1887

Abstract

The viral landscape of the honey bee (Apismellifera) has changed as a consequence of the global spread of the parasitic mite Varroa destructor and accompanying virulent strains of the iflavirus deformed wing virus (DWV), which the mite vectors. The presence of DWV in honey bee populations is known to influence the occurrence of other viruses, suggesting that the current known virome of A. mellifera may be undercharacterized. Here we tested this hypothesis by examining the honey bee virome in Australia, which is uniquely free of parasitic mites or DWV. Using a high-throughput sequencing (HTS) approach, we examined the RNA virome from nine pools of A. mellifera across Australia. In addition to previously reported honey bee viruses, several other insect viruses were detected, including strains related to aphid lethal paralysis virus (ALPV) and Rhopalosiphum padi virus (RhPV), which have recently been identified as infecting honey bees in the USA, as well as several other viruses recently found in Drosophila spp. A further 42 putative novel insect virus genomes spanning the order Picornavirales were assembled, which significantly increases the known viral diversity in A. mellifera. Among these novel genomes, we identified several that were similar (but different) to key A. mellifera viruses, such as DWV, that warrant further investigation. We propose that A. mellifera may be preferentially infected with viruses of the order Picornavirales and that a diverse population of these viruses may be representative of a Varroa-free landscape.

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2018-05-11
2019-09-18
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References

  1. Bailey L, Gibbs AJ, Woods RD. Sacbrood Virus of larval honey bee (Apis mellifera Linnaeus). Virology 1964; 23: 425– 429 [CrossRef] [PubMed]
    [Google Scholar]
  2. Anderson DL, Gibbs AJ. Inapparent virus-infections and their interactions in pupae of the honey bee (Apis mellifera Linnaeus) in Australia. J Gen Virol 1988; 69: 1617– 1625 [CrossRef]
    [Google Scholar]
  3. Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge GE et al. Global honey bee viral landscape altered by a parasitic mite. Science 2012; 336: 1304– 1306 [Crossref]
    [Google Scholar]
  4. Mondet F, de Miranda JR, Kretzschmar A, Le Conte Y, Mercer AR. On the front line: quantitative virus dynamics in honeybee (Apis mellifera L.) colonies along a new expansion front of the parasite Varroa destructor. PLoS Pathog 2014; 10: e1004323 [CrossRef] [PubMed]
    [Google Scholar]
  5. Genersch E, Aubert M. Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Vet Res 2010; 41: 54 [CrossRef] [PubMed]
    [Google Scholar]
  6. Roberts JMK, Anderson DL, Durr PA. Absence of deformed wing virus and Varroa destructor in Australia provides unique perspectives on honeybee viral landscapes and colony losses. Sci Rep 2017; 7: 6925 [CrossRef] [PubMed]
    [Google Scholar]
  7. McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Current Opinion in Insect Science 2015; 8: 121– 129 [Crossref]
    [Google Scholar]
  8. de Miranda JR, Genersch E. Deformed wing virus. J Invertebr Pathol 2010; 103: S48– S61 [CrossRef] [PubMed]
    [Google Scholar]
  9. Runckel C, Flenniken ML, Engel JC, Ruby JG, Ganem D et al. Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia. PLoS One 2011; 6: e20656 [CrossRef] [PubMed]
    [Google Scholar]
  10. Daughenbaugh KF, Martin M, Brutscher LM, Cavigli I, Garcia E et al. Honey bee infecting Lake Sinai viruses. Viruses-Basel 2015; 7: 3285– 3309 [Crossref]
    [Google Scholar]
  11. Mordecai GJ, Wilfert L, Martin SJ, Jones IM, Schroeder DC. Diversity in a honey bee pathogen: first report of a third master variant of the deformed wing virus quasispecies. Isme Journal 2016; 10: 1264– 1273 [Crossref]
    [Google Scholar]
  12. de Miranda JR, Cornman RS, Evans JD, Semberg E, Haddad N et al. Genome characterization, prevalence and distribution of a Macula-like virus from Apis mellifera and Varroa destructor. Viruses-Basel 2015; 7: 3586– 3602 [Crossref]
    [Google Scholar]
