Ecological Role of Viruses in Aquatic Ecosystems

Abstract

Over two decades of research have indicated that viruses play crucial roles in aquatic food webs as active constituents of the microbial loop and in the population ecology of both prokaryotic and eukaryotic microorganisms. Over the past 5 years, there has been a sharp increase in reported aquatic virus research, notably in the areas of freshwater viral ecology, viruses of eukaryotic microorganisms and viral genetic diversity. Recent studies of the interactions between viral infection, bacterivory and grazing have demonstrated the complex dynamics of viral infection within aquatic ecosystems. These reports have helped solidify our understanding of the environmental controls on viral abundance, impacts of viral infection upon host community structure and have elucidated new roles of viruses in biogeochemical cycles – such as photosystem gene expression. Previously unrecognised groups of viruses (ribonucleic acid viruses and single‐stranded deoxyribonucleic acid viruses) have also been revealed as diverse and active components of marine virioplankton assemblages.

Key Concepts:

  • Viruses are the most numerically dominant organisms on earth, and their abundance varies between habitats, often according to local primary productivity.

  • Both viral activity and bacterivory contribute significantly to bacterial mortality in aquatic ecosystems, which in turn influence global‐scale biogeochemical cycles.

  • Methodological advances, such as metagenomics and genomics, have greatly facilitated studies of marine viruses and resulted in key discoveries on viral diversity, viral–host gene transfer and viral influence on host cell physiology.

  • Photosystem genes are common in cyanophage and are hypothesised to enhance viral production rates.

  • Viral‐induced mortality may be a key factor in controlling or terminating algal blooms.

Keywords: virus; microbial loop; mortality; viriomics; diversity; aquatic

Figure 1.

Conceptualisation of the microbial loop incorporating viruses. Viruses cause mortality of all trophic levels, regenerating dissolved organic matter from phytoplankton, bacterioplankton and grazers.

Figure 2.

SYBR Green I stained plankton from Otisco Lake, upstate New York, prepared following the protocols of Noble and Fuhrman . The larger green dots are Bacteria and Archaea, whereas the smaller dots are viruses.

Figure 3.

Distribution of viruses (squares) and bacteria (triangles) with depth in the western (solid symbols) and eastern (open symbols) tropical North Atlantic Ocean (SJ0609 cruise, July 2006). Maximum virus abundance occurs in surface waters and is enhanced at the deep chlorophyll maximum relative to deeper waters. Viruses were enumerated by SYBR Green I staining and epifluorescence microscopy following protocols of Noble and Fuhrman .

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References

Angly F, Felts B, Breitbart M et al. (2006) The marine viromes of four oceanic regions. PLoS Biology 4: 2121–2131.

Bergh O, Borsheim KY, Bratbak G and Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340: 467–468.

Breitbart M, Felts B and Kelley S (2004) Diversity and population structure of a near‐shore marine‐sediment viral community. Proceedings. Biological Sciences/The Royal Society 271: 565–574.

Breitbart M, Salamon P, Andresen B et al. (2002) Genomic analysis of uncultured marine viral communities. Proceedings of the National Academy of Sciences of the USA 99: 14250–14255.

Brussaard CPD (2004) Viral control of phytoplankton populations – a review. Journal of Eukaryotic Microbiology 51: 125–138.

Culley A, Lang AS and Suttle CA (2003) High diversity of unknown picorna‐like viruses in the sea. Nature 424: 1054–1057.

Culley AI, Lang AS and Suttle CA (2006) Metagenomic analysis of coastal RNA virus communities. Science 312: 1795–1798.

Danovaro R, Corinaldesi C, Filippini M et al. (2008) Viriobenthos in freshwater and marine sediments: a review. Freshwater Biology 53: 1186–1213.

Edwards RA and Rohwer F (2005) Viral metagenomics. Nature Reviews in Microbiology 3: 504–510.

Filippini M and Middelboe M (2007) Viral abundance and genome size distribution in the sediment and water column of marine and freshwater ecosystems. FEMS Microbiology Ecology 60: 397–410.

Fuhrman JA (1992) Bacterioplankton roles in cycling of organic matter: the microbial food web. In: Falkowski PG and Woodhead AD (eds) Primary Productivity and Biogeochemical Cycles in the Sea. New York: Plenum Press.

