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:

The good viruses: viral mutualistic symbioses

Key Points

  • Viruses have traditionally been thought of as pathogens, but many confer a benefit to their hosts and some are essential for the host life cycle.

  • The polydnaviruses of endoparasitoid wasps have evolved with their hosts to become essential. Many of the viral genes are now encoded in the host nucleus.

  • Endogenous retroviruses are abundant in many genomes of higher eukaryotes, and some have been involved in the evolution of their hosts, such as placental mammals.

  • Some mammalian viruses can protect their hosts from infection by related viruses or from disease caused by completely unrelated pathogens, such as bubonic plague.

  • Viruses can protect their hosts by killing off competitors, as is seen with the killer viruses in yeasts.

  • A fungal virus confers thermal tolerance to a plant in a complex symbiosis involving its fungal host and the plant that the fungus colonizes.

  • Several acute plant viruses confer conditional mutualism by enhancing drought tolerance in plants.

  • Insect viruses have numerous mutualistic relationships with their hosts; in addition, viruses play parts in bacterium–insect mutualisms.

Abstract

Although viruses are most often studied as pathogens, many are beneficial to their hosts, providing essential functions in some cases and conditionally beneficial functions in others. Beneficial viruses have been discovered in many different hosts, including bacteria, insects, plants, fungi and animals. How these beneficial interactions evolve is still a mystery in many cases but, as discussed in this Review, the mechanisms of these interactions are beginning to be understood in more detail.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: The relationship between polydnaviruses, wasps and caterpillars.
Figure 2: Viruses as natural weapons.
Figure 3: A three-way mutualistic symbiosis.

Similar content being viewed by others

References

  1. Beijerinck, M. W. in Phylopathological Classics No. 7 (ed. Johnson, J.) (American Phytopathological Society Press, St. Paul, 1898). This paper describes the discovery of the first known virus, TMV.

    Google Scholar 

  2. Shen, H.-H. The challenge of discovering beneficial viruses. J. Med. Microbiol. 58, 531–532 (2009).

    Article  PubMed  Google Scholar 

  3. Canchaya, C., Proux, C., Fournous, G., Bruttin, A. & Brüssow, H. Prophage genomics. Microbiol. Mol. Biol. Rev. 67, 238–276 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. deBary, H. A. Die Erscheinung der Symbiose. (Strasburg, 1879) (in German).

    Google Scholar 

  5. Roossinck, M. J. Symbiosis versus competition in the evolution of plant RNA viruses. Nature Rev. Microbiol. 3, 917–924 (2005).

    Article  CAS  Google Scholar 

  6. Villarreal, L. P. Viruses and the Evolution of Life (American society for Microbiology Press, Washington DC, 2005).

    Book  Google Scholar 

  7. Koonin, E. V. On the origin of cells and viruses: a comparative-genomic perspective. Isr. J. Ecol. Evol. 52, 299–318 (2006).

    Article  Google Scholar 

  8. Webb, B. A. in The Insect Viruses (eds. Miller, L. K. & Ball, L. A.) 105–139 (Plenum, New York, 1998).

    Book  Google Scholar 

  9. Webb, B. A. et al. Polydnavirus genomes reflect their dula roles as mutualists and pathogens. Virology 347, 160–174 (2006).

    Article  CAS  PubMed  Google Scholar 

  10. Stoltz, D. B. & Whitfield, J. B. Making nice with viruses. Science 323, 884–885 (2009).

    Article  PubMed  Google Scholar 

  11. Bézier, A. et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926–930 (2009).

    Article  CAS  PubMed  Google Scholar 

  12. Edson, K. M., Vinson, S. B., Stoltz, D. B. & Summers, M. D. Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid's host. Science 211, 582–583 (1981).

    Article  CAS  PubMed  Google Scholar 

  13. Stasiak, K., Renault, S., Federici, B. A. & Bigot, Y. Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J. Insect Physiol. 51, 103–115 (2005).

