1887

Abstract

By providing pollination services, bees are among the most important insects, both in ecological and economical terms. Combined next-generation and classical sequencing approaches were applied to discover and study new insect viruses potentially harmful to bees. A bioinformatics virus discovery pipeline was used on individual Illumina transcriptomes of 13 wild bees from three species from the genus and 30 ants from six species of the genera and . This allowed the discovery and description of three sequences of a new virus termed Halictus scabiosae Adlikon virus (HsAV). Phylogenetic analyses of ORF1, RNA-dependent RNA-polymerase (RdRp) and capsid genes showed that HsAV is closely related to (+)ssRNA viruses of the unassigned genus but distant enough to belong to a different new genus we called Halictivirus. In addition, our study of ant transcriptomes revealed the first four sinaivirus sequences from ants (, and ). Maximum likelihood phylogenetic analyses were performed on a 594 nt fragment of the ORF1/RdRp region from 84 sinaivirus sequences, including 31 new Lake Sinai viruses (LSVs) from honey bees collected in five countries across the globe and the four ant viral sequences. The phylogeny revealed four main clades potentially representing different viral species infecting honey bees. Moreover, the ant viruses belonged to the LSV4 clade, suggesting a possible cross-species transmission between bees and ants. Lastly, wide honey bee screening showed that all four LSV clades have worldwide distributions with no obvious geographical segregation.

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2017-11-01
2019-12-11
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References

  1. Gallai N, Salles J-M, Settele J, Vaissière BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 2009;68:810–821 [CrossRef]
    [Google Scholar]
  2. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA et al. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 2007;274:303–313 [CrossRef][PubMed]
    [Google Scholar]
  3. Core A, Runckel C, Ivers J, Quock C, Siapno T et al. A new threat to honey bees, the parasitic phorid fly Apocephalus borealis. PLoS One 2012;7:e29639 [CrossRef][PubMed]
    [Google Scholar]
  4. Doublet V, Labarussias M, de Miranda JR, Moritz RF, Paxton RJ. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ Microbiol 2015;17:969–983 [CrossRef][PubMed]
    [Google Scholar]
  5. Evans JD, Schwarz RS. Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol 2011;19:614–620 [CrossRef][PubMed]
    [Google Scholar]
  6. Fairbrother A, Purdy J, Anderson T, Fell R. Risks of neonicotinoid insecticides to honeybees. Environ Toxicol Chem 2014;33:719–731 [CrossRef][PubMed]
    [Google Scholar]
  7. Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015;347:1255957 [CrossRef][PubMed]
    [Google Scholar]
  8. Kielmanowicz MG, Inberg A, Lerner IM, Golani Y, Brown N et al. Prospective large-scale field study generates predictive model identifying major contributors to colony losses. PLoS Pathog 2015;11:e1004816 [CrossRef][PubMed]
    [Google Scholar]
  9. Menail AH, Piot N, Meeus I, Smagghe G, Loucif-Ayad W. Large pathogen screening reveals first report of Megaselia scalaris (Diptera: Phoridae) parasitizing Apis mellifera intermissa (Hymenoptera: Apidae). J Invertebr Pathol 2016;137:33–37 [CrossRef][PubMed]
    [Google Scholar]
  10. Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K et al. Are bee diseases linked to pesticides? – a brief review. Environ Int 2016;89-90:7–11 [CrossRef][PubMed]
    [Google Scholar]
  11. VanEngelsdorp D, Meixner MD. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 2010;103:S80–S95 [CrossRef][PubMed]
    [Google Scholar]
  12. Cornman RS, Tarpy DR, Chen Y, Jeffreys L, Lopez D et al. Pathogen webs in collapsing honey bee colonies. PLoS One 2012;7:e43562 [CrossRef][PubMed]
    [Google Scholar]
  13. 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]
  14. McMenamin AJ, Genersch E. Honey bee colony losses and associated viruses. Curr Opin Insect Sci 2015;8:121–129 [CrossRef]
    [Google Scholar]
