Key Points
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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.
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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.
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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.
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Some mammalian viruses can protect their hosts from infection by related viruses or from disease caused by completely unrelated pathogens, such as bubonic plague.
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Viruses can protect their hosts by killing off competitors, as is seen with the killer viruses in yeasts.
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A fungal virus confers thermal tolerance to a plant in a complex symbiosis involving its fungal host and the plant that the fungus colonizes.
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Several acute plant viruses confer conditional mutualism by enhancing drought tolerance in plants.
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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.
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References
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.
Shen, H.-H. The challenge of discovering beneficial viruses. J. Med. Microbiol. 58, 531–532 (2009).
Canchaya, C., Proux, C., Fournous, G., Bruttin, A. & Brüssow, H. Prophage genomics. Microbiol. Mol. Biol. Rev. 67, 238–276 (2003).
deBary, H. A. Die Erscheinung der Symbiose. (Strasburg, 1879) (in German).
Roossinck, M. J. Symbiosis versus competition in the evolution of plant RNA viruses. Nature Rev. Microbiol. 3, 917–924 (2005).
Villarreal, L. P. Viruses and the Evolution of Life (American society for Microbiology Press, Washington DC, 2005).
Koonin, E. V. On the origin of cells and viruses: a comparative-genomic perspective. Isr. J. Ecol. Evol. 52, 299–318 (2006).
Webb, B. A. in The Insect Viruses (eds. Miller, L. K. & Ball, L. A.) 105–139 (Plenum, New York, 1998).
Webb, B. A. et al. Polydnavirus genomes reflect their dula roles as mutualists and pathogens. Virology 347, 160–174 (2006).
Stoltz, D. B. & Whitfield, J. B. Making nice with viruses. Science 323, 884–885 (2009).
Bézier, A. et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926–930 (2009).
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).
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).
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).
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).
Whitfield, J. B. & Asgari, S. Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. J. Insect Physiol. 49, 397–405 (2003).
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).
Volkoff, A.-N. et al. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog. 6, e1000923 (2010).
Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).
Kazazian, H. H. Jr. Mobile elements: drivers of genome evolution. Science 303, 1626–1632 (2004).
Ryan, F. P. Human endogenous retroviruses in health and disease: a symbiotic perspective. J. R. Soc. Med. 97, 560–565 (2004).
Eiden, M. V. Endogenous retroviruses — aiding and abetting genomic plasticity. Cell. Mol. Life Sci. 65, 3325–3328 (2008).
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).
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).
Ruprecht, K., Mayer, J., Sauter, M., Roemer, K. & Mueller-Lantzsch, N. Endogenous retroviruses and cancer. Cell. Mol. Life Sci. 65, 3366–3382 (2008).
Stocking, C. & Kozak, C. A. Murine endogenous retroviruses. Cell. Mol. Life Sci. 65, 3383–3398 (2008).
Wilson, C. A. Porcine endogenous retroviruses and xenotransplantation. Cell. Mol. Life Sci. 65, 3399–3412 (2008).
Tarlinton, R., Meers, J. & Young, P. Biology and evolution of the endogenous koala retrovirus. Cell. Mol. Life Sci. 65, 3413–3421 (2008).
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).
Jern, P. & Coffin, J. M. Effects of retroviruses on host genome function. Annu. Rev. Genet. 42, 709–732 (2008).
Ryan, F. Virolution (HarperCollins, London, 2009). This book contains numerous stories about beneficial viruses and how viruses have shaped the evolution of their hosts.
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.
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).
Stoye, J. P. Koala retrovirus: a genome invasion in real time. Genome Biol. 7, 241 (2006).
Harris, J. R. The evolution of placental mammals. FEBS Lett. 295, 3–4 (1991).
Dunlap, K. A. et al. Endogenous retroviruses regulate periimplantation placental growth and differentiation. Proc. Natl Acad. Sci. USA 103, 14390–14395 (2006).
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).
Hohn, T. et al. in Plant Virus Evolution (ed. Roossinck, M. J.) 53–81 (Springer, Heidelberg, 2008).
Staginnus, C. et al. Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biol. 7, 24 (2007).
Ruiz-Ferrer, V. & Voinnet, O. Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485–510 (2009).
Wu, Q., Wang, X. & Ding, S.-W. Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8, 12–15 (2010).
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).
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).
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).
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).
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).
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).
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).
Oldstone, M. B. A. Prevention of type I diabetes in nonobese diabetic mice by virus infection. Science 239, 500–502 (1988).
Lin, E. & Nemunaitis, J. Oncolytic viral therapies. Cancer Gene Ther. 11, 643–664 (2004).
