Inhibitory effect of gut bacteria from the Japanese honey bee, Apis cerana japonica, against Melissococcus plutonius, the causal agent of European foulbrood disease

Journal of Insect Science

Volumn 14, Issue , 2014, Pages

  Wu, Meihua ^a,c   Sugimura, Yuya ^a   Iwata, Kyoko ^a   Takaya, Noriko ^a   Takamatsu, Daisuke ^b,d   Kobayashi, Masaru ^b   Taylor, Demar ^c   Kimura, Kiyoshi ^a,c   Yoshiyama, Mikio ^a  

^a NATIONAL INSTITUTE OF LIVESTOCK AND GRASSLAND SCIENCE   (Japan)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

^d GIFU UNIVERSITY   (Japan)

Author keywords

honey bee disease; Microbial flora; probiotic

Indexed keywords

BACTERIAL DNA; BACTERIAL RNA; PROBIOTIC AGENT; RNA 16S;

ANIMAL; BACILLUS; BACTERIUM; BEE; BIOLOGICAL PEST CONTROL; ENTEROCOCCACEAE; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; JAPAN; LARVA; MICROBIOLOGY; PHYLOGENY; PHYSIOLOGY;

ANIMALS; BACILLUS; BACTERIA; BEES; DNA, BACTERIAL; ENTEROCOCCACEAE; JAPAN; LARVA; PEST CONTROL, BIOLOGICAL; PHYLOGENY; PROBIOTICS; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

EID: 84908686509     PISSN: None     EISSN: 15362442     Source Type: Journal    
DOI: 10.1673/031.014.129     Document Type: Article

References (47)