    Article  CAS  PubMed  Google Scholar 

  14. Renault, S., Stasiak, K., Federici, B. & Bigot, Y. Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J. Insect Physiol. 51, 137–148 (2005).

    Article  CAS  PubMed  Google Scholar 

  15. Lawrence, P. O. Purification and partial characterization of an entomopoxvirus (DlEPV) from a parasitic wasp of tephritid fruit flies. J. Insect Physiol. 2, 1–12 (2002).

    Google Scholar 

  16. Whitfield, J. B. & Asgari, S. Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J. Insect Physiol. 49, 397–405 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Bigot, Y., Samain, S., Augé-Gouillou, C. & Federici, B. A. Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis. BMC Evol. Biol. 18, 253 (2008).

    Article  CAS  Google Scholar 

  18. Volkoff, A.-N. et al. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog. 6, e1000923 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Kazazian, H. H. Jr. Mobile elements: drivers of genome evolution. Science 303, 1626–1632 (2004).

    Article  CAS  PubMed  Google Scholar 

  21. Ryan, F. P. Human endogenous retroviruses in health and disease: a symbiotic perspective. J. R. Soc. Med. 97, 560–565 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Eiden, M. V. Endogenous retroviruses — aiding and abetting genomic plasticity. Cell. Mol. Life Sci. 65, 3325–3328 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Maksakova, I. A., Mager, D. L. & Reiss, D. Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell. Mol. Life Sci. 65, 3329–3347 (2008).

    Article  CAS  PubMed  Google Scholar 

  24. Blikstad, V., Benachenhou, F., Sperber, G. O. & Blomberg, J. Evolution of human endogenous retroviral sequences: a conceptual account. Cell. Mol. Life Sci. 65, 3348–3365 (2008).

    Article  CAS  PubMed  Google Scholar 

  25. Ruprecht, K., Mayer, J., Sauter, M., Roemer, K. & Mueller-Lantzsch, N. Endogenous retroviruses and cancer. Cell. Mol. Life Sci. 65, 3366–3382 (2008).

    Article  CAS  PubMed  Google Scholar 

  26. Stocking, C. & Kozak, C. A. Murine endogenous retroviruses. Cell. Mol. Life Sci. 65, 3383–3398 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Wilson, C. A. Porcine endogenous retroviruses and xenotransplantation. Cell. Mol. Life Sci. 65, 3399–3412 (2008).

    Article  CAS  PubMed  Google Scholar 

  28. Tarlinton, R., Meers, J. & Young, P. Biology and evolution of the endogenous koala retrovirus. Cell. Mol. Life Sci. 65, 3413–3421 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Arnaud, F., Varela, M., Spencer, T. E. & Palmarini, M. Coevolution of endogenous Betaretroviruses of sheep and their host. Cell. Mol. Life Sci. 65, 3422–3432 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jern, P. & Coffin, J. M. Effects of retroviruses on host genome function. Annu. Rev. Genet. 42, 709–732 (2008).

    Article  CAS  PubMed  Google Scholar 

  31. Ryan, F. Virolution (HarperCollins, London, 2009). This book contains numerous stories about beneficial viruses and how viruses have shaped the evolution of their hosts.

    Google Scholar 

  32. Tarlinton, R. E., Meers, J. & Young, P. R. Retroviral invasion of the koala genome. Nature 442, 79–81 (2006). This paper documents the only known ongoing endogenization of a retrovirus.

    Article  CAS  PubMed  Google Scholar 

  33. Oliveira, N. M., Satija, H., Kouwenhoven, I. A. & Eiden, M. V. Changes in viral protein function that accompany retroviral endogenization. Proc. Natl Acad. Sci. USA 104, 17506–17511 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Stoye, J. P. Koala retrovirus: a genome invasion in real time. Genome Biol. 7, 241 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Harris, J. R. The evolution of placental mammals. FEBS Lett. 295, 3–4 (1991).

