1887

Abstract

Parasitoid wasps can be found in association with heritable viruses. Although some viruses have been shown to profoundly affect the biology and evolution of parasitoid wasps, the genetic and phenotypic diversity of parasitoid-associated viruses remains largely unexplored. We previously discovered a behaviour-manipulating DNA virus in the parasitoid wasp . In this species, which lays its eggs inside larvae, Leptopilina boulardi filamentous virus (LbFV) forces the females to lay their eggs in already parasitized larvae. This behavioural manipulation increases the chances for the horizontal transmission of the virus. Here, we describe in the same parasitoid species another virus, which we propose to call Leptopilina boulardi toti-like virus (LbTV). This double-stranded RNA virus is highly prevalent in insect laboratory lines as well as in parasitoids caught in the field. In some cases, LbTV was found in coinfection with LbFV, but did not affect the behaviour of the wasp. Instead we found that the presence of LbTV correlates with an increase in the number of offspring, mostly due to increased survival of parasitoid larvae. LbTV is vertically transmitted mostly through the maternal lineage even if frequent paternal transmission also occurs. Unlike LbFV, LbTV is not horizontally transmitted. Its genome encodes a putative RNA-dependent RNA polymerase (RdRp) showing similarities with RdRps of . These results underline the high incidence and diversity of inherited viruses in parasitoids as well as their potential impact on the phenotype of their hosts.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000360
2016-02-01
2019-12-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/523.html?itemId=/content/journal/jgv/10.1099/jgv.0.000360&mimeType=html&fmt=ahah

References

  1. Beckage N., Drezen J.. editors 2011; Parasitoid Viruses San Diego: Academic Press;
    [Google Scholar]
  2. Bessarab I. N., Liu H. W., Ip C. F., Tai J. H.. 2000; The complete cDNA sequence of a type II Trichomonas vaginalis virus. Virology267:350–359 [CrossRef][PubMed]
    [Google Scholar]
  3. Bessarab I. N., Nakajima R., Liu H. W., Tai J. H.. 2011; Identification and characterization of a type III Trichomonas vaginalis virus in the protozoan pathogen Trichomonas vaginalis . Arch Virol156:285–294 [CrossRef][PubMed]
    [Google Scholar]
  4. Bézier A., Annaheim M., Herbinière J., Wetterwald C., Gyapay G., Bernard-Samain S., Wincker P., Roditi I., Heller M., other authors. 2009; Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science323:926–930 [CrossRef][PubMed]
    [Google Scholar]
  5. Bigot Y., Rabouille A., Doury G., Sizaret P. Y., Delbost F., Hamelin M. H., Periquet G.. 1997; Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella . J Gen Virol78:1149–1163 [CrossRef][PubMed]
    [Google Scholar]
  6. Bruenn J. A.. 1993; A closely related group of RNA-dependent RNA polymerases from double-stranded RNA viruses. Nucleic Acids Res21:5667–5669 [CrossRef][PubMed]
    [Google Scholar]
  7. Cheng J., Jiang D., Fu Y., Li G., Peng Y., Ghabrial S. A.. 2003; Molecular characterization of a dsRNA totivirus infecting the sclerotial parasite Coniothyrium minitans . Virus Res93:41–50 [CrossRef][PubMed]
    [Google Scholar]
  8. Chomczynski P., Sacchi N.. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem162:156–159 [CrossRef][PubMed]
    [Google Scholar]
  9. David J. R.. 1962; A new medium for rearing Drosophila in axenic condition. Drosoph Inf Serv36:128
    [Google Scholar]
  10. Dupas S., Carton Y.. 1999; Two non-linked genes for specific virulence of Leptopilina boulardi against Drosophila melanogaster and D. yakuba . Evol Ecol13:211–220 [CrossRef]
    [Google Scholar]
  11. Gandon S., Rivero A., Varaldi J.. 2006; Superparasitism evolution: adaptation or manipulation?. Am Nat167:E1–E22 [CrossRef][PubMed]