  15. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 2010;25:345–353 [CrossRef][PubMed]
    [Google Scholar]
  16. Tehel A, Brown MJ, Paxton RJ. Impact of managed honey bee viruses on wild bees. Curr Opin Virol 2016;19:16–22 [CrossRef][PubMed]
    [Google Scholar]
  17. Bailey L, Gibbs AJ, Woods RD. Two viruses from adult honey bees (Apis mellifera Linnaeus). Virology 1963;21:390–395 [CrossRef][PubMed]
    [Google Scholar]
  18. 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]
  19. 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]
  20. Brutscher LM, McMenamin AJ, Flenniken ML. The buzz about honey bee viruses. PLoS Pathog 2016;12:e1005757 [CrossRef][PubMed]
    [Google Scholar]
  21. Clark TB. A filamentous virus of the honey bee. J Invertebr Pathol 1978;32:332–340 [CrossRef]
    [Google Scholar]
  22. Gauthier L, Cornman S, Hartmann U, Cousserans F, Evans JD et al. The Apis mellifera filamentous virus genome. Viruses 2015;7:3798–3815 [CrossRef][PubMed]
    [Google Scholar]
  23. 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]
  24. 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]
  25. Daughenbaugh KF, Martin M, Brutscher LM, Cavigli I, Garcia E et al. Honey bee infecting lake sinai viruses. Viruses 2015;7:3285–3309 [CrossRef][PubMed]
    [Google Scholar]
  26. Ravoet J, De Smet L, Wenseleers T, de Graaf DC. Genome sequence heterogeneity of Lake Sinai Virus found in honey bees and Orf1/RdRP-based polymorphisms in a single host. Virus Res 2015;201:67–72 [CrossRef][PubMed]
    [Google Scholar]
  27. Cavigli I, Daughenbaugh KF, Martin M, Lerch M, Banner K et al. Pathogen prevalence and abundance in honey bee colonies involved in almond pollination. Apidologie 2016;47:251–266 [CrossRef][PubMed]
    [Google Scholar]
  28. Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Del Nozal MJ et al. Holistic screening of collapsing honey bee colonies in Spain: a case study. BMC Res Notes 2014;7:649 [CrossRef][PubMed]
    [Google Scholar]
  29. 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]
  30. Parmentier L, Smagghe G, de Graaf DC, Meeus I. Varroa destructor Macula-like virus, Lake Sinai virus and other new RNA viruses in wild bumblebee hosts (Bombus pascuorum, Bombus lapidarius and Bombus pratorum). J Invertebr Pathol 2016;134:6–11 [CrossRef][PubMed]
    [Google Scholar]
  31. Ravoet J, De Smet L, Meeus I, Smagghe G, Wenseleers T et al. Widespread occurrence of honey bee pathogens in solitary bees. J Invertebr Pathol 2014;122:55–58 [CrossRef][PubMed]
    [Google Scholar]
  32. 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]
  33. Amakpe F, De Smet L, Brunain M, Ravoet J, Jacobs FJ et al. Discovery of Lake Sinai virus and an unusual strain of acute bee paralysis virus in West African apiaries. Apidologie 2015;35–47
    [Google Scholar]
  34. Gamboa V, Ravoet J, Brunain M, Smagghe G, Meeus I et al. Bee pathogens found in Bombus atratus from Colombia: a case study. J Invertebr Pathol 2015;129:36–39 [CrossRef][PubMed]
    [Google Scholar]
  35. Ahola T, Karlin DG. Sequence analysis reveals a conserved extension in the capping enzyme of the alphavirus supergroup, and a homologous domain in nodaviruses. Biol Direct 2015;10:16 [CrossRef][PubMed]
    [Google Scholar]
  36. Kuchibhatla DB, Sherman WA, Chung BY, Cook S, Schneider G et al. Powerful sequence similarity search methods and in-depth manual analyses can identify remote homologs in many apparently "orphan" viral proteins. J Virol 2014;88:10–20 [CrossRef][PubMed]
    [Google Scholar]
  37. Ravoet J, de Smet L, Wenseleers T, de Graaf DC. Vertical transmission of honey bee viruses in a Belgian queen breeding program. BMC Vet Res 2015;11:61 [CrossRef][PubMed]
    [Google Scholar]
  38. Edwards RA, Rohwer F. Opinion: viral metagenomics. Nat Rev Microbiol 2005;3:504–510 [CrossRef]
    [Google Scholar]
  39. Mokili JL, Rohwer F, Dutilh BE. Metagenomics and future perspectives in virus discovery. Curr Opin Virol 2012;2:63–77 [CrossRef][PubMed]
    [Google Scholar]
  40. Rosario K, Breitbart M. Exploring the viral world through metagenomics. Curr Opin Virol 2011;1:289–297 [CrossRef][PubMed]
    [Google Scholar]
