Abstract
Viruses represent some of the deadliest pathogens known to science. Recently they have been reported to have mutualistic interactions with their hosts, providing them direct or indirect benefits. The mutualism and symbiogenesis of such viruses with lower eukaryotic partners such as fungi, yeast, and insects have been reported but the full mechanism of interaction often remains an enigma. In many instances, these viral interactions provide resistance against several biotic and abiotic stresses, which could be the prime reason for the ecological success and positive selection of the hosts. These viruses modulate host metabolism and behavior, so both can obtain maximum benefits from the environment. They bring about micro- and macro-level changes in the hosts, benefiting their adaptation, reproduction, development, and survival. These virus-host interactions can be bilateral or tripartite with a variety of interacting partners. Exploration of these interactions can shed light on one of the well-coordinated biological phenomena of co-evolution and can be highly utilized for various applications in agriculture, fermentation and the pharmaceutical industries.




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Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99–108
Margulis L, Sagan D (2008) Acquiring genomes: a theory of the origins of species. Basic Books, New York
Goic B, Saleh MC (2012) Living with the enemy: viral persistent infections from a friendly viewpoint. Curr Opin Microbiol 15:531–537
Bao X, Roossinck MJ (2013) Multiplexed interactions: viruses of endophytic fungi. Adv Virus Res 86:37–58
Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581
Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515
Morsy MR, Oswald J, He J, Tang Y, Roossinck MJ (2010) 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
Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441
Isenor M, Kaminskyj SG, Rodriguez RJ, Redman RS, Gough KM (2010) Characterization of mannitol in Curvularia protuberata hyphae by FTIR and Raman spectromicroscopy. Analyst 135:3249–3254
Muñoz-Clares RA, Díaz-Sánchez ÁG, González-Segura L, Montiel C (2010) Kinetic and structural features of betaine aldehyde dehydrogenases: mechanistic and regulatory implications. Arch Biochem Biophys 493:71–81
Rosenberg NK, Lee RW, Yancey PH (2006) High contents of hypotaurine and thiotaurine in hydrothermal-vent gastropods without thiotrophic endosymbionts. J Exp Zool A Ecol Genet Physiol 305:655–662
Dadachova E, Casadevall A (2008) Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr Opin Microbiol 11:525–531
Rodriguez RJ, Woodward C, Kim YO, Redman RS (2009) Habitat-adapted symbiosis as a defense against abiotic and biotic stresses. In: White JF Jr, Torres MS (eds) Defensive mutualism in microbial symbiosis, vol 26. CRC Press, Boca Raton, pp 335–346
Al-Hamdani S, Stoelting A, Morsy M (2014) Influence of symbiosis between fungus, virus, and tomato plant in combating heat stress. J Ala Acad Sci 85:150–160
Schmitt MJ, Breinig F (2002) The viral killer system in yeast: from molecular biology to application. FEMS Microbiol Rev 26:257–276
Hanes SD, Burn VE, Sturley SL, Tipper DJ, Bostian KA (1986) Expression of a cDNA derived from the yeast killer preprotoxin gene: implications for processing and immunity. Proc Natl Acad Sci USA 83:1675–1679
Dignard D, Whiteway M, Germain D, Tessier D, Thomas DY (1991) Expression in yeast of a cDNA copy of the K2 killer toxin gene. Mol Gen Genet 227:127–136
Schmitt MJ, Tipper DJ (1995) Sequence of the M28 dsRNA: preprotoxin is processed to an α/β heterodimeric protein toxin. Virology 213:341–351
Icho T, Wickner RB (1989) The double-stranded RNA genome of yeast virus LA encodes its own putative RNA polymerase by fusing two open reading frames. J Biol Chem 264:6716–6723
Wickner RB (1996) Prions and RNA viruses of Saccharomyces cerevisiae. Annu Rev Genet 30:109–139
Hutchins K, Bussey H (1983) Cell wall receptor for yeast killer toxin: involvement of [1→ 6]-β-D-glucan. J Bacteriol 154:161–169
Schmitt M, Radler F (1988) Molecular structure of the cell wall receptor for killer toxin KT28 in Saccharomyces cerevisiae. J Bacteriol 170:2192–2196
Breinig F, Tipper DJ, Schmitt MJ (2002) Kre1p, the plasma membrane receptor for the yeast K1 viral toxin. Cell 108:395–405
Eisfeld K, Riffer F, Mentges J, Schmitt MJ (2000) Endocytotic uptake and retrograde transport of a virally encoded killer toxin in yeast. Mol Microbiol 37:926–940