Fuhrman JA and Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnology and Oceanography 40: 1236–1242.

Gobler CJ, Hutchins DA, Fisher NS, Cosper EM and Sanudo‐Wilhelmy SA (1997) Release and bioavailability of C, N, P, Se and Fe following viral lysis of a marine chrysophyte. Limnology and Oceanography 42: 1492–1504.

Lindell D, Jaffe JD, Coleman ML et al. (2007) Genome‐wide expression dynamics of a marine virus and host reveal features of co‐evolution. Nature 449: 83–86.

Liu Y‐M, Zhang Q‐Y, Yuan X‐P, Li Z‐Q and Gui J‐F (2006) Seasonal variation of virioplankton in a eutrophic shallow lake. Hydrobiologia 560: 323–334.

Llewellyn CA, Tarran GA, Galliene CP et al. (2008) Microbial dynamics during the decline of a spring diatom bloom in the Northeast Atlantic. Journal of Plankton Research 30: 261–273.

Lopez‐Bueno A, Tamames J, Velazquez D et al. (2009) High diversity of the viral community from an Antarctic lake. Science 326: 858–861.

Mann NH, Cook A, Millard A, Bailey S and Clokie M (2003) Bacterial photosynthesis genes in a virus. Nature 424: 741.

Massana R, del Campo J, Dinter C and Sommaruga R (2007) Crash of a population of the marine heterotrophic flagellate Cafeteria roenbergensis by viral infection. Environmental Microbiology 9: 2660–2669.

Maurice CF, Bouvier T, Comte J, Guillemette F and del Giorgio PA (2010) Seasonal variations of phage life strategies and bacterial physiological states in three northern temperate lakes. Environmental Microbiology 12: 628–641.

Mei ML and Danovaro R (2004) Virus production and life strategies in aquatic sediments. Limnology and Oceanography 49: 459–470.

Middelboe M and Glud RN (2006) Viral activity along a trophic gradient in a continental margin sediments off central Chile. Marine Biology Research 2: 41–51.

Middelboe M, Jacquet S and Weinbauer MG (2008) Viruses in freshwater ecosystems: an introduction to the exploration of viruses in new aquatic habitats. Freshwater Biology 53: 1069–1075.

Middelboe M and Jorgensen NOG (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall components. Journal of the Marine Biological Association of the United Kingdom 86: 605–612.

Nagasaki K and Yamaguchi M (1998) Intra‐species host specificity of HaV (Heterosigma akashiwo virus) clones. Aquatic Microbial Ecology 14: 109–112.

Noble RT and Fuhrman JA (1997) Virus decay and its causes in coastal waters. Applied and Environmental Microbiology 63: 77–83.

Noble RT and Fuhrman JA (1998) Use of SYBR Green I rapid epifluoresence counts of marine viruses and bacteria. Aquatic Microbial Ecology 14: 113–118.

Parada V, Herndl GJ and Weinbauer MG (2006) Viral burst size of heterotrophic prokaryotes in aquatic ecosystems. Journal of the Marine Biological Association of the United Kingdom 86: 613–621.

Paul JH (2008) Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME Journal 2: 579–589.

Paul JH and Sullivan MB (2005) Marine phage genomics: what have we learned? Current Opinion in Microbiology 16: 299–307.

Pienaar RN (1976) Virus‐like particles in three species of phytoplankton from San Juan Island, Washington. Phycologia 15: 185–190.

Ram ASP, Boucher D, Sime‐Ngando T, Debroas D and Romagoux JC (2005) Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: coupling with temperature. Microbial Ecology 50: 64–72.

Rohwer F, Segall A, Steward G et al. (2000) The complete genomic sequence of the marine phage Roseophage SI01 shares homology with nonmarine phages. Limnology and Oceanography 45: 408–418.

Sandaa R‐A, Clokie MRJ and Mann NH (2008) Photosynthetic genes in viral populations with a large genomic size range from Norwegian coastal waters. FEMS Microbiology Ecology 63: 2–11.

Sandaa R‐A, Gomez‐Consarnau L, Pinhassi J et al. (2009) Viral control of bacterial biodiversity – evidence from a nutrient‐enriched marine mesocosm experiment. Environmental Microbiology 11: 2585–2597.

