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Heterotrophic bacteria associated with Varroa destructor mite

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Abstract

Varroa bee hive attack is a serious and common problem in bee keeping. In our work, an ecto-microflora of Varroa destructor mites was characterised as a potential source of bacterial bee diseases. Using a cultivation approach, a variable population of bacteria was isolated from the body surface of Varroa mites with frequency of about 150 cfu per mite individual. Nine studied isolates were classified to four genera and six species by a combination of matrix-assisted laser desorption ionization time-of-flight (MALDI-TOF)- and 16S ribosomal RNA (rRNA)-based methods, suggesting relatively low diversity of Varroa mite-associated ecto-microflora. The Varroa mite-associated bacterial population was found to be dominated by Gram-positive bacteria of Bacillus and Microbacterium genera. Gram-negative bacteria were represented by members of Brevundimonas and Rhizobium genera. Most of the identified species are not known to be associated with Varroa mite, either honey bee or honey up until now and some of them are probably representatives of new bacterial taxa.

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References

  • Alippi, A.M. (1995) Detection of Bacillus larvae spores in Argentinian honeys by using a semi-selective medium. Microbiologia. 11(3), 343–350

    CAS  PubMed  Google Scholar 

  • Alippi, A.M., Albo, G.N., 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(10), 607–613

    Article  Google Scholar 

  • Alippi, A.M., Reynaldi, F.J., López, A.C., De Giusti, M.R., Aguilar, O.M. (2004) Molecular epidemiology of Paenibacillus larvae larvae and incidence of American foulbrood in Argentinean honeys from Buenos Aires Province. J. Apic. Res. 43(3), 135–143

    CAS  Google Scholar 

  • Apte-Deshpande, A., Paingankar, M., Gokhale, M.D., Deobagkar, D.N. (2012) Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLoS ONE . doi:10.1371/journal.pone.0040401

    PubMed Central  PubMed  Google Scholar 

  • Ball, B.V. (1985) Acute paralysis virus isolated from honeybee colonies infested with Warroa jacobsoni. J. Apic. Res. 24, 115–119

    CAS  Google Scholar 

  • Ball, B.V. (1997) Secondary infections and diseases associated with Varroa jacobsoni. Options Méditerranéennes. 21, 49–58

    Google Scholar 

  • Beilstein, F., Dreiseikelmann, B. (2006) Bacteriophages of freshwater Brevundimonas vesicularis isolates. Res. Microbiol. 157(3), 213–219

    Article  CAS  PubMed  Google Scholar 

  • Benoit, J.B., Yoder, J.A., Sammataro, D., Zettler, L.W. (2004) Mycoflora and fungal vector capacity of the parasitic mite Varroa destructor (Mesostigmata: Varroidae) in honey bee (Hymenoptera: Apidae) colonies. Int. J. Acarol. 30(2), 103–106

    Article  Google Scholar 

  • Berényi, O., Bakonyi, T., Derakhshifar, I., Köglberger, H., Nowotny, N. (2006) Occurrence of six honeybee viruses in diseased Austrian apiaries. Appl. Environ. Microbiol. 72(4), 2414–2420

    Article  PubMed Central  PubMed  Google Scholar 

  • Boecking, O., Genersch, E. (2008) Varroosis - the ongoing crisis in bee keeping. J. Verbr. Lebensm. 3(2), 221–228

    Article  Google Scholar 

  • Bouzar, H., Jones, J.B., Hodge, N.C. (1993) Differential characterization of Agrobacterium species using carbon source utilization pattern and fatty acid profiles. Phytopathology 83(7), 733–739

    Article  CAS  Google Scholar 

  • Bowen-Walker, P.L., 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 

  • Bowen-Walker, P.L., Martin, S.J., Gunn, A. (1999) The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. J. Invertebr. Pathol 73(1), 101–106