  41. Mordecai GJ, Brettell LE, Pachori P, Villalobos EM, Martin SJ et al. Moku virus; a new Iflavirus found in wasps, honey bees and Varroa. Sci Rep 2016;6:34983 [CrossRef][PubMed]
    [Google Scholar]
  42. Simmonds P, Adams MJ, Benkő M, Breitbart M, Brister JR et al. Consensus statement: virus taxonomy in the age of metagenomics. Nat Rev Microbiol 2017;15:161–168 [CrossRef][PubMed]
    [Google Scholar]
  43. Shirokikh NE, Spirin AS. Poly(A) leader of eukaryotic mRNA bypasses the dependence of translation on initiation factors. Proc Natl Acad Sci USA 2008;105:10738–10743 [CrossRef][PubMed]
    [Google Scholar]
  44. Manley R, Boots M, Wilfert L. Emerging viral disease risk to pollinating insects: ecological, evolutionary and anthropogenic factors. J Appl Ecol 2015;52:331–340 [CrossRef][PubMed]
    [Google Scholar]
  45. Evison SE, Roberts KE, Laurenson L, Pietravalle S, Hui J et al. Pervasiveness of parasites in pollinators. PLoS One 2012;7:e30641 [CrossRef][PubMed]
    [Google Scholar]
  46. Singh R, Levitt AL, Rajotte EG, Holmes EC, Ostiguy N et al. RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 2010;5:e14357 [CrossRef][PubMed]
    [Google Scholar]
  47. Yañez O, Zheng H-Q, Hu F-L, Neumann P, Dietemann V. A scientific note on Israeli acute paralysis virus infection of Eastern honeybee Apis cerana and vespine predator Vespa velutina. Apidologie 2012;43:587–589 [CrossRef]
    [Google Scholar]
  48. Monceau K, Bonnard O, Thiéry D. Vespa velutina: a new invasive predator of honeybees in Europe. J Pest Sci 2014;87:1–16 [CrossRef]
    [Google Scholar]
  49. Celle O, Blanchard P, Olivier V, Schurr F, Cougoule N et al. Detection of chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread. Virus Res 2008;133:280–284 [CrossRef][PubMed]
    [Google Scholar]
  50. Sébastien A, Lester PJ, Hall RJ, Wang J, Moore NE et al. Invasive ants carry novel viruses in their new range and form reservoirs for a honeybee pathogen. Biol Lett 2015;11:20150610 [CrossRef][PubMed]
    [Google Scholar]
  51. Yue C, Genersch E. RT-PCR analysis of deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). J Gen Virol 2005;86:3419–3424 [CrossRef][PubMed]
    [Google Scholar]
  52. Geoghegan JL, Duchêne S, Holmes EC. Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog 2017;13:e1006215 [CrossRef][PubMed]
    [Google Scholar]
  53. Drake JW, Holland JJ. Mutation rates among RNA viruses. Proc Natl Acad Sci USA 1999;96:13910–13913 [CrossRef][PubMed]
    [Google Scholar]
  54. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS et al. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 2008;72:457–470 [CrossRef][PubMed]
    [Google Scholar]
  55. Boncristiani HF, Di Prisco G, Pettis JS, Hamilton M, Chen YP. Molecular approaches to the analysis of deformed wing virus replication and pathogenesis in the honey bee, Apis mellifera. Virol J 2009;6:221 [CrossRef][PubMed]
    [Google Scholar]
  56. Gisder S, Aumeier P, Genersch E. Deformed wing virus: replication and viral load in mites (Varroa destructor). J Gen Virol 2009;90:463–467 [CrossRef][PubMed]
    [Google Scholar]
  57. Wilfert L, Long G, Leggett HC, Schmid-Hempel P, Butlin R et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 2016;351:594–597 [CrossRef][PubMed]
    [Google Scholar]
  58. Mazzei M, Carrozza ML, Luisi E, Forzan M, Giusti M et al. Infectivity of DWV associated to flower pollen: experimental evidence of a horizontal transmission route. PLoS One 2014;9:e113448 [CrossRef][PubMed]
    [Google Scholar]
  59. 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]
  60. Chen YP, Pettis JS, Corona M, Chen WP, Li CJ et al. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog 2014;10:e1004261 [CrossRef][PubMed]
    [Google Scholar]
  61. Palacios G, Hui J, Quan PL, Kalkstein A, Honkavuori KS et al. Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol 2008;82:6209–6217 [CrossRef][PubMed]
    [Google Scholar]
  62. Roberts JM, Anderson DL. A novel strain of sacbrood virus of interest to world apiculture. J Invertebr Pathol 2014;118:71–74 [CrossRef][PubMed]
    [Google Scholar]