Sawstrom C, Anesio MA, Graneli W and Laybourn‐Parry J (2006) Seasonal viral loop dynamics in two ultraoligotrophic Antarctic freshwater lakes. Microbial Ecology 53: 1–11.

Schwalbach MS, Hewson I and Fuhrman JA (2004) Viral effects on bacterial community composition in marine plankton microcosms. Aquatic Microbial Ecology 34: 117–127.

Sharon I, Alperovitch A, Rohwer F et al. (2009) Photosystem I gene cassettes are present in marine virus genomes. Nature 461: 258–262.

Sharon I, Tzahor S, Williamson SJ et al. (2007) Viral photosynthesis reaction center genes and transcripts in the marine environment. ISME Journal 1: 492–501.

Tarutani K, Nagasaki K and Yamaguchi M (2000) Viral impacts on total abundance and clonal composition of the harmful bloom‐forming phytoplankton Heterosigma akashiwo. Applied and Environmental Microbiology 66: 4916–4920.

Thingstad TF and Lignell R (1997) A theoretical approach to the question of how trophic interactions control carbon demand, growth rate, abundance and diversity. Aquatic Microbial Ecology 13: 19–27.

Weinbauer MG, Brettar I and Hofle MG (2003) Lysogeny and virus‐induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnology and Oceanography 48: 1457–1465.

Weinbauer MG, Fuks D and Peduzzi P (1993) Distribution of viruses and dissolved DNA along a coastal trophic gradient in the northern Adriatic Sea. Applied and Environmental Microbiology 59: 4074–4082.

Weinbauer MG and Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environmental Microbiology 6: 1–11.

Wilhelm SW and Suttle CA (1999) Viruses and nutrient cycles in the sea. Bioscience 49: 781–788.

Wilson WH, Tarran GA, Schroeder D et al. (2002) Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. Journal of the Marine Biological Association of the United Kingdom 82: 369–377.

Winget DM and Wommack KE (2009) Diel and daily fluctuations in virioplankton production in coastal ecosystems. Environmental Microbiology 11: 2904–2914.

Winter C, Smit A, Herndl GJ and Weinbauer MG (2004) Impact of virioplankton on archaeal and bacterial community richness as assessed in seawater batch cultures. Applied and Environmental Microbiology 70: 803–813.

Wommack KE, Hill RT, Kessel M, RusskCohen E and Colwell RR (1999a) Distribution of viruses in the Chesapeake Bay. Applied and Environmental Microbiology 58: 2965–2970.

Wommack KE, Ravel J, Hill RT, Chun J and Colwell RR (1999b) Population dynamics of Chesapeake Bay virioplankton: total‐community analysis by pulsed‐field gel electrophoresis. Applied and Environmental Microbiology 65: 231–240.

Further Reading

Comeau AM, Hatfull GF, Krisch HM et al. (2008) Exploring the prokaryotic virosphere. Research in Microbiology 159: 306–313.

Hambly E and Suttle CA (2005) The viriosphere, diversity and genetic exchange within phage communities. Current Opinion in Microbiology 8: 444–450.

Herndl GJ, Agogue H, Baltar F et al. (2008) Regulation of aquatic microbial processes: the ‘microbial loop’ of the sunlit surface waters and the dark ocean dissected. Aquatic Microbial Ecology 53: 59–68.

Rohwer F and Vega Thurber R (2009) Viruses manipulate the marine environment. Nature 459: 207–212.

Sandaa R‐A (2008) Burden or benefit? Virus‐host interactions in the marine environment. Research in Microbiology 159: 374–381.

Sawstrom C, Lisle J, Anesio MA, Priscu JC and Laybourn‐Parry J (2008) Bacteriophage in polar inland waters. Extremophiles 12: 167–175.

Sime‐Ngando T and Colombet J (2009) Virus et prohages dans les ecosystemes aquatiques. Reviews in Canadian Microbiology 55: 95–109.

Suttle CA (2007) Marine viruses – major players in the global ecosystems. Nature Reviews in Microbiology 5: 801–812.

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How to Cite close
Hewson, Ian, Chow, Cheryl, and Fuhrman, Jed A(Dec 2010) Ecological Role of Viruses in Aquatic Ecosystems. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022546]