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Intestinal enterobacteria of the hibernating Apis mellifera mellifera L. bees

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Dynamics of enterobacteria of normal intestinal microflora was studied in Apis mellifera mellifera L. bees hibernating under snow in the Western Urals. The cell numbers (N) of the predominant species Klebsiella oxytoca increased from 10-106 CFU/bee in November 2004 to 104-107 CFU/bee in March 2005; its frequency of occurrence (P) increased from 92 to 100%. Increase of Providencia rettgeri (11.2004: N up to 106, P 25%; 03.2005: N 102-106, P 80%) was accompanied by the substitution of Morganella morganii (11.2004: N up to 106, P 25%) with Proteus vulgaris (03.2005: N up to 105, P 8%). By spring, Hafnia alvei and Citrobacter sp., which are pathogenic to bees, disappeared (11.2004: N up to 105, P 13 and 10%, respectively). Endophytic species Pantoea agglomerans, Leclecria sp., and other representatives of the “Enterobacter agglomerans” group were present in November and after the first emergence in spring (N up to 105; November: P 15%; April: P 23%). In April, the number of enterobacteria decreased to 105, and P. rettgeri became the predominant species (P 54%) instead of K. oxytoca (P 43%).

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References

  1. White, G.F., The Bacteria of the Apiary: with Special Reference To Bee Diseases, Washington, DC: G.P.O., 1906.

    Google Scholar 

  2. Grobov, O.F. and Likhotin, A.K., Bolezni i vrediteli pchel (Diseases and Vermin of Bees), Moscow: Mir, 2003.

    Google Scholar 

  3. Khismatullin, R.G., Kuzyaev, R.Z., Lyapunov, Ya.E., Legotkina, G.I., Zakharova, T.V., and Avdeev, N.V., Standardization and Pollen Quality, Pchelovodstvo, 2004, no. 7, pp. 48–49.

  4. Tysset, C. and Durand, C., Contribution a l’etude du microbisme intestinal des abeilles butineuses saines (Apis mellifera L.). Denombrement et etude des groupements constitutifs (Premier memoire), Bulletin apicole de documentation scientifique et technique et information, 1968, vol. 11, no. 2, pp. 107–118.

    Google Scholar 

  5. Egorova, A.I., Microflora of Healthy Honey Bees (Apis mellifera L.) and of those Affected with European Foul Brood, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Dushanbe, 1968.

  6. Gilliam, M., Lorenz, B.J., and Richardson, G.V., Digestive Enzymes and Micro-Organisms in Honey Bees (Apis Melifera L.) Influence of Streptomycin, Age, Season and Pollen, Microbios, 1988, vol. 55, pp. 95–114.

    CAS  Google Scholar 

  7. Jeyaprakash, A., Hoy, M.A., and Allsopp, M.H., Bacterial Diversity in Worker Adults of Apis mellifera capensis and Apis mellifera scutellata (Insecta: Hymenoptera) Assessed Using 16S rRNA Sequences, J. Invertebr. Pathol., 2003, vol. 84, no. 2, pp. 96–103.

    Article  PubMed  CAS  Google Scholar 

  8. Kačániova M., Chlebo R., Kopernický M., Tracovická A., Microflora of the Honeybee Gastrointestinal Tract, Folia Microbiol., 2004, vol. 49, no. 2, pp. 169–171.w

    Article  Google Scholar 

  9. Enterobakterii. Rukovodstvo dlya vrachei (Enterobacteria. Manual for Physicians), Pokrovskii, V.I., Ed., Moscow: Meditsina, 1985.

    Google Scholar 

  10. Bergey’s Manual of Systematic Bacteriology, 8th ed., vol. 1–2, Holt, J.G., Ed, Baltimore-London: Williams and Wilkins, 1986. [Russ. Transl.: Opredelitel’bakterii Berdzhi, Moscow: Mir, 1997].

    Google Scholar 

  11. Hansen, D.S., Aucken, H.M., Abiola, T., and Podschun, R., Recommended Test Panel for Differentiation of Klebsiella Species on the Basis of a Trilateral Interlaboratory Evaluation of 18 Biochemical Tests, J. Clin. Microbiol., 2004, Aug., pp 3665–3669.

  12. Brenner, D.J., O’Hara, C.M., Grimont, P.A.D., Janda, J.M., Falsen, E., Aldova, E., Ageron, E., Schindler, J., Abbott, S.L., and Steigerwalt, A.G., Biochemical Identification of Citrobacter Species Defined by DNA Hybridization and Description of Citrobacter gillenii sp. nov (Formerly Citrobacter Genomospecies 10) and Citrobacter murliniae sp. nov. (Formerly Citrobacter Genomospecies 11), J. Clin. Microbiol., 1999, vol. 37, no. 8, pp. 2619–2624.

    PubMed  CAS  Google Scholar 

  13. Tarnueva, E.Yu., Guzeva, L.F., Grobov, O.F., Fomin, B.A., and Batuev, Yu.M., Citrobacter sp., an Agent of Bee Diseases, Veterinariya, 1994, no. 1, pp. 35–37.