de la Peña P, Barros F, Gascón S, Lazo PS, Ramos S (1981) Effect of yeast killer toxin on sensitive cells of Saccharomyces cerevisiae. J Biol Chem 256:10420–10425
Martinac B, Zhu H, Kubalski A, Zhou XL, Culbertson M, Bussey H et al (1990) Yeast K1 killer toxin forms ion channels in sensitive yeast spheroplasts and in artificial liposomes. Proc Natl Acad Sci USA 87:6228–6232
Ahmed A, Sesti F, Ilan N, Shih TM, Sturley SL, Goldstein SA (1999) A molecular target for viral killer toxin: TOK1 potassium channels. Cell 99:283–291
Schmitt MJ, Klavehn P, Wang J, Schönig I, Tipper DJ (1996) Cell cycle studies on the mode of action of yeast K28 killer toxin. Microbiol 142:2655–2662
Tao JI, Ginsberg ID, Banerjee NA, Held W, Koltin YI, Bruenn JA (1990) Ustilago maydis KP6 killer toxin: structure, expression in Saccharomyces cerevisiae, and relationship to other cellular toxins. Mol Cell Biol 10:1373–1381
Tercero JC, Wickner RB (1992) MAK3 encodes an N-acetyltransferase whose modification of the LA gag NH2 terminus is necessary for virus particle assembly. J Biol Chem 267:20277–20281
Fujimura TS, Wickner RB (1987) LA double-stranded RNA virus-like particle replication cycle in Saccharomyces cerevisiae: particle maturation in vitro and effects of mak10 and pet18 mutations. Mol Cell biol 7:420–426
Bussey H, Saville D, Greene D, Tipper DJ, Bostian KA (1983) Secretion of Saccharomyces cerevisiae killer toxin: processing of the glycosylated precursor. Mol Cell Biol 3:1362–1370
Zhu YS, Zhang XY, Cartwright CP, Tipper DJ (1992) Kex2-dependent processing of yeast K1 killer preprotoxin includes cleavage at ProArg-44. Mol Microbiol 6:511–520
Boone C, Sdicu AM, Wagner J, Degre R, Sanchez C, Bussey H (1990) Integration of the yeast K1 killer toxin gene into the genome of marked wine yeasts and its effect on vinification. Am J Enol Vitic 41:37–42
Radler F, Schmitt MJ, Meyer B (1990) Killer toxin of Hanseniaspora uvarum. Arch Microbiol 154:175–178
Weiler F, Schmitt MJ (2003) Zygocin, a secreted antifungal toxin of the yeast Zygosaccharomyces bailii, and its effect on sensitive fungal cells. FEMS Yeast Res 3:69–76
Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4:212–221
Webb BA (1998) Polydnavirus biology, genome structure, and evolution. In: The insect viruses. Springer, US, pp 105–139
Tanaka T (1987) Morphological changes in haemocytes of the host, Pseudaletia separata, parasitized by Microplitis mediator or Apanteles kariyai. Dev Comp Immunol 11:57–67
Strand MR, Pech LL (1995) Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. J Gen Virol 76:283–291
Espagne E, Dupuy C, Huguet E, Cattolico L, Provost B, Martins N et al (2004) Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306:286–289
Whitfield JB (2002) Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci USA 99:7508–7513
Stoltz D, Whitefield J (2009) Making Nice with Viruses. Science 323:884–885
Gasmi L, Boulain H, Gauthier J, Hua-Van A, Musset K, Jakubowska AK et al (2015) Recurrent domestication by Lepidoptera of genes from their parasites mediated by bracoviruses. PLoS Genet 11:e1005470
Stasiak K, Renault S, Federici BA, Bigot Y (2005) Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J Insect Physiol 51:103–115
Renault S, Stasiak K, Federici B, Bigot Y (2005) Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J Insect Physiol 51:137–148
Maure F, Brodeur J, Ponlet N, Doyon J, Firlej A, Elguero É, Thomas F (2011) The cost of a bodyguard. Biol Lett 7:843–846
Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J, Duval D et al (2015) Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc R Soc Lond B Biol Sci 282:20142773
Xu P, Liu Y, Graham RI, Wilson K, Wu K (2014) Densovirus is a mutualistic symbiont of a global crop pest Helicoverpa armigera and protects against a baculovirus and Bt biopesticide. PLoS Pathog 10:e1004490
Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79
Ghosh A, Das A, Vijayanandaraj S, Mandal B (2015) Cardamom bushy dwarf virus infection in large cardamom alters plant selection preference, life stages, and fecundity of aphid vector, Micromyzus kalimpongensis (Hemiptera: Aphididae). Environ Entomol 45:178–184
Weldon SR, Oliver KM (2016) Diverse bacteriophage roles in an aphid-bacterial defensive mutualism. In: Hurst C (ed) The mechanistic benefits of microbial symbionts. Advances in environmental microbiology, vol 2. Springer, Cham, pp 173–206
Digilio MC, Isidoro N, Tremblay E, Pennacchio F (2000) Host castration by Aphidius ervi venom proteins. J Insect Physiol 46:1041–1050