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).
Liu, T.-C. & Kirn, D. Gene therapy progress and prospects cancer: oncolytic viruses. Gene Ther. 15, 877–884 (2008).
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).
Barton, E. S. et al. Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447, 326–330 (2007).
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).
Bossi, L., Fuentes, J. A., Mora, G. & Figueroa-Bossi, N. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185, 6467–6471 (2003).
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).
Schmitt, M. J. & Breinig, F. The viral killer system in yeast: from molecular biology to application. FEMS Microbiol. Rev. 26, 257–276 (2002).
Magliani, W., Conti, S., Gerloni, M., Bertolotti, D. & Polonelli, L. Yeast killer systems. Clin. Microbiol. Rev. 10, 369–400 (1997).
Schmitt, M. J. & Breinig, F. Yeast viral killer toxins: lethality and self-protection. Nature Rev. Microbiol. 4, 212–221 (2006).
McBride, R., Greig, D. & Travisano, M. Fungal viral mutualism moderated by ploidy. Evolution 62, 2372–2380 (2008).
Villarreal, L. P. Persistence pays: how viruses promote host group survival. Curr. Opin. Microbiol. 12, 467–472 (2009).
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).
Bianchine, P. J. & Russo, T. A. The role of epidemic infectious diseases in the discovery of America. Allergy Proc. 13, 225–232 (1992).
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.
Campbell, J. Invisible Invaders: Smallpox and Other Diseases in Aboriginal Australia, 1780–1880 (Melbourne Univ. Press, Melbourne, 2007).
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).
Nuss, D. L. in Encyclopedia of Virology (eds Granoff, A. & Webster, R.) 580–585 (Elsevier, Amsterdam, 2008).
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).
Milgroom, M. G. & Cortesi, P. Biological control of chestnut blight with hypovirulence: a critical analysis. Annu. Rev. Phytopathol. 42, 311–338 (2004).
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).
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).
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).
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).
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.
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).
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).
Dadachova, E. & Casadevall, A. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11, 525–531 (2008).
Xu, P. et al. Virus infection improves drought tolerance. New Phytol. 180, 911–921 (2008).
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).
Roossinck, M. J. Lifestyles of plant viruses. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 365, 1899–1905 (2010).
Roossinck, M. J. et al. Ecogenomics: using massively parallel pyrosequencing to understand virus ecology. Mol. Ecol. 19, 81–88 (2010).
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).
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.
Perring, T. M. The Bemisia tabaci species complex. Crop Protect. 20, 725–737 (2001).
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).
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).
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).
Yin, Q. et al. Tomato yellow leaf curl China virus: monopartite genome organization and agroinfection of plants. Virus Res. 81, 69–76 (2001).
Jiu, M. et al. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS One 2, e182 (2007).
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).
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).
Varaldi, J., Patot, S., Nardin, M. & Gandon, S. A virus-shaping reproductive strategy in a Drosophila parasitoid. Adv. Parasitol. 70, 333–362 (2009).
Thomas-Orillard, M. A virus–Drosophila association: the first steps towards co-evolution? Biodivers. Conserv. 5, 1015–1021 (1996).
Zera, A. J. & Denno, R. F. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42, 207–230 (1997).
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).
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).
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).
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).
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).
Boyd, E. F. & Brüssow, H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10, 521–529 (2002).
Reyes, A. et al. Viruses in the faecal microbiota of monozygotic twins and their mothers. Nature 466, 334–338 (2010).
Mann, N. H., Cook, A., Millard, A., Bailey, S. & Clokie, M. Marine ecosystems: bacterial photosynthesis genes in a virus. Nature 242, 741 (2003).
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).
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).
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).
Dash, M. Tulipomania, The Story of the World's Most Coveted Flower and the Extraordinary Passions it Aroused (Three Rivers, New York, 1999).
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.
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Glossary
- Mutualistic
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Pertaining to a symbiosis that is beneficial to all partners.
- Provirus
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Viral genomic DNA that has integrated into the genome of the host cell.
- Symbiogenic
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Pertaining to a new species: formed by the fusion of symbiotic organisms.
- Antagonism
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A symbiotic relationship in which one partner benefits at the expense of the other.
- Commensalism
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A symbiotic relationship in which one partner benefits and the other is unaffected.
- Endoparasitoid
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A specific type of parasitoid organism that spends a portion of its life within another organism.
- Haemocoel
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In arthropods, the space between the organs through which haemolymph circulates.
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Roossinck, M. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9, 99–108 (2011). https://doi.org/10.1038/nrmicro2491
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DOI: https://doi.org/10.1038/nrmicro2491
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