  13. Remnant EJ, Shi M, Buchmann G, Blacquière T, Holmes EC et al. A diverse range of novel RNA viruses in geographically distinct honey bee populations. J Virol 2017; 91: e00158-17 [CrossRef] [PubMed]
    [Google Scholar]
  14. Levin S, Galbraith D, Sela N, Erez T, Grozinger CM et al. Presence of Apis rhabdovirus-1 in populations of pollinators and their parasites from two continents. Front Microbiol 2017; 8: 2482 [CrossRef] [PubMed]
    [Google Scholar]
  15. Chen YP, Siede R. Honey bee viruses. In Advances in Virus Research San Diego: Elsevier Academic Press Inc; 2007; pp. 33– 80
    [Google Scholar]
  16. de Miranda JR, Bailey L, Ball BV, Blanchard P, Budge GE et al. Standard methods for virus research in Apis mellifera. J Apic Res 2013; 52: 1– 56 [CrossRef]
    [Google Scholar]
  17. Webster CL, Waldron FM, Robertson S, Crowson D, Ferrari G et al. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS biology 2015; 13: e1002210 [Crossref]
    [Google Scholar]
  18. Nouri S, Salem N, Nigg JC, Falk BW. Diverse array of new viral sequences identified in worldwide populations of the Asian Citrus Psyllid (Diaphorina citri) using viral metagenomics. J Virol 2016; 90: 2434– 2445 [CrossRef] [PubMed]
    [Google Scholar]
  19. Ge X, Li Y, Yang X, Zhang H, Zhou P et al. Metagenomic analysis of viruses from bat fecal samples reveals many novel viruses in insectivorous bats in China. J Virol 2012; 86: 4620– 4630 [CrossRef] [PubMed]
    [Google Scholar]
  20. Fauver JR, Grubaugh ND, Krajacich BJ, Weger-Lucarelli J, Lakin SM et al. West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses, and totiviruses. Virology 2016; 498: 288– 299 [Crossref]
    [Google Scholar]
  21. Temmam S, Monteil-Bouchard S, Robert C, Baudoin JP, Sambou M et al. Characterization of viral communities of biting midges and identification of novel Thogotovirus species and Rhabdovirus genus. Viruses 2016; 8: 77 [CrossRef] [PubMed]
    [Google Scholar]
  22. Donaldson EF, Haskew AN, Gates JE, Huynh J, Moore CJ et al. Metagenomic analysis of the viromes of three North American bat species: viral diversity among different bat species that share a common habitat. J Virol 2010; 84: 13004– 13018 [CrossRef] [PubMed]
    [Google Scholar]
  23. Tokarz R, Williams SH, Sameroff S, Sanchez Leon M, Jain K et al. Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses. J Virol 2014; 88: 11480– 11492 [CrossRef] [PubMed]
    [Google Scholar]
  24. Webster CL, Longdon B, Lewis SH, Obbard DJ. Twenty-five new viruses associated with the Drosophilidae (Diptera). Evol BioinformOnline 2016; 12: 13– 25
    [Google Scholar]
  25. Shi M, Lin XD, Tian JH, Chen LJ, Chen X et al. Redefining the invertebrate RNA virosphere. Nature 2016; 540: 539– 543 [CrossRef] [PubMed]
    [Google Scholar]
  26. Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC et al. A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission. PLoS pathogens 2014; 10: e1004230 [Crossref]
    [Google Scholar]
  27. Le Gall O, Christian P, Fauquet CM, King AM, Knowles NJ et al. Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T = 3 virion architecture. Arch Virol 2008; 153: 715– 727 [CrossRef] [PubMed]
    [Google Scholar]
  28. Toriyama S, Guy PL, Fuji S, Takahashi M. Characterization of a new picorna-like virus, himetobi P virus, in plant hoppers. J Gen Virol 1992; 73: 1021– 1023 [CrossRef] [PubMed]
    [Google Scholar]
  29. Xu Y, Huang L, Wang Z, Fu S, Che J et al. Identification of Himetobi P virus in the small brown planthopper by deep sequencing and assembly of virus-derived small interfering RNAs. Virus Res 2014; 179: 235– 240 [CrossRef] [PubMed]
    [Google Scholar]
  30. Scotti PD, Gibbs AJ, Wrigley NG. Kelp fly virus. J Gen Virol 1976; 30: 1– 9 [CrossRef]
    [Google Scholar]
  31. Hartley CJ, Greenwood DR, Gilbert RJ, Masoumi A, Gordon KH et al. Kelp fly virus: a novel group of insect picorna-like viruses as defined by genome sequence analysis and a distinctive virion structure. J Virol 2005; 79: 13385– 13398 [CrossRef] [PubMed]
    [Google Scholar]
  32. Schoonvaere K, de Smet L, Smagghe G, Vierstraete A, Braeckman BP et al. Unbiased RNA shotgun metagenomics in social and solitary wild bees detects associations with eukaryote parasites and new viruses. PLoS One 2016; 11: e0168456 [CrossRef] [PubMed]