  63. Reddy KE, Noh JH, Choe SE, Kweon CH, Yoo MS et al. Analysis of the complete genome sequence and capsid region of black queen cell viruses from infected honeybees (Apis mellifera) in Korea. Virus Genes 2013;47:126–132 [CrossRef][PubMed]
    [Google Scholar]
  64. Romiguier J, Lourenco J, Gayral P, Faivre N, Weinert LA et al. Population genomics of eusocial insects: the costs of a vertebrate-like effective population size. J Evol Biol 2014;27:593–603 [CrossRef][PubMed]
    [Google Scholar]
  65. Gayral P, Weinert L, Chiari Y, Tsagkogeorga G, Ballenghien M et al. Next-generation sequencing of transcriptomes: a guide to RNA isolation in nonmodel animals. Mol Ecol Resour 2011;11:650–661 [CrossRef][PubMed]
    [Google Scholar]
  66. Birol I, Jackman SD, Nielsen CB, Qian JQ, Varhol R et al. De novo transcriptome assembly with ABySS. Bioinformatics 2009;25:2872–2877 [CrossRef][PubMed]
    [Google Scholar]
  67. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ et al. ABySS: a parallel assembler for short read sequence data. Genome Res 2009;19:1117–1123 [CrossRef][PubMed]
    [Google Scholar]
  68. Cahais V, Gayral P, Tsagkogeorga G, Melo-Ferreira J, Ballenghien M et al. Reference-free transcriptome assembly in non-model animals from next-generation sequencing data. Mol Ecol Resour 2012;12:834–845 [CrossRef][PubMed]
    [Google Scholar]
  69. Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res 1999;9:868–877 [CrossRef][PubMed]
    [Google Scholar]
  70. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 2010;11:119 [CrossRef][PubMed]
    [Google Scholar]
  71. Hyatt D, Locascio PF, Hauser LJ, Uberbacher EC. Gene and translation initiation site prediction in metagenomic sequences. Bioinformatics 2012;28:2223–2230 [CrossRef][PubMed]
    [Google Scholar]
  72. Remmert M, Biegert A, Hauser A, Söding J. HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat Methods 2011;9:173–175 [CrossRef][PubMed]
    [Google Scholar]
  73. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005;21:951–960 [CrossRef][PubMed]
    [Google Scholar]
  74. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009;10:421 [CrossRef][PubMed]
    [Google Scholar]
  75. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012;28:1647–1649 [CrossRef][PubMed]
    [Google Scholar]
  76. Finn RD, Attwood TK, Babbitt PC, Bateman A, Bork P et al. InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res 2017;45:D190–D199 [CrossRef][PubMed]
    [Google Scholar]
  77. Jones P, Binns D, Chang HY, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014;30:1236–1240 [CrossRef][PubMed]
    [Google Scholar]
  78. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002;30:3059–3066 [CrossRef][PubMed]
    [Google Scholar]
  79. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005;21:2104–2105 [CrossRef][PubMed]
    [Google Scholar]
  80. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001;17:754–755 [CrossRef][PubMed]
    [Google Scholar]
  81. Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 2006;34:W609–W612 [CrossRef][PubMed]
    [Google Scholar]
  82. Kryazhimskiy S, Plotkin JB. The population genetics of dN/dS. PLoS Genet 2008;4:e1000304 [CrossRef][PubMed]
    [Google Scholar]
  83. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986;3:418–426[PubMed]
    [Google Scholar]
  84. Yang Z. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998;15:568–573 [CrossRef][PubMed]
    [Google Scholar]
  85. Yang Z, Bielawski JP. Statistical methods for detecting molecular adaptation. Trends Ecol Evol 2000;15:496–503 [CrossRef][PubMed]
    [Google Scholar]
  86. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007;24:1586–1591 [CrossRef][PubMed]
    [Google Scholar]
  87. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD et al. GARD: a genetic algorithm for recombination detection. Bioinformatics 2006;22:3096–3098 [CrossRef][PubMed]
    [Google Scholar]
  88. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010;26:2455–2457 [CrossRef][PubMed]
    [Google Scholar]
  89. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012;9:772 [CrossRef][PubMed]
    [Google Scholar]
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