    Article  CAS  PubMed  Google Scholar 

  36. Dunlap, K. A. et al. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc. Natl Acad. Sci. USA 103, 14390–14395 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ryan, F. P. An alternative approach to medical genetics based on modern evolutionary biology. Part 4: HERVs in cancer. J. R. Soc. Med. 102, 474–480 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Hohn, T. et al. in Plant Virus Evolution (ed. Roossinck, M. J.) 53–81 (Springer, Heidelberg, 2008).

    Book  Google Scholar 

  39. Staginnus, C. et al. Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biol. 7, 24 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ruiz-Ferrer, V. & Voinnet, O. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485–510 (2009).

    Article  CAS  PubMed  Google Scholar 

  41. Wu, Q., Wang, X. & Ding, S.-W. Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8, 12–15 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Noreen, F., Akbergenov, R., Hohn, T. & Richert-Pöggeler, K. R. Distinct expression of endogenous Petunia vein clearing virus and the DNA transposon dTph1 in two Petunia hybrida lines is correlated with differences in histone modification and siRNA production. Plant J. 50, 219–229 (2007).

    Article  CAS  PubMed  Google Scholar 

  43. Gayral, P. et al. A single Banana streak virus integration event in the banana genome as the origin of infectious endogenous pararetrovirus. J. Virol. 82, 6697–6710 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. de la Maza, L. M. & Carter, B. J. Inhibition of adenovirus oncogenicity in hamsters by adeno-associated virus DNA. J. Natl. Cancer Inst. 67, 1323–1326 (1981).

    CAS  PubMed  Google Scholar 

  45. Heringlake, S. et al. GB virus C/hepatitis G virus infection: a favorable prognostic factor in human immunodeficiency virus-infected patients? J. Infect. Dis. 177, 1734–1726 (1998).

    Article  Google Scholar 

  46. Tillman, H. L. et al. Infection with GB virus C and reduced mortality among HIV-infected patients. N. Engl. J. Med. 345, 715–724 (2001).

    Article  Google Scholar 

  47. King, C. A., Baillie, J. & Sinclair, J. H. Human cytomegalovirus modulation of CCR5 expression on myeloid cells affects susceptibility to human immunodeficiency virus type 1 infection. J. Gen. Virol. 87, 2171–2180 (2006).

    Article  CAS  PubMed  Google Scholar 

  48. Deterding, K. et al. Hepatitis A virus infection suppresses hepatitis C virus replication and may lead to clearance of HCV. J. Hepatol. 45, 770–778 (2006).

    Article  CAS  PubMed  Google Scholar 

  49. Oldstone, M. B. A. Prevention of type I diabetes in nonobese diabetic mice by virus infection. Science 239, 500–502 (1988).

    Article  CAS  PubMed  Google Scholar 

  50. Lin, E. & Nemunaitis, J. Oncolytic viral therapies. Cancer Gene Ther. 11, 643–664 (2004).

    Article  CAS  PubMed  Google Scholar 

  51. Parato, K. A., Senger, D., Forsyth, P. A. J. & Bell, J. C. Recent progress in the battle between oncolytic viruses and tumours. Nature Rev. Cancer 5, 965–976 (2005).

    Article  CAS  Google Scholar 

  52. Liu, T.-C. & Kirn, D. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther. 15, 877–884 (2008).

    Article  CAS  PubMed  Google Scholar 

  53. Ottolino-Perry, K., Diallo, J.-S., Lichty, B. D., Bell, J. C. & McCart, J. A. Intelligent design: combination therapy with oncolytic viruses. Mol. Ther. 18, 251–263 (2010).

    Article  CAS  PubMed  Google Scholar 

  54. Barton, E. S. et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447, 326–330 (2007).

    Article  CAS  PubMed  Google Scholar 

  55. Lehnherr, H., Maguin, E., Jafri, S. & Yarmolinsky, M. B. Plasmid addiction genes of bacteriophage P1: doc, which causes cell death on curing of prophage, and phd, which prevents host death when prophage is retained. J. Mol. Biol. 233, 414–428 (1993).

