PubMed Central  Google Scholar 

  45. Baudoux, A. C., Noordeloos, A. A. M., Veldhuis, M. J. W. & Brussaard, C. P. D. Virally induced mortality ofPhaeocystis globosa during two spring blooms in temperate coastal waters.Aquat. Microb. Ecol.44, 207–217 (2006).

    Article  Google Scholar 

  46. Tomaru, Y. et al. Ecological dynamics of the bivalve-killing dinoflagellateHeterocapsa circularisquama and its infectious viruses in different locations of western Japan.Environ. Microbiol.9, 1376–1383 (2007).

    Article PubMed  Google Scholar 

  47. Winter, C., Herndl, G. J. & Weinbauer, M. G. Diel cycles in viral infection of bacterioplankton in the North Sea.Aquat. Microb. Ecol.35, 207–216 (2004).

    Article  Google Scholar 

  48. Winter, C., Smit, A., Szoeke-Denes, T., Herndl, G. J. & Weinbauer, M. G. Modelling viral impact on bacterioplankton in the North Sea using artificial neural networks.Environ. Microbiol.7, 881–893 (2005).

    Article CAS PubMed  Google Scholar 

  49. Bratbak, G., Heldal, M., Norland, S. & Thingstad, T. F. Viruses as partners in spring bloom microbial trophodynamics.Appl. Environ. Microbiol.56, 1400–1405 (1990).

    CAS PubMed PubMed Central  Google Scholar 

  50. Short, S. M. & Suttle, C. A. Temporal dynamics of natural communities of marine algal viruses and eukaryotes.Aquat. Microb. Ecol.32, 107–119 (2003).

    Article  Google Scholar 

  51. Sandaa, R. A. & Larsen, A. Seasonal variations in virus-host populations in Norwegian coastal waters: focusing on the cyanophage community infecting marineSynechococcus spp.Appl. Environ. Microbiol.72, 4610–4618 (2006).

    Article CAS PubMed PubMed Central  Google Scholar 

  52. Weinbauer, M. G. & Peduzzi, P. Frequency, size and distribution of bacteriophages in different marine bacterial morphotypes.Mar. Ecol. Prog. Ser.108, 11–20 (1994).

    Article  Google Scholar 

  53. 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 CAS  Google Scholar 

  54. Middelboe, M., Jorgensen, N. O. G. & Kroer, N. Effects of viruses on nutrient turnover and growth efficiency of non-infected marine bacterioplankton.Appl. Environ. Microbiol.62, 1991–1997 (1996).

    CAS PubMed PubMed Central  Google Scholar 

  55. Middelboe, M. & Lyck, P. G. Regeneration of dissolved organic matter by viral lysis in marine microbial communities.Aquat. Microb. Ecol.27, 187–194 (2002).

    Article  Google Scholar 

  56. Middelboe, M. & Jorgensen, N. O. G. Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds.J. Mar. Biolog. Assoc. UK86, 605–612 (2006).

    Article CAS  Google Scholar 

  57. Fuhrman, J. A. inPrimary Productivity and Biogeochemical Cycles in the Sea (eds Falkowski, P. G. & Woodhead, A. D.) 361–383 (Plenum, New York, 1992).

    Book  Google Scholar 

  58. Evans, C. et al. The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulfoniopropionate (DMSP) cleavage: anEmiliania huxleyi culture study.Limnol. Oceanogr.52, 1036–1045 (2007).

    Article  Google Scholar 

  59. Bratbak, G. et al. Viral activity in relation toEmiliania huxleyi blooms: a mechanism of DMSP release?Mar. Ecol. Prog. Ser.128, 133–142 (1995).

    Article CAS  Google Scholar 

  60. Hill, R. W., White, B. A., Cottrell, M. T. & Dacey, J. W. H. Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process.Aquat. Microb. Ecol.14, 1–6 (1998).

    Article  Google Scholar 

  61. Malin, G., Wilson, W. H., Bratbak, G., Liss, P. S. & Mann, N. H. Elevated production of dimethylsulfide resulting from viral infection of cultures ofPhaeocystis pouchetii.Limnol. Oceanogr.43, 1389–1393 (1998).