    [Google Scholar]
  12. Gao X., Alvo M., Chen J., Li G.. 2008; Nonparametric multiple comparison procedures for unbalanced one-way factorial designs. J Stat Plan Inference138:2574–2591 [CrossRef]
    [Google Scholar]
  13. Gouy M., Guindon S., Gascuel O.. 2010; SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol27:221–224 [CrossRef][PubMed]
    [Google Scholar]
  14. Grabherr M. G., Haas B. J., Yassour M., Levin J. Z., Thompson D. A., Amit I., Adiconis X., Fan L., Raychowdhury R., other authors. 2011; Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol29:644–652 [CrossRef][PubMed]
    [Google Scholar]
  15. Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O.. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol59:307–321 [CrossRef][PubMed]
    [Google Scholar]
  16. Haine E. R., Boucansaud K., Rigaud T.. 2005; Conflict between parasites with different transmission strategies infecting an amphipod host. Proc Biol Sci272:2505–2510 [CrossRef][PubMed]
    [Google Scholar]
  17. Haugland O., Mikalsen A. B., Nilsen P., Lindmo K., Thu B. J., Eliassen T. M., Roos N., Rode M., Evensen O.. 2011; Cardiomyopathy syndrome of Atlantic salmon (Salmo salar L.) is caused by a double-stranded RNA virus of the Totiviridae family. J Virol85:5275–5286 [CrossRef][PubMed]
    [Google Scholar]
  18. Huang S., Ghabrial S. A.. 1996; Organization and expression of the double-stranded RNA genome of Helminthosporium victoriae 190S virus, a totivirus infecting a plant pathogenic filamentous fungus. Proc Natl Acad Sci U S A93:12541–12546 [CrossRef][PubMed]
    [Google Scholar]
  19. Icho T., Wickner R. B.. 1989; The double-stranded RNA genome of yeast virus L-A encodes its own putative RNA polymerase by fusing two open reading frames. J Biol Chem264:6716–6723[PubMed]
    [Google Scholar]
  20. Isawa H., Kuwata R., Hoshino K., Tsuda Y., Sakai K., Watanabe S., Nishimura M., Satho T., Kataoka M., other authors. 2011; Identification and molecular characterization of a new nonsegmented double-stranded RNA virus isolated from Culex mosquitoes in Japan. Virus Res155:147–155 [CrossRef][PubMed]
    [Google Scholar]
  21. Jacas J. A., Budia F., Rodríguez-Cerezo E., Viñuela E.. 1997; Virus-like particules in the poison glant of the parasitic wasp Opius concolor . Ann Appl Biol130:587–592 [CrossRef]
    [Google Scholar]
  22. Koyama S., Urayama S., Ohmatsu T., Sassa Y., Sakai C., Takata M., Hayashi S., Nagai M., Furuya T., other authors. 2015; Identification, characterization and full-length sequence analysis of a novel dsRNA virus isolated from the arboreal ant Camponotus yamaokai . J Gen Virol96:1930–1937 [CrossRef][PubMed]
    [Google Scholar]
  23. Lafferty K., Thomas F., Poulin R.. 2000; Evolution of host manipulation by parasites and its consequences. In Evolutionary Biology of Host–Parasite Relationships: Theory Meets Reality pp117–127Edited by Poulin R., Morand S., Skorping A.. Amsterdam: Elsevier Science;
    [Google Scholar]
  24. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A., other authors. 2007; Clustal W and Clustal X version 2.0. Bioinformatics23:2947–2948 [CrossRef][PubMed]
    [Google Scholar]
  25. Lawrence P. O., Matos L. F.. 2005; Transmission of the Diachasmimorpha longicaudata rhabdovirus (DlRhV) to wasp offspring: an ultrastructural analysis. J Insect Physiol51:235–241 [CrossRef][PubMed]
    [Google Scholar]
  26. Li L., Wang A. L., Wang C. C.. 2001; Structural analysis of the − 1 ribosomal frameshift elements in giardiavirus mRNA. J Virol75:10612–10622 [CrossRef][PubMed]
    [Google Scholar]
  27. Liu W., Chen J.. 2009; A double-stranded RNA as the genome of a potential virus infecting Vicia faba . Virus Genes39:126–131 [CrossRef][PubMed]
    [Google Scholar]
  28. Liu H., Fu Y., Jiang D., Li G., Xie J., Cheng J., Peng Y., Ghabrial S. A., Yi X.. 2010; Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol84:11876–11887 [CrossRef][PubMed]
