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Comparison of Varroa destructor and Worker Honeybee Microbiota Within Hives Indicates Shared Bacteria

  • Invertebrate Microbiology
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Abstract

The ectoparasitic mite Varroa destructor is a major pest of the honeybee Apis mellifera. In a previous study, bacteria were found in the guts of mites collected from winter beehive debris and were identified using Sanger sequencing of their 16S rRNA genes. In this study, community comparison and diversity analyses were performed to examine the microbiota of honeybees and mites at the population level. The microbiota of the mites and honeybees in 26 colonies in seven apiaries in Czechia was studied. Between 10 and 50 Varroa females were collected from the bottom board, and 10 worker bees were removed from the peripheral comb of the same beehive. Both bees and mites were surface sterilized. Analysis of the 16S rRNA gene libraries revealed significant differences in the Varroa and honeybee microbiota. The Varroa microbiota was less diverse than was the honeybee microbiota, and the relative abundances of bacterial taxa in the mite and bee microbiota differed. The Varroa mites, but not the honeybees, were found to be inhabited by Diplorickettsia. The relative abundance of Arsenophonus, Morganella, Spiroplasma, Enterococcus, and Pseudomonas was higher in Varroa than in honeybees, and the Diplorickettsia symbiont detected in this study is specific to Varroa mites. The results demonstrated that there are shared bacteria between Varroa and honeybee populations but that these bacteria occur in different relative proportions in the honeybee and mite bacteriomes. These results support the suggestion of bacterial transfer via mites, although only some of the transferred bacteria may be harmful.

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References

  1. Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97

    Article  CAS  PubMed  Google Scholar 

  2. Alippi AM (1999) Bacterial diseases. In: Colin ME, Ball BV, Kilani M (eds) Bee disease diagnosis. Options mediterraneennes: serie B, vol 25, Etudes et recherches. CIHEAM, Zaragoza, pp 31–59

    Google Scholar 

  3. Mouches C, Bove JM, Tully JG, Rose DL, McCoy RE, Carle-Junca P, Garnier M, Saillard C (1983) Spiroplasma apis, a new species from the honey-bee Apis mellifera. Ann Microbiol (Inst Pasteur) 134A:383–397

    Article  CAS  Google Scholar 

  4. Mouches C, Bove JM, Albisetti J (1984) Pathogenicity of Spiroplasma apis and other spiroplasmas for honey-bees in southwestern France. Ann Microbiol (Inst Pasteur) 135A:151–155

    Article  CAS  Google Scholar 

  5. Schwarz RS, Teixeira EW, Tauber JP, Birke JM, Martins MF, Fonseca I, Evans JD (2014) Honey bee colonies act as reservoirs for two Spiroplasma facultative symbionts and incur complex, multiyear infection dynamics. Microbiol Open 3:341–355

    Article  Google Scholar 

  6. Cornman RS, Schatz MC, Johnston SJ, Chen Y-P, Pettis J, Hunt G, Bourgeois L, Elsik C, Anderson D, Grozinger CM, Jay D, Evans JD (2010) Genomic survey of the ectoparasitic mite Varroa destructor, a major pest of the honey bee Apis mellifera. BMC Genomics 11:602. doi:10.1186/1471-2164-11-602

    Article  PubMed  PubMed Central  Google Scholar 

  7. Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41:353–363

    Article  Google Scholar 

  8. Dietemann V, Pflugfelder J, Anderson D, Charriere J-D, Chejanovsky N, Dainat B, de Miranda J, Delaplane K, Dillier F-X, Fuch S, Gallmann P, Gauthier L, Imdorf A, Koeniger N, Kralj J, Meikle W, Pettis J, Rosenkranz P, Sammataro D, Smith D, Yanez O, Neumann P (2012) Varroa destructor: research avenues towards sustainable control. J Apic Res 51:125–132