1. Alippi, A. M, and F. J. Reynaldi. 2006. Inhibition of the growth of Paenibacillus larvae, the causal agent of American foulbrood of honey bees, by selected strains of aerobic spore-forming bacteria isolated from apiarian sources. Journal of Invertebrate Pathology 91: 141-146.
2. Arai, R., K. Tominaga, M. Wu, M. Okura, K. Ito, N. Okamura, H. Onishi, M. Osaki, Y. Sugimura, M. Yoshiyama, and D. Takamatsu. 2012. Diversity of Melissococcus plutonius from honey bee larvae in Japan and experimental reproduction of European foulbrood with cultured atypical isolates. PLoS One 7: e33708.
3. Audisio, M. C., M. J. Torres, D. C. Sabaté, C. Ibarguren, and M. C. Apella. 2011. Properties of different lactic acid bacteria isolated from Apis mellifera L. bee-gut. Microbiological Research 166: 1-13.
4. Aupinel, P., D. Fortini, H. Dufour, J. N. Tasei, B. Michaud, J. F. Odoux, M. H. Pham-delegue. 2005. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bulletin of Insectology 58: 107-111.
5. Bailey, L. 1983. Melissococcus pluton, the cause of European foulbrood of honey bees (Apis spp.). Journal of Applied Microbiology 55: 65-69.
6. Bailey, L., and M. D. Collins. 1982. Reclassification of Streptococcus pluton (White) in a new genus Melissococcus, as Melissococcus pluton nom. rev.; comb. nov. Journal of Applied Microbiology 53: 215-217.
7. Belloy, L., A. Imdorf, I. Fries, E. Forsgren, H. Berthoud, R. Kuhn, and J. D. Charrière. 2007. Spatial distribution of Melissococcus plutonius in adult honey bees collected from apiaries and colonies with and without symptoms of European foulbrood. Apidologie 38: 136-140.
8. Chen, Y. W., C. H. Wang, J. An, and K. K. Ho. 2000. Susceptibility of the Asian honey bee, Apis cerana, to American foulbrood, Paenibacillus larvae larvae. Journal of Apicultural Research 39: 169-175.
9. de Graaf, D. C, A. M. Alippi, M. Brown, J. D. Evans, M. Feldlaufer, A. Gregorc, M. Hornitzky, S. F. Pernal, D. M. Schuch, D. Titera, V. Tomkies, W. Ritter. 2006. Diagnosis of American foulbrood in honey bees: a synthesis and proposed analytical protocols. Letters in Applied Microbiology 43: 583-590.
10. Disayathanoowat, T., M. Yoshiyama, K. Kimura, and P. Chantawannakul. 2012. Isolation and characterization of bacteria from the midgut of the Asian honey bee (Apis cerana indica). Journal of Apicultural Research 51: 312-319.
11. Evans, J. D., and T. N. Armstrong. 2005. Inhibition of the American foulbroodbacterium, Paenibacillus larvae larvae, by bacteria isolated from honey bees. Journal of Apicultural Research 44: 168-171.
12. Evans, J. D., and T. N. Armstrong. 2006. Antagonistic interactions between honey bee bacterial symbionts and implications for disease. BMC Ecology 6: 4.
13. Evans, J. D, and D. L. Lopez. 2004. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). Journal of Economic Entomology 97: 752-756.
14. Forsgren, E. 2010. European foulbrood in honey bees. Journal of Invertebrate Pathology 103: S5-S9.
15. Forsgren, E., A. C. Lundhagen, A. Imdorf, and I. Fries. 2005. Distribution of Melissococcus plutonius in honey bee colonies with and without symptoms of European foulbrood. Microbial Ecology 50: 369-374.
16. Forsgren, E., T. C. Olofsson, A. Vasquez, and I. Fries. 2009. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41: 99-108.
17. Genersch, E. 2010. Honey bee pathology: current threats to honey bees and beekeeping. Applied Microbiology and Biotechnology 87: 87-97.
18. Gilliam, M. 1979. Microbiology of pollen and bee bread: the genus Bacillus. Apidologie 10: 269-274.
19. Gilliam, M. 1985. Microbes from apiarian sources: Bacillus spp. in frass of the greater wax moth. Journal of Invertebrate Pathology 45: 218-224.
20. Gilliam, M. 1997. Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters 155: 1-10.
21. Gilliam, M., and H. L. Morton. 1978. Bacteria belonging to the genus Bacillus isolated from honey bees, Apis mellifera, fed 2,4-D and antibiotics. Apidologie 9: 213-222.
22. Gilliam, M., and D. K. Valentine. 1976. Bacteria isolated from the intestinal contents of foraging worker honey bees, Apis mellifera: the genus Bacillus. Journal of Invertebrate Pathology 28: 275-276.
23. Gilliam, M., S. L. Buchmann, and B. J. Lorenz. 1984. Microbial flora of the larval provisions of the solitary bees, Centris pallida and Anthophora sp. Apidologie 15: 1-10.
24. Guo, X., D. Li, W. Lu, X. Piao, and X. Chen. 2006. Screening of Bacillus strains as potential probiotics and subsequent confirmation of the in vivo effectiveness of Bacillus subtilis MA139 in pigs. Antonie van Leeuwenhoek 90: 139-146.
