, Volume 47, Issue 1, pp 1–8 | Cite as

Coral-virus interactions: A double-edged sword?

  • Madeleine J. H. van OppenEmail author
  • Jo-Ann Leong
  • Ruth D. Gates
Review article


Marine viruses were little studied until 1989, when they were discovered to be extremely abundant in the sea. Virology is now a growing field of science in coral reef research, largely related to an increase in the frequency of coral bleaching events and other coral diseases. Because viruses are obligate symbionts, they are generally perceived as parasitic and harmful to their hosts. However, evidence that viruses confer benefits to their hosts is growing and their role as mutualists is emerging. Here we review both the detrimental and beneficial aspects of viral infections and argue that as the field of coral virology expands, in addition to their pathogenicity, the idea that viruses represent functionally beneficial components of the coral holobiont be considered.


Coral bleaching mutualism parasitism symbiosis Scleractinia 


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  1. Agranovsky, A.A., Lesemann, D.E., Maiss, E., Hull, R., and Atabekov, J.G. 1995. “Rattlesnake” structure of a filamentous plant RNA virus built of two capsid proteins.Proceedings of the National Academy of Sciences, USA 92: 2470–2473.CrossRefGoogle Scholar
  2. Ainsworth, T.D., Kvennefors, E.C., Blackall, L.L., Fine, M., and Hoegh-Guldberg, O. 2007. Disease and cell death in white syndrome of Acroporid corals on the Great Barrier Reef.Marine Biology 151: 19–29.CrossRefGoogle Scholar
  3. Ajayi, O. and Dewar, A.M. 1982. The effect of barley yellow dwarf virus on honeydew production by the cereal aphids,Sitobion avenae andMetopolophium dirhodum.Annals of Applied Biology 100: 203–212.CrossRefGoogle Scholar
  4. Barber, J., Chapman, D.J., and Telfer, A. 1987. Characterisation of a photosystem II reaction centre isolated from chloroplasts ofPisum sativum.FEBS Letters 220: 67–73.CrossRefGoogle Scholar
  5. Bergh, O., Borsheirn, K.Y., Bratbak, G., and Heldal, M. 1989. High abundance of viruses found in aquatic environments.Nature 340: 467–468.CrossRefPubMedGoogle Scholar
  6. Bigot, Y., Rabouille, A., Doury, G., Sizaret, P.Y., Delbost, F., Hamelin, M.H., and Periquet, G. 1997. Biological and molecular features of the relationships betweenDiadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host,Acrolepiopsis assectella.Journal of General Virology 78: 1149–1163.PubMedGoogle Scholar
  7. Blua, M.J. and Perring, T.M. 1992. Alatac production and population increase of aphid vectors on virus-infected host plants.Oecologia 92: 65–70.CrossRefGoogle Scholar
  8. Breitbart, M., Felts, B., Kelley, S., Mahaffy, J.M., Nulton, J., Salamon, P., and Rohwer, F. 2004. Diversity and population structure of a near-shore marine-sediment viral community.Proceedings of the Royal Society of London — Series B: Biological Sciences 271: 565–574.CrossRefPubMedGoogle Scholar
  9. Breitbart, M., Salamon, P., Andresen, B., Mahaffy, J.M., Segall, A.M., Mead, M., Azam, F., and Rohwer, F. 2002. Genomic analysis of uncultured marine viral communities.Proceedings of the National Academy of Science. USA 99: 14250–14255.CrossRefGoogle Scholar
  10. Brussaard, C.P.D. 2004. Viral control of phytoplankton populations — a review.Eukaryotic Microbiology 51: 125–138.CrossRefGoogle Scholar
  11. Buchel, C. and Wilhelm, C. 1993.In vivo analysis of slow chlorophyll fluorescence induction kinetics in algae: progress, problems and perspectives.Photochemistry and Photobiology 58: 137–148.CrossRefGoogle Scholar