    Article  CAS  PubMed  Google Scholar 

  56. Bossi, L., Fuentes, J. A., Mora, G. & Figueroa-Bossi, N. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185, 6467–6471 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Brown, S. P., Le Chat, L., De Paepe, M. & Taddei, F. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr. Biol. 16, 2048–2052 (2006).

    Article  CAS  PubMed  Google Scholar 

  58. Schmitt, M. J. & Breinig, F. The viral killer system in yeast: from molecular biology to application. FEMS Microbiol. Rev. 26, 257–276 (2002).

    Article  CAS  PubMed  Google Scholar 

  59. Magliani, W., Conti, S., Gerloni, M., Bertolotti, D. & Polonelli, L. Yeast killer systems. Clin. Microbiol. Rev. 10, 369–400 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Schmitt, M. J. & Breinig, F. Yeast viral killer toxins: lethality and self-protection. Nature Rev. Microbiol. 4, 212–221 (2006).

    Article  CAS  Google Scholar 

  61. McBride, R., Greig, D. & Travisano, M. Fungal viral mutualism moderated by ploidy. Evolution 62, 2372–2380 (2008).

    Article  PubMed  Google Scholar 

  62. Villarreal, L. P. Persistence pays: how viruses promote host group survival. Curr. Opin. Microbiol. 12, 467–472 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Malmstrom, C. M., McCullough, A. J., Johnson, H. A., Newton, L. A. & Borer, E. T. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145, 153–164 (2005).

    Article  PubMed  Google Scholar 

  64. Bianchine, P. J. & Russo, T. A. The role of epidemic infectious diseases in the discovery of America. Allergy Proc. 13, 225–232 (1992).

    Article  CAS  PubMed  Google Scholar 

  65. Mann, C. C. 1491: New Revelations of the Americas Before Columbus (Vintage Books, New York, 2006). This fascinating book gives an up-to-date assessment of how Europeans changed the American landscape forever, including the decimation of native populations by disease.

    Google Scholar 

  66. Campbell, J. Invisible Invaders: Smallpox and Other Diseases in Aboriginal Australia, 1780–1880 (Melbourne Univ. Press, Melbourne, 2007).

    Google Scholar 

  67. Liu, Y.-C., Linder-Basso, D., Hillman, B. I., Kaneso, S. & Milgroom, M. G. Evidence for interspecies transmission of viruses in natural populations of filamentous fungi in the genus Cryphonectria. Mol. Ecol. 12, 1619–1628 (2003).

    Article  PubMed  Google Scholar 

  68. Nuss, D. L. in Encyclopedia of Virology (eds Granoff, A. & Webster, R.) 580–585 (Elsevier, Amsterdam, 2008).

    Book  Google Scholar 

  69. Dawe, A. L. & Nuss, D. L. Hypoviruses and chestnut blight: exploiting viruses to understand and modulate fungal pathogenesis. Annu. Rev. Genetics 35, 1–29 (2001).

    Article  CAS  Google Scholar 

  70. Milgroom, M. G. & Cortesi, P. Biological control of chestnut blight with hypovirulence: a critical analysis. Annu. Rev. Phytopathol. 42, 311–338 (2004).

    Article  CAS  PubMed  Google Scholar 

  71. Buck, K. W., Brasier, C. M., Paoletti, M. & Crawford, L.J. in Genes in the Environment (eds Hails, R. S., Beringer, J. E. & Godfray, H. C. J.) 26–45 (Blackwell, Oxford, UK, 2001).

    Google Scholar 

  72. Zhao, T., Havens, W. M. & Ghabrial, S. A. Disease phenotype of virus-infected Helminthosporium victoriae is independent of overexpression of the cellular alcohol oxidase/RNA-binding protein Hv-p68. Phytopathology 96, 326–332 (2006).