25. Hong, H. A., L. H. Duc, and S. M. Cutting. 2005. The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews 29: 813-835.
26. Klein, A. M., B. E. Vaissiere, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham, C. Kremen, and T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274: 303-313.
27. Martinson, V. G., B. N. Danforth, R. L. Minckley, O. Rueppell, S. Tingek, and N. A. Moran. 2011. A simple and distinctivemicrobiota associated with honey bees and bumble bees. Molecular Ecology 20: 619-628.
28. Martinson, V. G., J. Moy, and N. A. Moran. 2012. Establishment of characteristic gut bacteria during development of the honey bee worker. Applied and Environmental Microbiology 78: 2830-2840.
29. Mckee, B. A., R. D. Goodman, and M. A. Hornitzky. 2004. The transmission of European foulbrood (Melissococcus plutonius) to artificially reared honey bee larvae (Apis mellifera). Journal of Apicultural Research 43: 93-100.
30. Miyagi, T., C.Y.S. Peng, R. Y. Chuang, E. C. Mussen, M. S. Spivak, and R. H. Doi. 2000. Verification of oxytetracycline-resistant American foulbrood pathogen Paenibacillus larvae in the United States. Journal of Invertebrate Pathology 75: 95-96.
31. Mohr, K. I., and C. C. Tebbe. 2006. Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environmental Microbiology 8: 258-272.
32. Moran, N. A., A. K. Hansen, J. E. Powell, and Z. L. Sabree. 2012. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 7: e36393.
33. Morse, R. A., and N. W. Calderone. 2000. The value of honey bees as pollinators of U.S. crops in 2000. Bee Culture 128: 1-15.
34. Mutinelli, F. 2003. European legislation governing the authorisation of veterinary medical products with particular reference to the use of drugs for the control of honey bee diseases. Apiacta 38: 156-168.
35. Pətruicə, S., and D. Mot. 2012. The effect of using prebiotic and probiotic products on intestinal micro-flora of the honey bee (Apis mellifera carpatica). Bulletin of Entomological Research 30: 1-5.
36. Peng, Y., Y. Fang, S. Xu, and L. Ge. 1987. The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. Journal of Invertebrate Pathology 49: 54-60.
37. Pettis, J. S., J. Kochansky, and M. F. Feldlaufer. 2004. Larval Apis mellifera L. (Hymenoptera: Apidae) mortality after topical application of antibiotics and dusts. Journal of Economic Entomology 97: 171-176.
38. Porrini, M. P., M. C. Audisio, D. C. Sabaté, C. Ibarguren, S. K. Medici, E. G. Sarlo, P. M. Garrido, and M. J. Eguaras. 2010. Effect of bacterial metabolites on microsporidian Nosema ceranae and on its host Apis mellifera. Journal of Parasitology Research 107: 381-388.
39. Reynaldi, F. J., M. R. De Giusti, and A. M. Alippi. 2004. Inhibition of the growth of Ascosphaera apis by Bacillus and Paenibacillus strains isolated from honey. Revista Argentina de Microbiología 36: 52-55.
40. Sabaté, D. C., L. Carrillo, and M. C. Audisio. 2009. Inhibition of Paenibacillus larvae and Ascosphaera apis by Bacillus subtilis isolated from honey bee gut and honey samples. Research in Microbiology 160: 193-199.
41. Sabaté, D. C., M. S. Cruz, M. R. Benitez-Ahrendts, and M. C. Audisio. 2012. Beneficial effects of Bacillus subtilis subsp. subtilis Mori2, a honey-associated strain, on honey bee colony performance. Probiotics and Antimicrobial Proteins 4: 39-46.
42. Thompson, H. M., and M. A. Brown. 2001. Is contact colony treatment with antibiotics an effective control for European foulbrood? Bee World 82: 130-138.
43. Thompson, H. M., R. J. Waite, S. Wilkins, M. A. Brown, T. Bigwood, M. Shaw, C. Ridgway, and M. Sharman. 2005. Effects of European foulbrood treatment regime on oxytetracycline levels in honey extracted from treated honey bee (Apis mellifera) colonies and toxicity to brood. Food Additives and Contaminants 22: 573-578.
44. Van Engelsdorp, D., and M. D. Meixner. 2010. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103: S80-S95.
45. Vasquez, A., E. Forsgren, I. Fries, R. J. Paxton, E. Flaberg, L. Szekely, and T. C. Olofsson. 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honey bees. PLoS One 7: e33188.
46. Weisburg, W. G., S. M. Barns, D. A. Pelletier, and D. J. Lane. 1991. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173: 697-703.
47. Yoshiyama, M., and K. Kimura. 2009. Bacteria in the gut of Japanese honey bee, Apis cerana japonica, and their antagonistic effect against Paenibacillus larvae, the causal agent of American foulbrood. Journal of Invertebrate Pathology 102: 91-96.