    Article CAS  Google Scholar 

  62. 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 CAS  Google Scholar 

  63. Mioni, C. E., Poorvin, L. & Wilhelm, S. W. Virus and siderophore-mediated transfer of available Fe between heterotrophic bacteria: characterization using an Fe-specific bioreporter.Aquat. Microb. Ecol.41, 233–245 (2005).

    Article  Google Scholar 

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

    Article  Google Scholar 

  65. Buesseler, K. O. et al. Revisiting carbon flux through the ocean's twilight zone.Science316, 567–570 (2007).

    Article CAS PubMed  Google Scholar 

  66. Thompson, J. R. et al. Genotypic diversity within a natural coastal bacterioplankton population.Science307, 1311–1313 (2005).

    Article CAS PubMed  Google Scholar 

  67. Pommier, T. et al. Global patterns of diversity and community structure in marine bacterioplankton.Mol. Ecol.16, 867–880 (2007).

    Article CAS PubMed  Google Scholar 

  68. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through Eastern Tropical Pacific.PLoS Biol.5, 398–431 (2007).

    Article CAS  Google Scholar 

  69. Polz, M. F., Hunt, D. E., Preheim, S. P. & Weinreich, D. M. Patterns and mechanisms of genetic and phenotypic differentiation in marine microbes.Phil. Trans. R. Soc. Lond. B, Biol. Sci.361, 2009–2021 (2006).

    Article  Google Scholar 

  70. Pedros-Alio, C. Marine microbial diversity: can it be determined?Trends Microbiol.14, 257–263 (2006).

    Article CAS PubMed  Google Scholar 

  71. Pernthaler, J. Predation on prokaryotes in the water column and its ecological implications.Nature Rev. Microbiol.3, 537–546 (2005).

    Article CAS  Google Scholar 

  72. Fuhrman, J. A. & Suttle, C. A. Viruses in marine planktonic systems.Oceanography6, 51–63 (1993).

    Article  Google Scholar 

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

    Article PubMed  Google Scholar 

  74. Wommack, K. E., Ravel, J., Hill, R. T. & Colwell, R. R. Hybridization analysis of Chesapeake Bay virioplankton.Appl. Environ. Microbiol.65, 241–250 (1999).

    CAS PubMed PubMed Central  Google Scholar 

  75. Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand.Aquat. Microb. Ecol.13, 19–27 (1997).

    Article  Google Scholar 

  76. Thingstad, T. F. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems.Limnol. Oceanogr.45, 1320–1328 (2000).

    Article  Google Scholar 

  77. Pedros-Alio, C., Calderon-Paz, J. I. & Gasol, J. M. Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton.FEMS Microbiol. Ecol.32, 157–165 (2000).

    Article CAS PubMed  Google Scholar 

  78. Murray, A. G. & Jackson, G. A. Viral dynamics: a model of the effects size, shape, motion and abundance of single-celled planktonic organisms and other particles.Mar. Ecol. Prog. Ser89, 103–116 (1992).

    Article  Google Scholar 

  79. Hennes, K. P., Suttle, S. A. & Chan, A. M. Fluorescently labeled virus probes show that natural virus populations can control the structure of marine microbial communities.Appl. Environ. Microbiol.61, 3623–3627 (1995).

    CAS PubMed PubMed Central  Google Scholar 

  80. Brussaard, C. P. D. Viral control of phytoplankton populations — a review.J. Eukaryot. Microbiol.51, 125–138 (2004).

    Article PubMed  Google Scholar 

  81. Martinez, J. M., Schroeder, D. C., Larsen, A., Bratbak, G. & Wilson, W. H. Molecular dynamics ofEmiliania huxleyi and cooccurring viruses during two separate mesocosm studies.Appl. Environ. Microbiol.73, 554–562 (2007).

    Article CAS PubMed  Google Scholar 

  82. Brussaard, C. P. D., Kuipers, B. & Veldhuis, M. J. W. A mesocosm study ofPhaeocystis globosa population dynamics: 1. Regulatory role of viruses in bloom.Harmful Algae4, 859–874 (2005).

    Article  Google Scholar 

  83. Nagasaki, K., Ando, M., Itakura, S., Imai, I. & Ishida, Y. Viral mortality in the final stage ofHeterosigma akashiwo (Raphidophyceae) red tide.J. Plankton Res.16, 1595–1599 (1994).

    Article  Google Scholar 

  84. Muhling, M. et al. Genetic diversity of marineSynechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton.Environ. Microbiol.7, 499–508 (2005).