    Google Scholar 

  • Chen, Y.P., Siede, R. (2007) Honey bee viruses. Adv. Virus Res. 70, 33–80

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y.P., Pettis, J.S., Evans, J.D., Kramer, M., Feldlaufer, M.F. (2004) Transmission of Kashmir bee virus by the ectoparasitic mite Varroa destructor. Apidologie. 35(4), 441–448

    Article  Google Scholar 

  • Davis, E.P., Boopathy, R., Manning, J. (1997) Use of trinitrobenzene as a nitrogen source by Pseudomonas vesicularis isolated from soil. Curr. Microbiol. 34(3), 192–197

    Article  CAS  PubMed  Google Scholar 

  • De la Rúa, P., Jaffé, R., Dall’Olio, R., Muñoz, I., Serrano, J. (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40(3), 263–284

    Article  Google Scholar 

  • De Rycke, P.H., Joubert, J.J., Hosseinian, S.H., Jacobs, F.J. (2002) The possible role of Varroa destructor in the spreading of American foulbrood among apiaries. Exp. Appl. Acarol. 27(4), 313–318

    Article  PubMed  Google Scholar 

  • Dworkin, M., Falkow, S., Rosemberg, E., Schleifer, K.H., Stackebrandt, E. (2006) The Prokaryotes: A Handbook on the Biology of Bacteria. Springer, Berlin

    Book  Google Scholar 

  • Egemen, O., Ozkaya, O., Bingol, D., Akan, M. (2012) Rhizobium radiobacter: an unusual pathogen isolated on an active chronic ulcerous inflammation. J. Plast. Reconstr. Aes. 65(8), 233–235

    Article  Google Scholar 

  • Escobar, M.A., Dandekar, A.M. (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci. 8(8), 380–386

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, L., Sánchez-Juanes, F., García-Fraile, P., Rivas, R., Mateos, P.F., et al. (2011) MALDI-TOF Mass Spectrometry Is a Fast and Reliable Platform for Identification and Ecological Studies of Species from Family Rhizobiaceae. PLoS ONE 6(5), e20223

  • Funke, G., Haase, G., Schnitzler, N., Schrage, N., Reinert, R.R. (1997) Endophthalmitis due to Microbacterium species: case report and review of microbacterium infections. Clin. Infect. Dis. 24(4), 713–716

    Article  CAS  PubMed  Google Scholar 

  • Genersch, E. (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J. Invertebr. Pathol. 103(suppl. 1), 10–19

    Article  Google Scholar 

  • Gilliam, M. (1978) Bacteria belonging to the genus Bacillus isolated from selected organs of queen honey bees, Apis mellifera. J. Invertebr. Pathol. 31(3), 389–391

    Article  CAS  PubMed  Google Scholar 

  • Gilliam, M. (1979) Microbiology of pollen and bee bread: the genus Bacillus. Apidologie 10(3), 269–274

    Article  Google Scholar 

  • Gilliam, M., Prest, D.B. (1987) Microbiology of feces of the larval honey bee, Apis mellifera. J. Invertebr. Pathol. 41(1), 70–75

    Article  Google Scholar 

  • Gilliam, M., Valentine, D.K. (1976) Bacteria isolated from the intestinal contents of foraging worker honey bees, Apis mellifera: the genus Bacillus. J. Invertebr. Pathol. 28(2), 275–276

    Article  Google Scholar 

  • Gliński, Z., Jarosz, J. (1992) Varroa jacobsoni as a carrier of bacterial infections to a recipient bee host. Apidologie 23(1), 25–31

    Article  Google Scholar 

  • Gutiérrez, A.M., Cabriales, J.J.P., Vega, M.M. (2010) Isolation and characterization of hexavalent chromium-reducing rhizospheric bacteria from a wetland. Int. J. Phytoremediation 12(4), 317–334

    Article  Google Scholar 

  • Hung, W.L., Wade, W.G., Boden, R., Kelly, D.P., Wood, A.P. (2011) Facultative methylotrophs from the human oral cavity and methylotrophy in strains of Gordonia, Leifsonia, and Microbacterium. Arch. Microbiol. 193(6), 407–417