    Article  Google Scholar 

  9. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:S96–S119

    Article  PubMed  Google Scholar 

  10. Bowen-Walker PL, Gunn A (2001) The effect of the ectoparasitic mite, Varroa destructor on adult worker honeybee (Apis mellifera) emergence weights, water, protein, carbohydrate, and lipid levels. Entomol Exp Appl 101:207–217

    Article  CAS  Google Scholar 

  11. Annoscia D, Del Piccolo F, Nazzi F (2012) How does the mite Varroa destructor kill the honeybee Apis mellifera? Alteration of cuticular hydrocarbons and water loss in infested honeybees. J Insect Physiol 58:1548–1555

    Article  CAS  PubMed  Google Scholar 

  12. Erban T, Harant K, Hubalek M, Vitamvas P, Kamler M, Poltronieri P, Tyl J, Markovic M, Titera D (2015) In-depth proteomic analysis of Varroa destructor: detection of DWV-complex, ABPV, VdMLV and honeybee proteins in the mite. Sci Rep 5:13907. doi:10.1038/srep13907

    Article  PubMed  PubMed Central  Google Scholar 

  13. Martin S, Hogarth A, van Breda J, Perrett J (1998) A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera L. colonies in the United Kingdom. Apidologie 29:369–370

    Article  Google Scholar 

  14. Grobov OF, Sotnikov AN, Shtondina DA (2008) Interaction of Varroa destructor to different organisms. [Vzaimootnosheniya Varroa destructor s razlichnymi organizmami.] Vet patol 26:5–19. (in Russian)

  15. Ryabov EV, Wood GR, Fannon JM, Moore JD, Bull JC, Chandler D, Mead A, Burroughs N, Evans DJ (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. doi:10.1371/journal.ppat.1004230

    Article  PubMed  PubMed Central  Google Scholar 

  16. Liu TP, Ritter W (1988) Morphology of some microorganisms associated with the female mite Varroa jacobsoni: a survey by electron microscopy. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds) Africanized honeybees and bee mites. Ellis Horwood, Chichester, pp 467–474

    Google Scholar 

  17. Cicero JM, Sammataro D (2010) The salivary glands of adult female Varroa destructor (Acari: Varroidae), an ectoparasite of the honey bee, Apis mellifera (Hymenoptera: Apidae). Int J Acarol 36:377–386

    Article  Google Scholar 

  18. Hubert J, Erban T, Kamler M, Kopecky J, Nesvorna M, Hejdankova S, Titera D, Tyl J, Zurek L (2015) Bacteria detected in the honeybee parasitic mite Varroa destructor collected from beehive winter debris. J Appl Microbiol 119:640–654

    Article  CAS  PubMed  Google Scholar 

  19. Glinski ZF, Jarosz J (1990) Serratia marcescens, artificially contaminating brood and worker honeybees, contaminates the Varroa jacobsoni mite. J Apic Res 29:107–111

    Article  Google Scholar 

  20. Sandionigi A, Vicario S, Prosdocimi EM, Galimberti A, Ferri E, Bruno A, Balech B, Mezzasalma V, Casiraghi M (2015) Towards a better understanding of Apis mellifera and Varroa destructor microbiomes: introducing ‘phyloh’ as a novel phylogenetic diversity analysis tool. Mol Ecol Resour 15:697–710

    Article  CAS  PubMed  Google Scholar 

  21. Glinski Z, Jarosz J (1990) Micro-organisms associated fortuitously with Varroa jacobsoni. Microbios 62:59–68

    Google Scholar 

  22. Kanbar G, Engels W (2003) Ultrastructure and bacterial infection of wounds in honey bee (Apis mellifera) pupae punctured by Varroa mites. Parasitol Res 90:349–354

    Article  CAS  PubMed  Google Scholar 

  23. Kanbar G, Engels W, Nicholson GJ, Hertle R, Winkelmann G (2004) Tyramine functions as a toxin in honey bee larvae during Varroa-transmitted infection by Melissococcus pluton. FEMS Microbiol Lett 234:149–154