    Article CAS PubMed  Google Scholar 

  85. Hewson, I., Wingett, D. M., Williamson, K. E., Fuhrman, J. A. & Wommack, K. E. Viral and bacterial assemblage covariance in oligotrophic waters of the West Florida Shelf (Gulf of Mexico).J. Mar. Biolog. Assoc. UK86, 591–603 (2006).

    Article CAS  Google Scholar 

  86. Bouvier, T. & del Giorgio, P. A. Key role of selective viral-induced mortality in determining marine bacterial community composition.Environ. Microbiol.9, 287–297 (2007).

    Article CAS PubMed  Google Scholar 

  87. Schwalbach, M. S., Hewson, I. & Fuhrman, J. A. Viral effects on bacterial community composition in marine plankton microcosms.Aquat. Microb. Ecol.34, 117–127 (2004).

    Article  Google Scholar 

  88. Hewson, I. & Fuhrman, J. A. Viral impacts upon marine bacterioplankton assemblage structure.J. Mar. Biol. Assoc. UK86, 577–589 (2006).

    Article CAS  Google Scholar 

  89. Winter, C., Smit, A., Herndl, G. J. & Weinbauer, M. G. Impact of virioplankton on archaeal and bacterial community richness as assessed in seawater batch cultures.Appl. Environ. Microbiol.70, 804–813 (2004).

    Article CAS PubMed PubMed Central  Google Scholar 

  90. Weinbauer, M. G. et al. Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity.Environ. Microbiol.9, 777–788 (2007).

    Article CAS PubMed  Google Scholar 

  91. Munn, C. B. Viruses as pathogens of marine organisms — from bacteria to whales.J. Mar. Biol. Assoc. UK86, 453–467 (2006).

    Article  Google Scholar 

  92. Flegel, T. W. Detection of major penaeid shrimp viruses in Asia, a historical perspective with emphasis on Thailand.Aquaculture258, 1–33 (2006).

    Article  Google Scholar 

  93. Saksida, S. M. Infectious haematopoietic necrosis epidemic (2001 to 2003) in farmed Atlantic salmonSalmo salar in British Columbia.Dis. Aquat. Org.72, 213–223 (2006).

    Article CAS  Google Scholar 

  94. Vlak, J. M. et al. in8th Report of the International Committee on Taxonomy of Viruses (eds Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A.) 187–192 (Elsevier, Amsterdam, 2004).

    Google Scholar 

  95. Kurath, G. et al. Phylogeography of infectious haematopoietic necrosis virus in North America.J. Gen. Virol.84, 803–814 (2003).

    Article CAS PubMed  Google Scholar 

  96. Skall, H. F., Olesen, N. J. & Mellergaard, S. Viral haemorrhagic septicaemia virus in marine fish and its implications for fish farming — a review.J. Fish Dis.28, 509–529 (2005).

    Article CAS PubMed  Google Scholar 

  97. Meyers, T. R., Short, S. & Lipson, K. Isolation of the North American strain of viral hemorrhagic septicemia virus (VHSV) associated with epizootic mortality in two new host species of Alaskan marine fish.Dis. Aquat. Org.38, 81–86 (1999).

    Article CAS  Google Scholar 

  98. Einer-jensen, K., Ahrens, P., Forsberg, R. & Lorenzen, N. Evolution of the fish rhabdovirus viral haemorrhagic septicaemia virus.J. Gen. Virol.85, 1167–1179 (2004).

    Article CAS PubMed  Google Scholar 

  99. Gagne, N. et al. Isolation of viral haemorrhagic septicaemia virus from mummichog, stickleback, striped bass and brown trout in eastern Canada.J. Fish Dis.30, 213–223 (2007).

    Article CAS PubMed  Google Scholar 

  100. Elsayed, E. et al. Isolation of viral haemorrhagic septicaemia virus from muskellunge, Esox masquinongy (Mitchill), in Lake St Clair, Michigan, USA reveals a new sublineage of the North American genotype.J. Fish Dis.29, 611–619 (2006).

    Article CAS PubMed  Google Scholar 

  101. Viral Hemorrhagic Septicemia in the Great Lakes in Emerging Disease Notice[online] (2006).

  102. Munday, B. L., Kwang, J. & Moody, N. Betanodavirus infections of teleost fish: a review.J. Fish Dis.25, 127–142 (2002).