  12. Cervino, J.M., Hayes, R., Goreau, T.J., and Smith, G.W. 2004. Zooxanthellae regulation in Yellow Blotch/Band and other coral diseases contrasted with temperature related bleaching:In situ destruction vs expulsion.Symbiosis 37: 63–85.Google Scholar
  13. Chang, P.H., Kuo, S.T., Lai, S.H., Yang, H.S., Ting, Y.Y., Hsu, C.L., and Chen, H.C. 2005. Herpes-like virus infection causing mortality of cultured abaloneHaliotis diversicolor supertexta in Taiwan.Diseases of Aquatic Organisms 65: 23–27.CrossRefPubMedGoogle Scholar
  14. Cochlan, W.P., Wikner, J., Steward, G.F., Smith, D.C., and Azam, F. 1993. Spatial distribution of viruses, bacteria and chlorophyll a in neritic, oceanic and estuarine environments.Marine Ecology Progress Series 92: 77–87.CrossRefGoogle Scholar
  15. Comps, M. 1988. Epizootic diseases of oysters associated with viral infections. In:Disease Processes In Marine Bivalve Mollusks. Fisher, W.S., ed. American Fisheries Society, Bethesda, MD. pp. 23–37.Google Scholar
  16. Davy, J.E. and Patten, N.L. 2007. Morphological diversity of virus-like particles within the surface microlayer of scleractinian corals.Aquatic Microbial Ecology 47: 37–44.CrossRefGoogle Scholar
  17. Davy, S.K., Burchett, S.G., Dale, A.L., Davies, P., Davy, J.E., Muncke, C., Hoegh-Guldberg, O., and Wilson, W.H. 2006. Viruses: agents of coral disease?Diseases of Aquatic Organisms 69: 101–110.CrossRefPubMedGoogle Scholar
  18. Fereres, A., Lister, R.M., Araya, J.E., and Foster, J.E. 1989. Development and reproduction of the English grain aphid (Homoptera: Aphididae) on wheat cultivars infected with barley yellow dwarf virus.Environmental Entomology 18: 388–393.Google Scholar
  19. Friedman, C.S., Estes, R.M., Stokes, N.A., Burge, C.A., Hargove, J.S., Barber, B.J., Elston, R.A., Burreson, E.M., and Reece, K.S. 2005. Herpes virus in juvenile Pacific oystersCrassostrea gigas from Tomales Bay, California, coincides with summer mortality episodes.Diseases of Aquatic Organisms 63: 33–41.CrossRefPubMedGoogle Scholar
  20. Fuhrman, J.A. 1999. Marine viruses and their biogeochemical and ecological effects.Nature 399: 541–548.CrossRefPubMedGoogle Scholar
  21. Greenwood, A.D., Leib-Mösch, C., and Seifarth, W. 2005. Abyssl: A novel L2-like non-LTR retroelement of the snakelocks anemone (Anemonia sulcata).Cytogenetic and Genome Research 110: 553–558.CrossRefPubMedGoogle Scholar
  22. Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world’s coral reefs.Marine and Freshwater Research 50: 839–866.CrossRefGoogle Scholar
  23. Jiu, M., Zhou, X.P., Tong, L., Xu, J., Yang, X., Wan, F.H., and Liu, S.S. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly.PLoS ONE 2: e182.CrossRefPubMedGoogle Scholar
  24. Kojima, K.K., Kuma, K., Toh, H., and Fujiwara, H. 2006. Identification of rDNA-specific non-LTR retrotransposons in Cnidaria.Molecular Biology and Evolution 23: 1984–1993.CrossRefPubMedGoogle Scholar
  25. Lohr, J., Munn, C.B., and Wilson, W.H. 2007. Characterization of a latent virus-like infection of symbiotic zooxanthellae.Applied and Environmental Microbiology 73: 2976–2981.CrossRefPubMedGoogle Scholar
  26. Mann, N.H., Cook, A., Millard, A., Bailey, S., and Clokie, M. 2003. Bacterial photosynthesis genes in a virus.Nature 424: 741.CrossRefPubMedGoogle Scholar
  27. Márquez, L.M., Redman, R.S., Rodriguez, R.J., and Roossinck, M.J. 2007. A virus in a fungus in a plant: Three-way symbiosis required for thermal tolerance.Science 315: 513–515.CrossRefPubMedGoogle Scholar