    Article  CAS  PubMed  Google Scholar 

  24. Kanbar G, Engels W, Nicholson GJ, Hertle R, Winkelmann G (2005) Corrigendum to: “Tyramine functions as a toxin in honey bee larvae during Varroa-transmitted infection by Melissococcus pluton”. FEMS Microbiol Lett 234(2004):149–154, FEMS Microbiol Lett 245:193–193

    Google Scholar 

  25. Alippi AM, Albo GN, Marcangeli J, Leniz D, Noriega A (1995) The mite Varroa jacobsoni does not transmit American foulbrood from infected to healthy colonies. Exp Appl Acarol 19:607–613

    Article  Google Scholar 

  26. De Rycke PH, Joubert JJ, Hosseinian SH, Jacobs FJ (2002) The possible role of Varroa destructor in the spreading of American foulbrood among apiaries. Exp Appl Acarol 27:313–318

    Article  PubMed  Google Scholar 

  27. Glinski Z, Jarosz J (1992) Varroa jacobsoni as a carrier of bacterial infections to a recipient bee host. Apidologie 23:25–31

    Article  Google Scholar 

  28. Kopecky J, Nesvorna M, Hubert J (2014) Bartonella-like bacteria carried by domestic mite species. Exp Appl Acarol 64:21–32

    Article  CAS  PubMed  Google Scholar 

  29. Barbieri E, Paster BJ, Hughes D, Zurek L, Moser DP, Teske A, Sogin ML (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ Microbiol 3:151–167

    Article  CAS  PubMed  Google Scholar 

  30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998

    Article  CAS  PubMed  Google Scholar 

  33. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642

    Article  CAS  PubMed  Google Scholar 

  34. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596

    Article  CAS  PubMed  Google Scholar 

  35. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cariveau DP, Elijah Powell J, Koch H, Winfree R, Moran NA (2014) Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus). ISME J 8:2369–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinf 12:385. doi:10.1186/1471-2105-12-385

    Article  Google Scholar 

  39. Engel P, James RR, Koga R, Kwong WK, McFrederick QS, Moran NA (2013) Standard methods for research on Apis mellifera gut symbionts. J Apic Res 52:UNSP 52.4.07. doi:10.3896/IBRA.1.52.4.07

  40. Kutner MH, Nachtsheim CJ, Neter J, Li W (2005) Applied linear statistical models, 5th edn. McGraw-Hill Irwin, Boston

    Google Scholar 

  41. Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  42. Labovitz S (1970) The assignment of numbers to rank order categories. Am Sociol Rev 35:515–524

    Article  Google Scholar 

  43. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 16 Dec 2015

  44. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: community ecology package. CRAN—The Comprehensive R Archive Network. http://CRAN.R-project.org/package=vegan. Accessed 16 Dec 2015

  45. Stewart CN Jr, Excoffier L (1996) Assessing population genetic structure and variability with RAPD data: application to Vaccinium macrocarpon (American cranberry). J Evol Biol 9:153–171

    Article  CAS  Google Scholar 

  46. Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83:557–574

    Article  Google Scholar 

  47. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:4. http://palaeo-electronica.org/2001_1/past/issue1_01.htm. Accessed 7 Aug 2015

  48. Chao A, Chazdon RL, Colwell RK, Shen T-J (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159

    Article  Google Scholar 

  49. Cailliez F (1983) The analytical solution of the additive constant problem. Psychometrika 48:305–308

    Article  Google Scholar 

  50. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5, e1000352. doi:10.1371/journal.pcbi.1000352

    Article  PubMed  PubMed Central  Google Scholar 

  51. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2015) gplots: various R programming tools for plotting data. CRAN—The Comprehensive R Archive Network. https://CRAN.R-project.org/package=gplots. Accessed 16 Dec 2015

  52. Whitaker D, Christman M (2014) clustsig: significant cluster analysis. CRAN—The Comprehensive R Archive Network. https://CRAN.R-project.org/package=clustsig. Accessed 16 Dec 2015