    Article  Google Scholar 

  103. Cutrin, J. M. et al. Emergence of pathogenic betanodaviruses belonging to the SJNNV genogroup in farmed fish species from the Iberian Peninsula.J. Fish Dis.30, 225–232 (2007).

    Article CAS PubMed  Google Scholar 

  104. Hall, A. J., Jepson, P. D., Goodman, S. J. & Harkonen, T. Phocine distemper virus in the North and European Seas — data and models, nature and nurture.Biol. Conserv.131, 221–229 (2006).

    Article  Google Scholar 

  105. Di Guardo, G., Marruchella, G., Agrimi, U. & Kennedy, S. Morbillivirus infections in aquatic mammals: a brief overview.J. Vet. Med. A, Physiol. Pathol. Clin. Med.52, 88–93 (2005).

    Article CAS  Google Scholar 

  106. Britt, J. O., Nagy, A. Z. & Howard, E. B. Acute viral-hepatitis in California sea lions.J. Am. Vet. Med. Assoc.175, 921–923 (1979).

    PubMed  Google Scholar 

  107. Geraci, J. R. et al. Mass mortality of harbor seals — pneumonia associated with influenza A virus.Science215, 1129–1131 (1982).

    Article CAS PubMed  Google Scholar 

  108. Burek, K. A. et al. Infectious disease and the decline of Steller sea lions (Eumetopias jubatus) in Alaska, USA: insights from serologic data.J. Wildl. Dis.41, 512–524 (2005).

    Article PubMed  Google Scholar 

  109. Smith, A. W. et al. Vesivirus viremia and seroprevalence in humans.J. Med. Virol.78, 693–701 (2006).

    Article CAS PubMed PubMed Central  Google Scholar 

  110. Cottrell, M. T. & Suttle, C. A. Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryotic marine phytoplankter,Micromonas pusilla.Mar. Ecol. Prog. Ser78, 1–9 (1991).

    Article  Google Scholar 

  111. Cottrell, M. T. & Suttle, C. A. Genetic diversity of algal viruses which lyse the photosynthetic picoflagellateMicromonas pusilla (Prasinophyceae).Appl. Environ. Microbiol.61, 3088–3091 (1995).

    CAS PubMed PubMed Central  Google Scholar 

  112. Wilson, W. H., Joint, I. R., Carr, N. G. & Mann, N. H. Isolation and molecular characterization of five marine cyanophages propagated onSynechococcus sp. strain WH7803.Appl. Environ. Microbiol.59, 3736–3743 (1993).

    CAS PubMed PubMed Central  Google Scholar 

  113. Kellogg, C. A., Rose, J. B., Jiang, S. C., Thurmond, J. M. & 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  Google Scholar 

  114. 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 

  115. 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. (Monaco)19, 209–216 (1999).

    Google Scholar 

  116. Short, S. M. & Suttle, C. A. Use of the polymerase chain reaction and denaturing gradient gel electrophoresis to study diversity in natural virus communities.Hydrobiologia401, 19–32 (1999).

    Article CAS  Google Scholar 

  117. Wommack, K. E., Ravel, J., Hill, R. T., Chun, J. & Colwell, R. R. Population dynamics of Chesapeake Bay virioplankton: total community analysis using pulsed field gel electrophoresis.Appl. Environ. Microbiol.65, 231–240 (1999).

    CAS PubMed PubMed Central  Google Scholar 

  118. 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).

    Article  Google Scholar 

  119. Filee, J., Tetart, F., Suttle, C. A. & Krisch, H. M. Marine T4-type bacteriophages, a ubiquitous component of the dark matter of the biosphere.Proc. Natl Acad. Sci. USA102, 12471–12476 (2005).

    Article CAS PubMed PubMed Central  Google Scholar 

  120. 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 

  121. Zeidner, G. et al. Potential photosynthesis gene recombination betweenProchlorococcus andSynechococcus via viral intermediates.Environ. Microbiol.7, 1505–1513 (2005).

    Article CAS PubMed  Google Scholar 

  122. 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 

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

    Article CAS  Google Scholar 

  124. Paul, J. H. & Sullivan, M. B. Marine phage genomics: what have we learned?Curr. Opin. Biotechnol.16, 299–307 (2005).