  14. Vassart, M., Thevenon, J., and Cotto, F., Etude sanitaire du rucher Neo-caledonien, Bull. Tech. Apic., 1988, vol. 15, no. 4, pp. 195–202.

    Google Scholar 

  15. Gilliam, M. and Morton, N., Enterobacteriaceae Isolated from Honey Bees Treated with 2,4-D and Antibiotics, J. Invertebr. Path, 1974, vol. 23, pp. 42–45.

    Article  Google Scholar 

  16. García, D.G., Mogollón, M.A.R., and Nieves, J.S., Cultured Microbiological Content of the Intestinal Tract and Stored Pollen of Apis mellifera (Hymenoptera: Apidae), Acta Biologica Colombiana, 2006, vol. 11, no. 1, pp. 123–129.

    Google Scholar 

  17. Tysset, C. and Rousseau, M., Des germes phytopatogenes du genre Erwinia commensaux du tractus intestinal de l’abeille adulte (Apis melifeca L.), Bull. Tech. Apic, 1967, no. 2, pp. 175–194.

  18. Fritzsch, W. and Bremer, R., Bienengesundheitsdienst, Jena: VHB Gustav Fisher, 1975.

    Google Scholar 

  19. Toumanoff, C., Flore bacterienne intestinale de l’abeille adulte, Les Maladies Des Abeilles, La Revue Francaise d’apiculture, 1951, no. 68-numero special, pp. 145–151.

  20. Derkach, V.S. and Pereshivailo, S.I., Bee Paratyphoid, Veterinarne Dilo, 1926, no. 7–8, pp. 7–11.

  21. Salimov, R.M., Distribution and Role of Some Enterobacteriaceae in Bee Pathology, Doctoral (Veterinary) Dissertation, Moscow, 1994.

  22. Grimont, F. and Grimont, P.A.D., The Genus Enterobacter, in The Prokaryotes. 2nd ed., Balows, A., Truper, H.G., Dworkin, M., Harder, W., and Schleifer, K.H., Eds., New York: Springer, 1991, pp. 2797–2815.

    Google Scholar 

  23. Inoue, K., Sugiyama, K., Kosako, Y., Sakazaki, R., and Yamai, S., Enterobacter cowanii sp. nov., a New Species of the Family Enterobacteriaceae, Curr. Microbiol., 2000, vol. 41, pp. 417–420.

    Article  PubMed  CAS  Google Scholar 

  24. Araújo, W.L., Maccheroni, W.Jr., Aguilar-Vildoso, C.I., Barroso, P.A.V., Saridakis, H.O., and Azevedo, J.L., Variability and Interactions Between Endophytic Bacteria and Fungi Isolated from Leaf Tissues of Citrus Rootstocks, Can. J. Microbiol., 2001, vol. 47, pp. 229–236.

    Article  PubMed  Google Scholar 

  25. Spiewak, R., Skorska, C., Prazmo, Z., and Dutkievicz, J., Pollen As a Potential Factor Aggravating Pollinosis, Ann. Agric. Environ. Med, 1996, no. 3, pp. 57–59.

  26. Benhizia, Y., Benhizia, H., Benguedouar, A., Muresu, R., Giacomini, A., and Squartini, A., Gamma Proteobacteria Can Nodulate Legumes of the Genus Hedysarum, Syst. Appl. Microbiol., 2004, vol. 27, no. 4, pp. 462–468.

    Article  PubMed  CAS  Google Scholar 

  27. Khismatullin, R.G., Lyapunov, Y.E., and Kuzyaev, R.Z., Enterobacteria of Commercial Honeybee Collected Pollen, Abstr. 39th Apimondia Intern. Apicultural Congress, Dublin, Ireland, August 21–26, 2005, p. 130.

  28. Smolka-Shimchevskaya, B., Effect of Some Therapeutic Chemical Compounds on Bee Intestinal Flora, Apiakta, 1989, vol. 24, pp. 70–77.

    Google Scholar 

  29. Grimont, P.A.D. and Lysenko, O., Species and Biotipe Identification of Serratia Strains Associated with Insects, Curr. Microbiol., 1979, vol. 2, pp. 139–142.

    Article  Google Scholar 

  30. Schwartzbrod, J., Definition of Coliforms, COST 624 “Optimal Management of Wastewater Systems” Working Group no. 5 “Treatment Scenarios. Rep. 7th Working Group Meeting, May 2–3, 2002, Nancy, France, http://www.ensic.inpl-nancy.fr/COSTWWTP/Work_Group/Wg5/Nancy_report_2002.pdf

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Correspondence to Ya. E. Lyapunov.

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Original Russian Text © Ya.E. Lyapunov, R.Z. Kuzyaev, R.G. Khismatullin, O.A. Bezgodova, 2008, published in Mikrobiologiya, 2008, Vol. 77, No. 3, pp. 421–428.

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Lyapunov, Y.E., Kuzyaev, R.Z., Khismatullin, R.G. et al. Intestinal enterobacteria of the hibernating Apis mellifera mellifera L. bees. Microbiology 77, 373–379 (2008). https://doi.org/10.1134/S0026261708030181

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