  28. Meints, R.H., Van Etten, J.L., Kuczmarski, D., Lee, K., and Ang, B. 1981. Viral infection of the symbioticChlorella-like alga present inHydra viridis.Virology 113: 698–703.CrossRefPubMedGoogle Scholar
  29. Mills, A.M., Ward, M.E., Heyl, T.P., and Van Dover, C.L. 2005. Parasitism as a potential contributor to massive clam mortality at the Blake Ridge Diapir methane-hydrate seep.Journal ofthe Marine Biological Association of the UK 85: 1480–1497.Google Scholar
  30. Moran, N.A., Degnan, P.H., Santos, S.R., Dunbar, H.E., and Ochman, H. 2005. The players in a mutualistic symbiosis: Insects, bacteria, viruses, and virulence genes.Proceedings of the National Academy of Science. USA 102: 16919–16926.CrossRefGoogle Scholar
  31. Mühling, M., Fuller, N.J., Millard, A., Somerfield, P.J., Marie, D., Wilson, W.H., Scanlan, D.J., Post, A.F., Joint, I., and Mann, N.H. 2005. Genetic diversity of marineSynechococcus and cooccurring cyanophage communities: evidence for viral control of phytoplankton.Environmental Microbiology 7: 499–508.CrossRefPubMedGoogle Scholar
  32. Munn, C.B. 2006. Viruses as pathogens of marine organisms — from bacteria to whales.Journal of the Marine Biological Association ofthe UK 86: 453–467.CrossRefGoogle Scholar
  33. Musser, R.O., Hum-Musser, S.M., Felton, G.W., and Gergerich, R.C. 2003. Increased larval growth and preference for virus-infected leaves by the Mexican bean beetle,Epilaehna varivestis Mulsant, a plant virus vector.Journal of Insect Behavior 16: 247–256CrossRefGoogle Scholar
  34. Nathanson, N. and Griffin, D.E. 2007. Virus-cell interactions. In:Viral Pathogenesis and Immunity. Nathanson, N., ed. Academic Press, New York, pp. 41–44.Google Scholar
  35. O’Brien, T.L., Macleod, R., and Maclean, M.C. 1984. Absence of lytic virus in 2 species of symbiotic algae within the sea anemoneAnthopleura xanthogrammica (Coelenterata: Anthozoa).Transactions ofthe American Microscopical Society 103: 228–232.CrossRefGoogle Scholar
  36. Patten, N.L., Harrison, P.L., and Mitchell, J.G. 2008. Prevalence of virus-like particles within a staghom scleractinian coral (Acropora muricata) from the Great Barrier Reef. Coral Reefs Online early:DOI 1O.1007/s00338-00008-00356-00339.Google Scholar
  37. Patten, N.L., Seymour, J.R., and Mitchell, J.G. 2006. Flow cytometric analysis of virus-like particles and heterotrophic bacteria within coral-associated reef water.Journal of the Marine Biological Association of the UK 86: 563–566.CrossRefGoogle Scholar
  38. Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I., and Rosenberg, E. 2006. The Coral Probiotic Hypothesis.Environmental Microbiology 8: 2068–2073.CrossRefPubMedGoogle Scholar
  39. Rohwer, F., Seguritan, V., Azam, F., and Knowlton, N. 2002. Diversity and distribution of coral-associated bacteria.Marine Ecology Progress Series 243: 1–10.CrossRefGoogle Scholar
  40. Roossinck, M.J. 2005. Symbiosis versus competition in plant virus evolution.Nature Reviews Microbiology 3: 917–924.CrossRefPubMedGoogle Scholar
  41. Seaton, G.G.R., Hurry, V.M., and Rohozinsk, J. 1996. Novel amplification of non-photochemical chlorophyll fluorescence quenching following viral infection inChlorella.FEBS Letters 389: 319–323.CrossRefPubMedGoogle Scholar
  42. Seymour, J.R., Patten, N., Bourne, D.G., and Mitchell, J.G. 2005. Spatial dynamics of virus-like particles and heterotrophic bacteria within a shallow coral reef system.Marine Ecology Progress Series 288: 1–8.CrossRefGoogle Scholar