    Article CAS PubMed  Google Scholar 

  125. Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus.Nature424, 741 (2003).

    Article CAS PubMed  Google Scholar 

  126. Lindell, D. et al. Transfer of photosynthesis genes to and fromProchlorococcus viruses.Proc. Natl Acad. Sci. USA101, 11013–11018 (2004).

    Article CAS PubMed PubMed Central  Google Scholar 

  127. Lindell, D., Jaffe, J. D., Johnson, Z. I., Church, G. M. & Chisholm, S. W. Photosynthesis genes in marine viruses yield proteins during host infection.Nature438, 86–89 (2005).

    Article CAS PubMed  Google Scholar 

  128. Clokie, M. R. J. et al. Transcription of a 'photosynthetic' T4-type phage during infection of a marine cyanobacterium.Environ. Microbiol.8, 827–835 (2006).

    Article CAS PubMed  Google Scholar 

  129. Sullivan, M. B. et al. Prevalence and evolution of core photosystem II genes in marine cyanobacterial viruses and their hosts.PLoS Biol.4, 1344–1357 (2006).

    Article CAS  Google Scholar 

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

    Article CAS  Google Scholar 

  131. Breitbart, M. et al. Genomic analysis of uncultured marine viral communities.Proc. Natl Acad. Sci. USA99, 14250–14255 (2002).

    Article CAS PubMed PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  133. Angly, F. E. et al. The marine viromes of four oceanic regions.PLoS Biol.4, 2121–2131 (2006).

    Article CAS  Google Scholar 

  134. Culley, A. I., Lang, A. S. & Suttle, C. A. High diversity of unknown picorna-like viruses in the sea.Nature424, 1054–1057 (2003).

    Article CAS PubMed  Google Scholar 

  135. Culley, A. I. & Steward, G. F. New genera of RNA viruses in subtropical seawater inferred from polymerase gene sequences.Appl. Environ. Microbiol. July 2007 (doi: 10.1128/AEM.01065-07).

    Article CAS PubMed PubMed Central  Google Scholar 

  136. Culley, A. I., Lang, A. S. & Suttle, C. A. Metagenomic analysis of coastal RNA virus communities.Science312, 1795–1798 (2006).

    Article CAS PubMed  Google Scholar 

  137. Seshadri, R., Kravitz, S. A., Smarr, L., Gilna, P. & Frazier, M. CAMERA: a community resource for metagenomics.PLoS Biol.5, 394–397 (2007).

    Article CAS  Google Scholar 

  138. Alonso, C. & Pernthaler, J.Roseobacter and SAR11 dominate microbial glucose uptake in coastal North Sea waters.Environ. Microbiol.8, 2022–2030 (2006).

    Article CAS PubMed  Google Scholar 

  139. Mary, I. et al. SAR11 dominance among metabolically active low nucleic acid bacterioplankton in surface waters along an Atlantic meridional transect.Aquat. Microb. Ecol.45, 107–113 (2006).

    Article  Google Scholar 

  140. Malmstrom, R. R., Kiene, R. P., Cottrell, M. T. & Kirchman, D. L. Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the North Atlantic ocean.Appl. Environ. Microbiol.70, 4129–4135 (2004).

    Article CAS PubMed PubMed Central  Google Scholar 

  141. Malmstrom, R. R., Cottrell, M. T., Elifantz, H. & Kirchman, D. L. Biomass production and assimilation of dissolved organic matter by SAR11 bacteria in the Northwest Atlantic Ocean.Appl. Environ. Microbiol.71, 2979–2986 (2005).

    Article CAS PubMed PubMed Central  Google Scholar 

  142. Hewson, I. & Fuhrman, J. A. Characterization of lysogens in bacterioplankton assemblages of the Southern California Borderland.Microb. Ecol.53, 631–638 (2007).

    Article PubMed  Google Scholar 

  143. Gonzalez, J. M. et al. Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom.Appl. Environ. Microbiol.66, 4237–4246 (2000).

    Article CAS PubMed PubMed Central  Google Scholar 

  144. Suzuki, M. T. et al. Phylogenetic screening of ribosomal RNA gene-containing clones in bacterial artificial chromosome (BAC) libraries from different depths in Monterey Bay.Microb. Ecol.48, 473–488 (2004).