    [Google Scholar]
  29. Longdon B., Jiggins F. M.. 2012; Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?. Proc R Soc Ser B Biol Sci279:3889–3898 [CrossRef]
    [Google Scholar]
  30. Longdon B., Jiggins F. M.. 2010; Paternally transmitted parasites. Curr Biol20:R695–R696 [CrossRef][PubMed]
    [Google Scholar]
  31. Longdon B., Wilfert L., Obbard D. J., Jiggins F. M.. 2011; Rhabdoviruses in two species of Drosophila: vertical transmission and a recent sweep. Genetics188:141–150 [CrossRef][PubMed]
    [Google Scholar]
  32. López Ferber M., Ferreiro Ríos A., Kuhl G., Comendador M. A., Louis C.. 1997; Infection of the gonads of the SimES strain of Drosophila simulans by the hereditary reovirus DSV. J Invertebr Pathol70:143–149 [CrossRef][PubMed]
    [Google Scholar]
  33. Maejima K., Himeno M., Komatsu K., Kakizawa S., Yamaji Y., Hamamoto H., Namba S.. 2008; Complete nucleotide sequence of a new double-stranded RNA virus from the rice blast fungus, Magnaporthe oryzae . Arch Virol153:389–391 [CrossRef][PubMed]
    [Google Scholar]
  34. Martin R. R., Zhou J., Tzanetakis I. E.. 2011; Blueberry latent virus: an amalgam of the Partitiviridae and Totiviridae . Virus Res155:175–180 [CrossRef][PubMed]
    [Google Scholar]
  35. Martinez J., Duplouy A., Woolfit M., Vavre F., O'Neill S. L., Varaldi J.. 2012a; Influence of the virus LbFV and of Wolbachia in a host-parasitoid interaction. PLoS One7:e35081 [CrossRef][PubMed]
    [Google Scholar]
  36. Martinez J., Fleury F., Varaldi J.. 2012b; Heritable variation in an extended phenotype: the case of a parasitoid manipulated by a virus. J Evol Biol25:54–65 [CrossRef][PubMed]
    [Google Scholar]
  37. Mouton L., Henri H., Bouletreau M., Vavre F.. 2003; Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol Ecol12:3459–3465 [CrossRef][PubMed]
    [Google Scholar]
  38. Nomura K., Osaki H., Iwanami T., Matsumoto N., Ohtsu Y.. 2003; Cloning and characterization of a totivirus double-stranded RNA from the plant pathogenic fungus, Helicobasidium mompa Tanaka. Virus Genes26:219–226 [CrossRef][PubMed]
    [Google Scholar]
  39. Oliveira D.C.S.G., Hunter W. B., Ng J., Desjardins C. A., Dang P. M., Werren J. H.. 2010; Data mining cDNAs reveals three new single stranded RNA viruses in Nasonia (Hymenoptera: Pteromalidae). Insect Mol Biol19:(Suppl. 1)99–107 [CrossRef][PubMed]
    [Google Scholar]
  40. Park Y., James D., Punja Z. K.. 2005; Co-infection by two distinct totivirus-like double-stranded RNA elements in Chalara elegans (Thielaviopsis basicola). Virus Res109:71–85 [CrossRef][PubMed]
    [Google Scholar]
  41. Patot S., Lepetit D., Charif D., Varaldi J., Fleury F.. 2009; Molecular detection, penetrance, and transmission of an inherited virus responsible for behavioral manipulation of an insect parasitoid. Appl Environ Microbiol75:703–710 [CrossRef][PubMed]
    [Google Scholar]
  42. Poulos B. T., Tang K. F., Pantoja C. R., Bonami J. R., Lightner D. V.. 2006; Purification and characterization of infectious myonecrosis virus of penaeid shrimp. J Gen Virol87:987–996 [CrossRef][PubMed]
    [Google Scholar]
  43. Preisig O., Wingfield B. D., Wingfield M. J.. 1998; Coinfection of a fungal pathogen by two distinct double-stranded RNA viruses. Virology252:399–406 [CrossRef][PubMed]
    [Google Scholar]
  44. Rabouille A., Bigot Y., Drezen J. M., Sizaret P. Y., Hamelin M. H., Periquet G.. 1994; A member of the Reoviridae (DpRV) has a ploidy-specific genomic segment in the wasp Diadromus pulchellus (Hymenoptera). Virology205:228–237 [CrossRef][PubMed]
    [Google Scholar]
  45. Reineke A., Asgari S.. 2005; Presence of a novel small RNA-containing virus in a laboratory culture of the endoparasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae). J Insect Physiol51:127–135 [CrossRef][PubMed]