  43. Stat, M., Carter, D., and Hoegh-Guldberg, O. 2006. The evolutionary history ofSymbiodinium and scleractinian hosts — Symbiosis, diversity, and the effect of climate change.Perspectives in Plant Ecology. Evolution and Systematics 8: 23–43.CrossRefGoogle Scholar
  44. Suttle, C.A. 2005. Viruses in the sea.Nature 437: 356–361.CrossRefPubMedGoogle Scholar
  45. Van Etten, J.L., Meints, R.H., Burbank, D.E., Kuczmarski, D., Cuppels, D., and Lane, L.C. 1981. Isolation and characterization of a virus from intracellular green alga symbiotic withHydra viridis.Virology 113: 704–711.CrossRefPubMedGoogle Scholar
  46. Van Etten, J.L., Meints, R.H., Kuczmarski, D., Burbank, D.E., and Lee, K. 1982. Viruses of symbioticChlorella-like algae fromParamecium bursaria andHydra viridis.Proceedings of the National Academy of Science. USA 79: 3867–3871.CrossRefGoogle Scholar
  47. Villarreal, L.P. 2005.Viruses and The Evolution of Life. ASM Press, American Society for Microbiology, Washington, D.C.Google Scholar
  48. Warner, M.E., Fitt, W.K., and Schmidt, G.W. 1996. The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: A novel approach.Plant Cell Environment 19: 291–299.CrossRefGoogle Scholar
  49. Warner, M.E., Fitt, W.K., and Schmidt, G.W. 1999. Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching.Proceedings of the National Academy of Science 96: 8007–8012.CrossRefGoogle Scholar
  50. Webb, B.A., Strand, M.R., Dickey, S.E., Beck, M.H., Hilgarth, R.S., Barney, W.E., Kadash, K., Kroemer, J.A., Lindstrom, K.G., Rattanadechakul, W., Shelby, K.S., Thoetkiattikul, H., Turnbull, M.W., and Witherell, R.A. 2006. Polydnavirus genomes reflect their dual roles as mutualists and pathogens.Virology 347: 160–174.CrossRefPubMedGoogle Scholar
  51. Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H., and Rohwer, F. 2007. Metagenomic analysis of the microbial community associated with the coralPorites astreoides.Environmental Microbiology 9: 2707–2719.CrossRefPubMedGoogle Scholar
  52. Weigele, P.R., Pope, W.H., Pedulla, M.L., Houtz, J.M., Smith, A.L., Conway, J.F., King, J., Hatfull, G.F., Lawrence, J.G., and Hendrix, R.W. 2007. Genomic and structural analysis of Syn9, a cyanophage infecting marineProchlorococcus andSynechococcus.Environmental Microbiology 9: 1675–1695.CrossRefPubMedGoogle Scholar
  53. Wilson, W.H. and Chapman, D.M. 2001. Observation of virus-like particles in thin sections of the plumose anemone,Metridium senile.Journal of the Marine Biological Association of the UK 81: 879–880.CrossRefGoogle Scholar
  54. Wilson, W.H., Dale, A.L., Davy, J.E., and Davy, S.K. 2005. An enemy within? Observations of virus-like particles in reef corals.Coral Reefs 24: 145–148.CrossRefGoogle Scholar
  55. Wilson, W.H., Francis, I., Ryan, K., and Davy, S.K. 2001. Temperature induction of viruses in symbiotic dinoflagellates.Aquatic Microbial Ecology 255: 99–102.CrossRefGoogle Scholar
  56. Wommack, K.E. and Colwell, R.R. 2000. Virioplankton: Viruses in Aquatic Ecosystems.Microbiology and Molecular Biology Reviews 64: 69–114.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2009

Authors and Affiliations

  • Madeleine J. H. van Oppen
    • 1
    Email author
  • Jo-Ann Leong
    • 2
  • Ruth D. Gates
    • 2
  1. 1.Australian Institute of Marine ScienceTownsville MCAustralia
  2. 2.Hawaii Institute of Marine Biology, SOESTUniversity of HawaiiKaneoheUSA

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