    Article CAS PubMed  Google Scholar 

  145. Selje, N., Simon, M. & Brinkhoff, T. A newly discoveredRoseobacter cluster in temperate and polar oceans.Nature427, 445–448 (2004).

    Article CAS PubMed  Google Scholar 

  146. Wagner-Dobler, I. & Biebl, H. Environmental biology of the marineRoseobacter lineage.Annu. Rev. Microbiol.60, 255–280 (2006).

    Article CAS PubMed  Google Scholar 

  147. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea.Science304, 66–74 (2004).

    Article CAS PubMed  Google Scholar 

  148. Tomaru, Y., Tarutani, K., Yamaguchi, M. & Nagasaki, K. Quantitative and qualitative impacts of viral infection on aHeterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan.Aquat. Microb. Ecol.34, 227–238 (2004).

    Article  Google Scholar 

  149. Gobler, C. J., Anderson, O. R., Gastrich, M. D. & Wilhelm, S. W. Ecological aspects of viral infection and lysis in the harmful brown tide algaAureococcus anophagefferens.Aquat. Microb. Ecol.47, 25–36 (2007).

    Article  Google Scholar 

  150. Borderia, A. V. & Elena, S. F.r- and K-selection in experimental populations of vesicular stomatitis virus.Infect. Genet. Evol.2, 137–143 (2002).

    Article PubMed  Google Scholar 

  151. Wichman, H. A., Wichman, J. & Bull, J. J. Adaptive molecular evolution for 13,000 phage generations: a possible arms race.Genetics170, 19–31 (2005).

    Article CAS PubMed PubMed Central  Google Scholar 

  152. Tai, V. et al. Characterization of HaRNAV, a single-stranded RNA virus causing lysis ofHeterosigma akashiwo (Raphidophyceae).J. Phycol.39, 343–352 (2003).

    Article CAS  Google Scholar 

  153. Mizumoto, H., Tomaru, Y., Takao, Y., Shirai, Y. & Nagasaki, K. Intraspecies host specificity of a single-stranded RNA virus infecting a marine photosynthetic protist is determined at the early steps of infection.J. Virol.81, 1372–1378 (2007).

    Article CAS PubMed  Google Scholar 

  154. Brussaard, C. P. D., Noordeloos, A. A. M., Sandaa, R. A., Heldal, M. & Bratbak, G. Discovery of a dsRNA virus infecting the marine photosynthetic protistMicromonas pusilla.Virology319, 280–291 (2004).

    Article CAS PubMed  Google Scholar 

  155. 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  Google Scholar 

  156. Sandaa, R. A., Heldal, M., Castberg, T., Thyrhaug, R. & Bratbak, G. Isolation and characterization of two viruses with large genome size infectingChrysochromulina ericina (Prymnesiophyceae) andPyramimonas orientalis (Prasinophyceae).Virology290, 272–280 (2001).

    Article CAS PubMed  Google Scholar 

  157. Brussaard, C. P. D., Short, S. M., Frederickson, C. M. & Suttle, C. A. Isolation and phylogenetic analysis of novel viruses infecting the phytoplanktonPhaeocystis globosa (Prymnesiophyceae).Appl. Environ. Microbiol.70, 3700–3705 (2004).

    Article CAS PubMed PubMed Central  Google Scholar 

  158. Nagasaki, K. & Yamaguchi, M. Isolation of a virus infectious to the harmful bloom causing microalgaHeterosigma akashiwo (Raphidophyceae).Aquat. Microb. Ecol.13, 135–140 (1997).

    Article  Google Scholar 

  159. Weinbauer, M. G., Brettar, I. & Hofle, M. G. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters.Limnol. Oceanogr.48, 1457–1465 (2003).

    Article  Google Scholar 

  160. McDaniel, L. & Paul, J. H. Effect of nutrient addition and environmental factors on prophage induction in natural populations of marineSynechococcus species.Appl. Environ. Microbiol.71, 842–850 (2005).

    Article CAS PubMed PubMed Central  Google Scholar 

  161. Ortmann, A. C., Lawrence, J. E. & Suttle, C. A. Lysogeny and lytic viral production during a bloom of the cyanobacteriumSynechococcus spp.Microb. Ecol.43, 225–231 (2002).