    Article  CAS  PubMed  Google Scholar 

  73. Yu, X. et al. A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc. Natl Acad. Sci. USA 107, 8387–8392 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J. & Henson, J. M. Thermotholerance generated by plant/fungal symbiosis. Science 298, 1581 (2002).

    Article  CAS  PubMed  Google Scholar 

  75. Márquez, L. M., Redman, R. S., Rodriguez, R. J. & Roossinck, M. J. A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315, 513–515 (2007). This paper describes a very novel mutualistic symbiosis that allows plants and endophytic fungi to survive harsh geothermal soils.

    Article  CAS  PubMed  Google Scholar 

  76. Morsy, M. R., Oswald, J., He, J., Tang, Y. & Roossinck, M. J. Teasing apart a three-way symbiosis: Transcriptome analyses of Curvularia protuberata in response to viral infection and heat stress. Biochem. Biophys. Res. Commun. 401, 225–230 (2010).

    Article  CAS  PubMed  Google Scholar 

  77. Hottiger, T., Boller, T. & Wiemken, A. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiae cells subjected to temperature shifts. FEBS Lett. 220, 113–115 (1987).

    Article  CAS  PubMed  Google Scholar 

  78. Dadachova, E. & Casadevall, A. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11, 525–531 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Xu, P. et al. Virus infection improves drought tolerance. New Phytol. 180, 911–921 (2008).

    Article  PubMed  Google Scholar 

  80. Xie, W. S., Antoniw, J. F., White, R. F. & Jolliffe, T. H. Effects of beet cryptic virus infection on sugar beet in field trials. Ann. appl. Biol. 124, 451–459 (1994).

    Article  Google Scholar 

  81. Roossinck, M. J. Lifestyles of plant viruses. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 365, 1899–1905 (2010).

    Article  Google Scholar 

  82. Roossinck, M. J. et al. Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol. Ecol. 19, 81–88 (2010).

    Article  PubMed  Google Scholar 

  83. Nakatsukasa-Akune, M. et al. Suppression of root nodule formation by artificial expression of the TrEnodDR1 (coat protein of White clover cryptic virus 2) gene in Lotus japonicus. Mol. Plant Microbe Interact. 18, 1069–1080 (2005).

    Article  CAS  PubMed  Google Scholar 

  84. Lesnaw, J. A. & Ghabrial, S. A. Tulip breaking: past, present and future. Plant Dis. 84, 1052–1060 (2000). A nice review of tulipomania and the virus that caused it.

    Article  CAS  PubMed  Google Scholar 

  85. Perring, T. M. The Bemisia tabaci species complex. Crop Protect. 20, 725–737 (2001).

    Article  Google Scholar 

  86. Rojas, M. R., Hagen, C., Lucas, W. J. & Gilbertson, R. L. Exploiting chinks in the plant's armor: evolution and emergences of geminiviruses. Annu. Rev. Phytopathol. 43, 361–394 (2005).

    Article  CAS  PubMed  Google Scholar 

  87. Zang, L.-S., Chen, W.-Q. & Liu, S.-S. Comparison of performance on different host plants between the B biotype and a non-B biotype of Bemisia tabaci from Zhejiang, China. Entomol. Exp. Appl. 121, 221–227 (2006).

    Article  Google Scholar 

  88. Xie, Y., Zhou, X., Zhang, Z. & Qi, Y. Tobacco curly shoot virus isolated in Yunnan is adistinct species of Begomovirus. Chin. Sci. Bull. 47, 197–200 (2002).

    Article  CAS  Google Scholar 

  89. Yin, Q. et al. Tomato yellow leaf curl China virus: monopartite genome organization and agroinfection of plants. Virus Res. 81, 69–76 (2001).