    [Google Scholar]
  46. Renault S., Petit A., Bénédet F., Bigot S., Bigot Y.. 2002; Effects of the Diadromus pulchellus ascovirus, DpAV-4, on the hemocytic encapsulation response and capsule melanization of the leek-moth pupa, Acrolepiopsis assectella . J Insect Physiol48:297–302 [CrossRef][PubMed]
    [Google Scholar]
  47. Renault S., Bigot S., Lemesle M., Sizaret P. Y., Bigot Y.. 2003; The cypovirus Diadromus pulchellus RV-2 is sporadically associated with the endoparasitoid wasp D. pulchellus and modulates the defence mechanisms of pupae of the parasitized leek-moth, Acrolepiopsis assectella . J Gen Virol84:1799–1807 [CrossRef][PubMed]
    [Google Scholar]
  48. Renault S., Stasiak K., Federici B., Bigot Y.. 2005; Commensal and mutualistic relationships of reoviruses with their parasitoid wasp hosts. J Insect Physiol51:137–148 [CrossRef][PubMed]
    [Google Scholar]
  49. Romo M., Leuchtmann A., García B., Zabalgogeazcoa I.. 2007; A totivirus infecting the mutualistic fungal endophyte Epichloë festucae . Virus Res124:38–43 [CrossRef][PubMed]
    [Google Scholar]
  50. Sabanadzovic S., Valverde R. A., Brown J. K., Martin R. R., Tzanetakis I. E.. 2009; Southern tomato virus: the link between the families Totiviridae and Partitiviridae . Virus Res140:130–137 [CrossRef][PubMed]
    [Google Scholar]
  51. Sabanadzovic S., Abou Ghanem-Sabanadzovic N., Valverde R. A.. 2010; A novel monopartite dsRNA virus from rhododendron. Arch Virol155:1859–1863 [CrossRef][PubMed]
    [Google Scholar]
  52. Scheffter S., Widmer G., Patterson J. L.. 1994; Complete sequence of Leishmania RNA virus 1-4 and identification of conserved sequences. Virology199:479–483 [CrossRef][PubMed]
    [Google Scholar]
  53. Scheffter S. M., Ro Y. T., Chung I. K., Patterson J. L.. 1995; The complete sequence of Leishmania RNA virus LRV2-1, a virus of an Old World parasite strain. Virology212:84–90 [CrossRef][PubMed]
    [Google Scholar]
  54. Schlenke T. A., Morales J., Govind S., Clark A. G.. 2007; Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster . PLoS Pathog3:1486–1501 [CrossRef][PubMed]
    [Google Scholar]
  55. Stasiak K., Renault S., Federici B. A., Bigot Y.. 2005; Characteristics of pathogenic and mutualistic relationships of ascoviruses in field populations of parasitoid wasps. J Insect Physiol51:103–115 [CrossRef][PubMed]
    [Google Scholar]
  56. Stielow B., Menzel W.. 2010; Complete nucleotide sequence of TaV1, a novel totivirus isolated from a black truffle ascocarp (Tuber aestivum Vittad.). Arch Virol155:2075–2078 [CrossRef][PubMed]
    [Google Scholar]
  57. Stoltz D., Makkay A.. 2000; Co-replication of a reovirus and a polydnavirus in the ichneumonid parasitoid Hyposoter exiguae . Virology278:266–275 [CrossRef][PubMed]
    [Google Scholar]
  58. Stoltz D. B., Krell P., Cook D., MacKinnon E. A., Lucarotti C. J.. 1988; An unusual virus from the parasitic wasp Cotesia melanoscela . Virology162:311–320 [CrossRef][PubMed]
    [Google Scholar]
  59. Stuart K. D., Weeks R., Guilbride L., Myler P. J.. 1992; Molecular organization of Leishmania RNA virus 1. Proc Natl Acad Sci U S A89:8596–8600 [CrossRef][PubMed]
    [Google Scholar]
  60. Tai J. H., Ip C. F.. 1995; The cDNA sequence of Trichomonas vaginalis virus-T1 double-stranded RNA. Virology206:773–776 [CrossRef][PubMed]
    [Google Scholar]
  61. Talavera G., Castresana J.. 2007; Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol56:564–577 [CrossRef][PubMed]
    [Google Scholar]
  62. Thézé J., Leclercq S., Moumen B., Cordaux R., Gilbert C.. 2014; Remarkable diversity of endogenous viruses in a crustacean genome. Genome Biol Evol6:2129–2140 [CrossRef][PubMed]
    [Google Scholar]
  63. Thomas F., Fauchier J., Lafferty K. D.. 2002; Conflict of interest between a nematode and a trematode in an amphipod host: test of the sabotage hypothesis. Behav Ecol Sociobiol51:296–301 [CrossRef]