  53. Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69

    Article  Google Scholar 

  54. Vanikova S, Noskova A, Pristas P, Judova J, Javorsky P (2015) Heterotrophic bacteria associated with Varroa destructor mite. Apidologie 46:369–379

    Article  CAS  Google Scholar 

  55. De Ruijter A, Kaas JP (1983) The anatomy of the Varroa-mite. In: Cavalloro R (ed) Varroa jacobsoni Oud. affecting honey bees: present status and needs. Proceedings of a Meeting of the EC Experts’ Group / Wageningen, 7–9 February 1983. A.A.Balkema, Rotterdam, Netherlands, pp 45–47

  56. Novakova E, Hypsa V, Moran NA (2009) Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9:143. doi:10.1186/1471-2180-9-143

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hypsa V, Dale C (1997) In vitro culture and phylogenetic analysis of “Candidatus Arsenophonus triatominarum”, an intracellular bacterium from the triatomine bug, Triatoma infestans. Int J Syst Bacteriol 47:1140–1144

    Article  CAS  PubMed  Google Scholar 

  58. Corby-Harris V, Maes P, Anderson KE (2014) The bacterial communities associated with honey bee (Apis mellifera) foragers. PLoS ONE 9, e95056. doi:10.1371/journal.pone.0095056

    Article  PubMed  PubMed Central  Google Scholar 

  59. Clark TB (1977) Spiroplasma sp., a new pathogen in honey bees. J Invertebr Pathol 29:112–113

    Article  Google Scholar 

  60. Meeus I, Vercruysse V, Smagghe G (2012) Molecular detection of Spiroplasma apis and Spiroplasma melliferum in bees. J Invertebr Pathol 109:172–174

    Article  CAS  PubMed  Google Scholar 

  61. Paredes JC, Herren JK, Schupfer F, Marin R, Claverol S, Kuo C-H, Lemaitre B, Beven L (2015) Genome sequence of the Drosophila melanogaster male-killing Spiroplasma strain MSRO endosymbiont. MBio 6:e02437–14. doi:10.1128/mBio.02437-14

    Article  PubMed  PubMed Central  Google Scholar 

  62. Bruce WA, Hackett KJ, Shimanuki H, Henegar RB (1990) Bee mites: vectors of honey bee pathogens? In: Ritter W (ed) Proceedings of the International Symposium on Recent Research on Bee Pathology, September 5–7, 1990, Gent. International Federation of Beekeepers Association Apimondia, Gent, pp 180–182

    Google Scholar 

  63. Boecking O, Genersch E (2008) Varroosis—the ongoing crisis in bee keeping. J Consum Protect Food Saf 3:221–228

    Google Scholar 

  64. Mouton L, Thierry M, Henri H, Baudin R, Gnankine O, Reynaud B, Zchori-Fein E, Becker N, Fleury F, Delatte H (2012) Evidence of diversity and recombination in Arsenophonus symbionts of the Bemisia tabaci species complex. BMC Microbiol 12:S10. doi:10.1186/1471-2180-12-S1-S10

    Article  PubMed  PubMed Central  Google Scholar 

  65. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M (2007) Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3:23–25

    Article  CAS  PubMed  Google Scholar 

  66. Nakayama S, Parratt SR, Hutchence KJ, Lewis Z, Price TAR, Hurst GDD (2015) Can maternally inherited endosymbionts adapt to a novel host? Direct costs of Spiroplasma infection, but not vertical transmission efficiency, evolve rapidly after horizontal transfer into D. melanogaster. Heredity 114:539–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Chechetkina UE, Evteeva NI, Rechkin AI (2010) Comparison of the composition of enterobacteria in honey bees Apis mellifera L. during the wintering and in the active honey season. Vestn Nizhegorod Univ N I Lobachevskogo 2:475–478 (in Russian with English summary)