    Article  CAS  PubMed  Google Scholar 

  90. Jiu, M. et al. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS One 2, e182 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Mann, R. S., Sidhu, J. S., Butter, N. S., Sohi, A. S. & Sekhon, P. S. Performance of Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy and Cotton leaf curl virus infected cotton. Fla. Entomol. 91, 249–255 (2008).

    Article  Google Scholar 

  92. Rossignol, P. A. et al. Enhanced mosquito blood-finding success on parasitemic hosts: evidence for vector–parasite mutualism. Proc. Natl Acad. Sci. USA 82, 7725–7727 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Varaldi, J., Patot, S., Nardin, M. & Gandon, S. A virus-shaping reproductive strategy in a Drosophila parasitoid. Adv. Parasitol. 70, 333–362 (2009).

    Article  PubMed  Google Scholar 

  94. Thomas-Orillard, M. A virus–Drosophila association: the first steps towards co-evolution? Biodivers. Conserv. 5, 1015–1021 (1996).

    Article  Google Scholar 

  95. Zera, A. J. & Denno, R. F. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42, 207–230 (1997).

    Article  CAS  PubMed  Google Scholar 

  96. Ryabov, E. V., Keane, G., Naish, N., Evered, C. & Winstanley, D. Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea. Proc. Natl Acad. Sci. USA 106, 8465–8470 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Gildow, F. E. & D'Arcy, C. J. Barley and oats as reservoirs for an aphid virus and the influcence on barley yellow dward virus transmission. Phytopathology. 78, 811–816 (1988).

    Article  Google Scholar 

  98. Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E. & Ochman, H. The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc. Natl Acad. Sci. USA 102, 16919–16926 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Oliver, K. M., Degnan, P. H., Hunter, M. S. & Moran, N. A. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992–994 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Brüssow, H., Canchaya, C. & Hardt, W.-D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Boyd, E. F. & Brüssow, H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10, 521–529 (2002).

    Article  CAS  PubMed  Google Scholar 

  102. Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334–338 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 242, 741 (2003).

    Article  CAS  Google Scholar 

  104. Pierce, S. K., Maugel, T. K., Rumpho, M. E., Hanten, J. J. & Mondy, W. L. Annual viral expression in a sea slug population: life cycle control and symbiotic chloroplast maintenance. Biol. Bull. 197, 1–6 (1999).

    Article  CAS  PubMed  Google Scholar 

  105. Rumpho, M. E. et al. Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica. Proc. Natl Acad. Sci. USA 105, 17867–17871 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Pierce, S. K., Curtis, N. E., Hanten, J. J., Boerner, S. L. & Schwartz, J. A. Transfer, integration and expression of functional nuclear genes between multicellular species. Symbiosis 42, 57–64 (2007).

    Google Scholar 

  107. Dash, M. Tulipomania, The Story of the World's Most Coveted Flower and the Extraordinary Passions it Aroused (Three Rivers, New York, 1999).

    Google Scholar 

Download references

Acknowledgements

The author is grateful to colleagues for helpful discussions, especially R. Redman, F. Ryan and L. Villarreal, and to her current and former laboratory members T. Feldman, L. Márquez, M. Morsy and P. Xu.

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The author declares no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Marilyn Roossinck's homepage

Glossary

Mutualistic

Pertaining to a symbiosis that is beneficial to all partners.

Provirus

Viral genomic DNA that has integrated into the genome of the host cell.

Symbiogenic

Pertaining to a new species: formed by the fusion of symbiotic organisms.

Antagonism

A symbiotic relationship in which one partner benefits at the expense of the other.

Commensalism

A symbiotic relationship in which one partner benefits and the other is unaffected.

Endoparasitoid

A specific type of parasitoid organism that spends a portion of its life within another organism.

Haemocoel

In arthropods, the space between the organs through which haemolymph circulates.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roossinck, M. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9, 99–108 (2011). https://doi.org/10.1038/nrmicro2491

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro2491

This article is cited by

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