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800
Schmid M, Sieber R, Zimmermann YS, Vorburger C (2012) Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. Funct Ecol 26:207–215
Asplen MK, Bano N, Brady CM, Desneux N, Hopper KR, Malouines C et al (2014) Specialisation of bacterial endosymbionts that protect aphids from parasitoids. Ecol Entomol 39:736–739
van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JF (1999) Isolation and characterization of APSE-1, a bacteriophage infecting the secondary endosymbiont of Acyrthosiphon pisum. Virology 262:104–113
Degnan PH, Moran NA (2008) Diverse phage-encoded toxins in a protective insect endosymbiont. Appl Environ Microbiol 74:6782–6791
Ohara M, Oswald E, Sugai M (2004) Cytolethal distending toxin: a bacterial bullet targeted to nucleus. J Biochem 136:409–413
Endo Y, Tsurugi K, Yutsudo T, Takeda Y, Ogasawara T, Igarashi K (1988) Site of action of a Vero toxin (VT2) from Escherichia coli O157: H7 and of Shiga toxin on eukaryotic ribosomes. Eur J Biochem 171:45–50
Weldon SR, Strand MR, Oliver KM (2013) Phage loss and the breakdown of a defensive symbiosis in aphids. Proc R Soc Lond B Biol Sci 280:20122103
Duron O (2014) Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. FEMS Microbiol Ecol 90:184–194
Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119
Nazzi F, Brown SP, Annoscia D, Del Piccolo F, Di Prisco G, Varricchio P et al (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8:e1002735
Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC, Chandler D et al (2014) A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS Pathog 10:e1004230
Flenniken ML, Andino R (2013) Non-specific dsRNA-mediated antiviral response in the honey bee. PLoS One 8:e77263
Di Prisco G, Annoscia D, Margiotta M, Ferrara R, Varricchio P, Zanni V et al (2016) A mutualistic symbiosis between a parasitic mite and a pathogenic virus undermines honey bee immunity and health. Proc Natl Acad Sci USA. 7:201523515
Thomas-Orillard M (1996) A virus-Drosophila association: the first steps towards co-evolution? Biodivers Conserv 5:1015–1021
Park CM, Banerjee N, Koltin Y, Bruenn JA (1996) The Ustilago maydis virally encoded KP1 killer toxin. Mol Microbiol 20:957–963
Gage MJ, Bruenn J, Fischer M, Sanders D, Smith TJ (2001) KP4 fungal toxin inhibits growth in Ustilago maydis by blocking calcium uptake. Mol Microbiol 41:775–785
Theisen S, Molkenau E, Schmitt MJ (2000) Wicaltin, a new protein toxin secreted by the yeast Williopsis californica and its broad-spectrum antimycotic potential. J Microbiol Biotechnol 10:547–550
Edson KM, Vinson SB, Stoltz DB, Summers MD (1981) Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid’s host. Science 211:582–583
Burke GR, Walden KK, Whitfield JB, Robertson HM, Strand MR (2014) Widespread genome reorganization of an obligate virus mutualist. PLoS Genet 10:e1004660
Bao X, Roossnick MJ (2013) A life history view of mutualistic viral symbioses: quantity or quality for cooperation? Curr Opin Microbiol 16:514–518
Maiti IB, Dey N, Pattanaik S, Dahlman DL, Rana RL, Webb BA (2003) Antibiosis-type insect resistance in transgenic plants expressing a teratocyte secretory protein (TSP14) gene from a hymenopteran endoparasite (Microplitis croceipes). Plant Biotechnol J 1:209–219
Urwin PE, McPherson MJ, Atkinson HJ (1998) Enhanced transgenic plant resistance to nematodes by dual proteinase inhibitor constructs. Planta 204:472–479
Acknowledgements
Authors acknowledge Dr. Tuli Dey, Dr. Rohan Khadilkar and Dr. Sneha Bansode for their critical comments. Authors also acknowledge Ms. Yoshita Bhide and Ms. Shriya Lele for their editorial assistance.
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Financial support is provided by the research grant from Department of Science and Technology, Government of India under ECR/2015/000502 Grant and Savitribai Phule Pune University, Pune 411007, Maharashtra India.
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The concept was developed and articulated by SSJ and RSJ. Manuscript was written and edited by SSJ and RSJ.
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Handling Editor: Robert H.A. Coutts.
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Jagdale, S.S., Joshi, R.S. Enemies with benefits: mutualistic interactions of viruses with lower eukaryotes. Arch Virol 163, 821–830 (2018). https://doi.org/10.1007/s00705-017-3686-5
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DOI: https://doi.org/10.1007/s00705-017-3686-5