    Article  CAS  PubMed  Google Scholar 

  • Indiragandhi, P., Yoon, C., Yang, J.O., Cho, S., Sa, T.M., Kim, G.H. (2010) Microbial communities in the developmental stages of B and Q biotypes of sweet potato whitefly, Bemisia tabaci (hemiptera: Aleyrodidae). J. Korean Soc. Appl. Biol. Chem. 53(5), 605–617

    Article  CAS  Google Scholar 

  • Iurlina, M.O., Fritz, R. (2005) Characterization of microorganisms in Argentinean honeys from different sources. Int. J. Food Microbiol. 105(3), 297–304

    Article  CAS  PubMed  Google Scholar 

  • Kacaniova, M., Chlebo, R., Kopernicky, M., Trakovicka, A. (2004) Microflora of the honeybee gastrointestinal tract. Folia Microbiol. 49(2), 169–171

    Article  CAS  Google Scholar 

  • Kim, O.S., Cho, Y.J., Lee, K., Yoon, S.H., Kim, M., et al. (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int. J. Syst. Evol. Microbiol. 62(3), 716–721

    Article  CAS  PubMed  Google Scholar 

  • Kotiranta, A., Lounatmaa, K., Haapasalo, M. (2000) Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect. 2(2), 189–198

    Article  CAS  PubMed  Google Scholar 

  • Laffineur, K., Avesani, V., Cornu, G., Charlier, J., Janssens, M., Wauters, G., Delmée, M. (2003) Bacteremia due to a novel Microbacterium species in a patient with leukemia and description of Microbacterium paraoxydans sp. nov. J. Clin. Microbiol. 41(5), 2242–2246

    Article  PubMed Central  PubMed  Google Scholar 

  • Le Conte, Y., Ellis, M., Ritter, W. (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41(3), 353–363

    Article  Google Scholar 

  • Maniatis, T., Fritsch, E.F., Sambrook, J. (1982) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory. Cold Spring Harbor, New York

    Google Scholar 

  • Morais, P.V., da Costa, M.S. (1990) Alterations in the major heterotrophic bacterial populations isolated from a still bottled mineral water. J. Appl. Bacteriol. 69(5), 750–757

    Article  CAS  PubMed  Google Scholar 

  • Mounier, J., Rea, M.C., O’Connor, P.M., Fitzgerald, G.F., Cogan, T.M. (2007) Growth characteristics of Brevibacterium, Corynebacterium, Microbacterium, and Staphylococcus spp. isolated from surface-ripened cheese. Appl. Environ. Microbiol. 73(23), 7732–7739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nazzi, F., Brown, S.P., Annoscia, D., Piccolo, F.D., Prisco, G.D., Varricchio, P., Vedova, G.D., Cattonaro, F., Caprio, E., Pennacchio, F. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog . doi:10.1371/journal.ppat.1002735

    PubMed Central  PubMed  Google Scholar 

  • Oldroyd, B.P. (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends Ecol. Evol. 14(8), 312–315

    Article  PubMed  Google Scholar 

  • Pospiech, A., Neumann, B. (1995) A versatile quick-prep of genomic DNA from Gram-positive bacteria. Trends Genet. 11(6), 217–218

    Article  CAS  PubMed  Google Scholar 

  • Reddy, C.A., Beveridge, T.J., Breznak, J.A., Marzluf, G.A., Schmidt, T.M., Snyder, L.R. (2007) Methods for General and Molecular Microbiology. ASM Press, Washington DC. ISBN: 1555812236

    Google Scholar 

  • Ringø, E., Sperstad, S., Kraugerud, O.F., Krogdahl, Å. (2008) Use of 16S rRNA gene sequencing analysis to characterize culturable intestinal bacteria in Atlantic salmon (Salmo salar) fed diets with cellulose or non-starch polysaccharides from soy. Aquat. Res. 39(10), 1087–1100