    Article CAS PubMed  Google Scholar 

  162. Suttle, C. A. inHandbook of Methods in Aquatic Microbial Ecology (eds Kemp, P. F., Sherr, B. F., Sherr, E. B. & Cole, J. J.) 121–134 (Lewis, Boca Raton, 1993).

    Google Scholar 

  163. Borsheim, K. Y., Bratbak, G. & Heldal, M. Enumeration and biomass estimation of planktonic bacteria and viruses by transmission electron microscopy.Appl. Environ. Microbiol.56, 352–356 (1990).

    CAS PubMed PubMed Central  Google Scholar 

  164. Hara, S., Terauchi, K. & Koike, I. Abundance of viruses in marine waters — assessment by epifluorescence and transmission electron-microscopy.Appl. Environ. Microbiol.57, 2731–2734 (1991).

    CAS PubMed PubMed Central  Google Scholar 

  165. Weinbauer, M. G. & Suttle, C. A. Comparison of epifluorescence and transmission electron microscopy for counting viruses in natural marine waters.Aquat. Microb. Ecol.13, 225–232 (1997).

    Article  Google Scholar 

  166. Tomaru, Y. & Nagasaki, K. Flow cytometric detection and enumeration of DNA and RNA viruses infecting marine eukaryotic microalgae.J. Oceanogr.63, 215–221 (2007).

    Article CAS  Google Scholar 

  167. Morales, C. E. Carbon and nitrogen content of copepod fecal pellets — effect of food concentration and feeding behavior.Mar. Ecol. Prog. Ser36, 107–114 (1987).

    Article CAS  Google Scholar 

  168. Frangoulis, C., Christou, E. D. & Hecq, J. H. Comparison of marine copepod outfluxes: nature, rate, fate and role in the carbon and nitrogen cycles.Adv. Mar. Biol.47, 253–309 (2005).

    Article CAS PubMed  Google Scholar 

  169. Caron, D. A. et al. The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda.Deep-Sea Res. I42, 943–972 (1995).

    Article CAS  Google Scholar 

  170. Fukuda, H., Sohrin, R., Nagata, T. & Koike, I. Size distribution and biomass of nanoflagellates in meso- and bathypelagic layers of the subarctic Pacific.Aquat. Microb. Ecol.46, 203–207 (2007).

    Article  Google Scholar 

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Acknowledgements

Thanks are owed to T. F. Thingstad for discussions on the biological pump. The comments of C. Pedros-Alio, K. E. Wommack, C. Winter and S. W. Wilhelm are much appreciated, as well as discussions with A. M. Chan, C. Chenard, J. L. Clasen, M. Fischer, J. Labonte, J. Payet and members of the Scientific Commitee on Oceanic Research Marine Virus working group.

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  1. Departments of Earth and Ocean Sciences, University of British Columbia, Botany, and Microbiology and Immunology, 1461 BioSciences, 6270 University Boulevard, Vancouver, V6T 1Z4, British Columbia, Canada

    Curtis A. Suttle

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DATABASES

Entrez Genome

IHNV

VVHSV

WSSV

Entrez Genome Project

Emiliania huxleyi

Micromonas pusilla

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Glossary

Virosphere

The portion of the Earth in which viruses occur or which is affected by viruses; sometimes called the viriosphere.

Heterotrophic

Describes an organism that uses organic compounds for both energy and growth.

Autotrophic

Describes an organism that uses inorganic compounds for both energy and growth. In the oceans phytoplankton are the most common autotrophs.

Biome

An ecological area that contains similar groupings or communities of organisms.

Diel

A 24-hour period that corresponds to a cycle of light and darkness.

Pycnocline

The depth of the ocean at which the maximum change in density occurs owing to changes in the temperature or salinity.

Viral shunt

The viral-mediated movement of nutrients from organisms to pools of dissolved and non-living particulate organic matter.

Photic zone

The area of the ocean to which light penetrates.

Pyrosequencing

A high-throughput method for sequencing DNA, in which light is emitted each time a nucleotide is incorporated into a complimentary strand of DNA.

Virioplankton

Composed of un-attached (free) viruses in marine waters or freshwaters. Nominally defined as nucleic-acid-containing particles that can pass through a 200-nm pore-size filter.

Protist

A eukaryotic photosynthetic and heterotrophic organism that belongs to the kingdom Protista.

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