    Google Scholar 

  68. Lyapunov YE, Kuzyaev RZ, Khismatullin RG, Bezgodova OA (2008) Intestinal enterobacteria of the hibernating Apis mellifera mellifera L. bees. Microbiology 77:373–379

    Article  CAS  Google Scholar 

  69. Gupta AK, Nayduch D, Verma P, Shah B, Ghate H, Patole M, Shouche Y (2012) Phylogenetic characterization of bacteria in the gut of house flies (Musca domestica L.). FEMS Microbiol Ecol 79:581–593

    Article  CAS  PubMed  Google Scholar 

  70. Audisio MC, Terzolo HR, Apella MC (2005) Bacteriocin from honeybee beebread Enterococcus avium, active against Listeria monocytogenes. Appl Environ Microbiol 71:3373–3375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Lewis CM, Zervos MJ (1990) Clinical manifestations of enterococcal infection. Eur J Clin Microbiol Infect Dis 9:111–117

    Article  CAS  PubMed  Google Scholar 

  72. Nagoba BS, Selkar SP, Wadher BJ, Gandhi RC (2013) Acetic acid treatment of pseudomonal wound infections—a review. J Infect Public Health 6:410–415

    Article  CAS  PubMed  Google Scholar 

  73. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:619–628

    Article  PubMed  Google Scholar 

  74. Martinson VG, Moy J, Moran NA (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830–2840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci U S A 109:11002–11007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Engel P, Moran NA (2013) The gut microbiota of insects—diversity in structure and function. FEMS Microbiol Rev 37:699–735

    Article  CAS  PubMed  Google Scholar 

  77. Kwong WK, Moran NA (2013) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. Int J Syst Evol Microbiol 63:2008–2018

    Article  CAS  PubMed  Google Scholar 

  78. Moran NA (2015) Genomics of the honey bee microbiome. Curr Opin Insect Sci 10:22–28

    Article  PubMed  Google Scholar 

  79. Mediannikov O, Sekeyova Z, Birg M-L, Raoult D (2010) A novel obligate intracellular gamma-proteobacterium associated with ixodid ticks, Diplorickettsia massiliensis, gen. nov., sp. nov. PLoS ONE 5, e11478. doi:10.1371/journal.pone.0011478

    Article  PubMed  PubMed Central  Google Scholar 

  80. Taylor M, Mediannikov O, Raoult D, Greub G (2012) Endosymbiotic bacteria associated with nematodes, ticks and amoebae. FEMS Immunol Med Microbiol 64:21–31

    Article  CAS  PubMed  Google Scholar 

  81. Nuzzaci G, de Lillo E (1995) Functional morphology of the mouthparts of Varroa jacobsoni Oudemans female (Acari: Varroidae). In: Kropczynska D, Boczek J, Tomczyk A (eds) The Acari: physiological and ecological aspects of Acari–host relationships. Dabor, Warszawa, pp 79–89

    Google Scholar 

  82. Strick H, Madel G (1988) Transmission of the pathogenic bacterium Hafnia alvei to honey bees by the ectoparasitic mite Varroa jacobsoni. In: Needham GR, Page RE Jr, Delfinado-Baker M, Bowman CE (eds) Africanized honeybees and bee mites. Ellis Horwood, Chichester, pp 462–466

    Google Scholar 

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Acknowledgments

This study was supported by the Ministry of Education, Youth and Sports of the Czech Republic through Grant No. LH14060 (KONTAKT; cooperation between Czechia and the USA). The authors thank Sylvie Hejdankova and Martin Markovic for their technical help. We appreciate the advice provided by the reviewers of the original manuscript. We also acknowledge the help and support of beekeepers in the collection of data and samples. Finally, we thank the American Journal Experts for providing language editing service.

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Hubert, J., Kamler, M., Nesvorna, M. et al. Comparison of Varroa destructor and Worker Honeybee Microbiota Within Hives Indicates Shared Bacteria. Microb Ecol 72, 448–459 (2016). https://doi.org/10.1007/s00248-016-0776-y

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