    [Google Scholar]
  33. Schoonvaere K, Smagghe G, Francis F, de Graaf DC. Study of the metatranscriptome of eight social and solitary wild bee species reveals novel viruses and bee parasites. Front Microbiol 2018; 9: 177 [CrossRef] [PubMed]
    [Google Scholar]
  34. Mihara T, Nishimura Y, Shimizu Y, Nishiyama H, Yoshikawa G et al. Linking virus genomes with host taxonomy. Viruses 2016; 8: 66 [CrossRef] [PubMed]
    [Google Scholar]
  35. Di Prisco G, Pennacchio F, Caprio E, Boncristiani HF, Evans JD et al. Varroa destructor is an effective vector of Israeli acute paralysis virus in the honeybee, Apis mellifera. J Gen Virol 2011; 92: 151– 155 [CrossRef] [PubMed]
    [Google Scholar]
  36. de Miranda JR, Cordoni G, Budge G. The acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J Invertebr Pathol 2010; 103: S30– S47 [CrossRef] [PubMed]
    [Google Scholar]
  37. Carrillo-Tripp J, Dolezal AG, Goblirsch MJ, Miller WA, Toth AL et al. In vivo and in vitro infection dynamics of honey bee viruses. Sci Rep 2016; 6: 22265 [CrossRef] [PubMed]
    [Google Scholar]
  38. Chen Y, Zhao Y, Hammond J, Hsu HT, Evans J et al. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J Invertebr Pathol 2004; 87: 84– 93 [CrossRef] [PubMed]
    [Google Scholar]
  39. Tentcheva D, Gauthier L, Zappulla N, Dainat B, Cousserans F et al. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl Environ Microbiol 2004; 70: 7185– 7191 [CrossRef] [PubMed]
    [Google Scholar]
  40. Genersch E, von der Ohe W, Kaatz H, Schroeder A, Otten C et al. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 2010; 41: 332– 352 [CrossRef]
    [Google Scholar]
  41. Traynor KS, Rennich K, Forsgren E, Rose R, Pettis J et al. Multiyear survey targeting disease incidence in US honey bees. Apidologie 2016; 47: 325– 347 [Crossref]
    [Google Scholar]
  42. Mordecai GJ, Brettell LE, Martin SJ, Dixon D, Jones IM et al. Superinfection exclusion and the long-term survival of honey bees in Varroa-infested colonies. ISME J 2016; 10: 1182– 1191 [CrossRef] [PubMed]
    [Google Scholar]
  43. Todd JH, De Miranda JR, Ball BV. Incidence and molecular characterization of viruses found in dying New Zealand honey bee (Apis mellifera) colonies infested with Varroa destructor. Apidologie 2007; 38: 354– 367 [CrossRef]
    [Google Scholar]
  44. Berényi O, Bakonyi T, Derakhshifar I, Köglberger H, Topolska G et al. Phylogenetic analysis of deformed wing virus genotypes from diverse geographic origins indicates recent global distribution of the virus. Appl Environ Microbiol 2007; 73: 3605– 3611 [CrossRef] [PubMed]
    [Google Scholar]
  45. Granberg F, Vicente-Rubiano M, Rubio-Guerri C, Karlsson OE, Kukielka D et al. Metagenomic detection of viral pathogens in Spanish honeybees: co-infection by aphid lethal paralysis, Israel acute paralysis and Lake Sinai viruses. PLoS One 2013; 8: e57459 [CrossRef] [PubMed]
    [Google Scholar]
  46. Ravoet J, Maharramov J, Meeus I, de Smet L, Wenseleers T et al. Comprehensive bee pathogen screening in Belgium reveals Crithidia mellificae as a new contributory factor to winter mortality. PLoS One 2013; 8: e72443 [CrossRef] [PubMed]
    [Google Scholar]
  47. Liu S, Vijayendran D, Carrillo-Tripp J, Miller WA, Bonning BC. Analysis of new aphid lethal paralysis virus (ALPV) isolates suggests evolution of two ALPV species. J Gen Virol 2014; 95: 2809– 2819 [CrossRef] [PubMed]
    [Google Scholar]
  48. Greninger AL, Jerome KR. Draft genome sequence of goose dicistrovirus. Genome Announc 2016; 4: e00068-16 [CrossRef] [PubMed]
    [Google Scholar]
  49. Carrillo-Tripp J, Bonning BC, Miller WA. Challenges associated with research on RNA viruses of insects. Curr Opin Insect Sci 2015; 8: 62– 68 [CrossRef]
    [Google Scholar]
  50. Giacobino A, Molineri AI, Pacini A, Fondevila N, Pietronave H et al. Varroa destructor and viruses association in honey bee colonies under different climatic conditions. Environ Microbiol Rep 2016; 8: 407– 412 [CrossRef] [PubMed]
    [Google Scholar]
  51. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731– 2739 [CrossRef] [PubMed]
    [Google Scholar]
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