    Article  Google Scholar 

  • Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2009) Biology and control of Varroa destructor. J. Invertebr. Pathol. 103(suppl. 1), 96–119

    Google Scholar 

  • Shang, S.T., Chiu, S.K., Chan, M.C., Wang, N.C., Yang, Y.S., Lin, J.C., Chang, F.Y. (2012) Invasive Brevundimonas vesicularis bacteremia: Two case reports and review of the literature. J. Microbiol. Immunol. Infect. 45(6), 468–472

    Article  PubMed  Google Scholar 

  • Shen, M.Q., Cui, L.W., Ostiguy, N., Cox-Foster, D. (2005) Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. J. Gen. Virol. 86(8), 2281–2289

    Article  CAS  PubMed  Google Scholar 

  • Shi, W., Syrenne, R., Sun, J.Z., Yuan, J.S. (2010) Molecular approaches to study the insect gut symbiotic microbiota at the ‘omics’ age. Insect Sci. 17(3), 199–219

    Article  CAS  Google Scholar 

  • Shivaji, S., Reddy, G.S., Aduri, R.P., Kutty, R., Ravenschlag, K. (2004) Bacterial diversity of a soil sample from Schirmacher Oasis. Antarctica. Cell Mol. Biol. 50(5), 525–536

    CAS  Google Scholar 

  • Shivaji, S., Chaturvedi, P., Suresh, K., Reddy, G.S.N., Dutt, C.B.S., Wainwright, M., Narlikar, J.V., Bhargava, P.M. (2006) Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int. J. Syst. Evol. Microbiol. 56(7), 1465–1473

    Article  CAS  PubMed  Google Scholar 

  • Snowdon, A.J., Cliver, D.O. (1996) Microorganisms in honey. Int. J. Food Microbiol. 31(1–3), 1–26

    Article  CAS  PubMed  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nie, M., Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28(10), 2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • van Belkum, A., Welker, M., Erhard, M., Chatellier, S. (2012) Biomedical mass spectrometry in today’s and tomorrow’s clinical microbiology laboratories. J. Clin. Microbiol. 50(5), 1513–1517

    Article  PubMed Central  PubMed  Google Scholar 

  • Vilanova, C., Marco, G., Domínguez-Escribà, L., Genovés, S., Sentandreu, V., Bataller, E., Ramón, D., Porcar, M. (2012) Bacteria from acidic to strongly alkaline insect midguts: potential sources of extreme cellulolytic enzymes. Biomass Bioenerg. 45, 288–294

    Article  CAS  Google Scholar 

  • Weisburg, W.G., Barns, S.M., Pelletier, D.A., Lane, D.J. (1991) 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173(2), 697–703

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang, M.L., Chen, I.H., Chen, T.C., Lin, W.R., Lin, C.Y., Lu, P.L. (2006) Case report: infective endocarditis caused by Brevundimonas vesicularis. BMC Infect. Dis. 6, 179

    Article  PubMed Central  PubMed  Google Scholar 

  • Young, J.M., Kuykendall, L.D., Martinez–Romero, E., Kerr, A., Sawada, H. (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int. J. Syst. Evol. Microbiol. 51(1), 89–103

    CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Slovak Grant Agency VEGA, grant no. VEGA 2/0016/12.

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Correspondence to Peter Pristas.

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Manuscript editor: Yves Le Conte

Bactéries hétérotrophes associées à Varroa destructor

Varroa destructor/ Acari/ Microbacterium/ microflore externe/ hétérotrophie

Die Assoziation heterotropher Bakterien mit der Milbe Varroa destructor

Varroa destructor/ Ekto-Mikroflora/ Microbacterium/ heterotrophe Bakterien

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Vanikova, S., Noskova, A., Pristas, P. et al. Heterotrophic bacteria associated with Varroa destructor mite. Apidologie 46, 369–379 (2015). https://doi.org/10.1007/s13592-014-0327-9

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