    [Google Scholar]
  64. Tuomivirta T. T., Hantula J.. 2003; Two unrelated double-stranded RNA molecule patterns in Gremmeniella abietina type A code for putative viruses of the families Totiviridae and Partitiviridae . Arch Virol148:2293–2305 [CrossRef][PubMed]
    [Google Scholar]
  65. Tuomivirta T. T., Hantula J.. 2005; Three unrelated viruses occur in a single isolate of Gremmeniella abietina var. abietina type A. Virus Res110:31–39 [CrossRef][PubMed]
    [Google Scholar]
  66. Varaldi J., Fouillet P., Ravallec M., López-Ferber M., Boulétreau M., Fleury F.. 2003; Infectious behavior in a parasitoid. Science302:1930 [CrossRef][PubMed]
    [Google Scholar]
  67. Varaldi J., Gandon S., Rivero A., Patot S., Fleury F.. 2006a; A newly discovered virus manipulates superparasitism behavior in a parasitoid wasp. In Insect Symbiosis, vol. 2 (Contemporary Topics Entomol) pp119–139Edited by Bourtzis K., Miller T. A.. Boca Raton, FL: Taylor and Francis/CRC Press;[CrossRef]
    [Google Scholar]
  68. Varaldi J., Ravallec M., Labrosse C., Lopez-Ferber M., Boulétreau M., Fleury F.. 2006b; Artifical transfer and morphological description of virus particles associated with superparasitism behaviour in a parasitoid wasp. J Insect Physiol52:1202–1212 [CrossRef][PubMed]
    [Google Scholar]
  69. Varaldi J., Petit S., Boulétreau M., Fleury F.. 2006c; The virus infecting the parasitoid Leptopilina boulardi exerts a specific action on superparasitism behaviour. Parasitology132:747–756 [CrossRef][PubMed]
    [Google Scholar]
  70. Vavre F., Mouton L., Pannebakker B. A.. 2009; Drosophila–parasitoid communities as model systems for host–Wolbachia interactions. In Parasitoids of Drosophila (Advances in Parasitologyvol. 70 chapter 12 pp299–331Edited by Prevost G.. London: Academic Press;
    [Google Scholar]
  71. Wang A. L., Yang H. M., Shen K. A., Wang C. C.. 1993; Giardiavirus double-stranded RNA genome encodes a capsid polypeptide and a gag-pol-like fusion protein by a translation frameshift. Proc Natl Acad Sci U S A90:8595–8599 [CrossRef][PubMed]
    [Google Scholar]
  72. Webster C. L., Waldron F. M., Robertson S., Crowson D., Ferrari G., Quintana J. F., Brouqui J. M., Bayne E. H., Longdon B., other authors. 2015; The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster . PLoS Biol13:e1002210 [CrossRef][PubMed]
    [Google Scholar]
  73. Wu Q., Luo Y., Lu R., Lau N., Lai E. C., Li W. X., Ding S. W.. 2010; Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci U S A107:1606–1611 [CrossRef][PubMed]
    [Google Scholar]
  74. Xu P., Liu Y., Graham R. I., 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 Pathog10:e1004490 [CrossRef][PubMed]
    [Google Scholar]
  75. Yang X., Zhang Y., Ge X., Yuan J., Shi Z.. 2012; A novel totivirus-like virus isolated from bat guano. Arch Virol157:1093–1099 [CrossRef][PubMed]
    [Google Scholar]
  76. Yokoi T., Yamashita S., Hibi T.. 2007; The nucleotide sequence and genome organization of Magnaporthe oryzae virus 1. Arch Virol152:2265–2269 [CrossRef][PubMed]
    [Google Scholar]
  77. Zchori-Fein E., Gottlieb Y., Kelly S. E., Brown J. K., Wilson J. M., Karr T. L., Hunter M. S.. 2001; A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proc Natl Acad Sci U S A98:12555–12560 [CrossRef][PubMed]
    [Google Scholar]
  78. Zhai Y., Attoui H., Mohd Jaafar F., Wang H. Q., Cao Y. X., Fan S. P., Sun Y. X., Liu L. D., Mertens P. P., other authors. 2010; Isolation and full-length sequence analysis of Armigeres subalbatus totivirus, the first totivirus isolate from mosquitoes representing a proposed novel genus (Artivirus) of the family Totiviridae . J Gen Virol91:2836–2845 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000360
Loading
/content/journal/jgv/10.1099/jgv.0.000360
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error