Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2013, Article ID 479893, 9 pages
http://dx.doi.org/10.1155/2013/479893
Research Article

Genetic and Biochemical Diversity of Paenibacillus larvae Isolated from Tunisian Infected Honey Bee Broods

1Laboratory of Microorganisms and Active Biomolecules, Faculty of Sciences of Tunis, University of Tunis El Manar, 2092 Tunis, Tunisia
2LR Biotechnology and Bio-Geo Resources Valorization, Higher Institute for Biotechnology, Biotechpole Sidi Thabet, University of Manouba, 2020 Ariana, Tunisia
3Department of Food Environmental and Nutritional Sciences (DeFENS), University of Milan, 20133 Milan, Italy
4Laboratoire de Zoologie et Apicultures, Institut National Agronomique de Tunis, 43 avenue Charles Nicolle, 1082 Tunis-Mahrajène, Tunisia
5Dipartimento di Scienze Agrarie, Forestali e Alimentari, University of Turin, I-10095 Grugliasco, Italy

Received 30 April 2013; Accepted 27 July 2013

Academic Editor: George Tsiamis

Copyright © 2013 Chadlia Hamdi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. Genersch, E. Forsgren, J. Pentikäinen et al., “Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation,” International Journal of Systematic and Evolutionary Microbiology, vol. 56, no. 3, pp. 501–511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Alippi, A. C. López, F. J. Reynaldi, D. H. Grasso, and O. M. Aguilar, “Evidence for plasmid-mediated tetracycline resistance in Paenibacillus larvae, the causal agent of American Foulbrood (AFB) disease in honeybees,” Veterinary Microbiology, vol. 125, no. 3-4, pp. 290–303, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Alippi, G. N. Albo, F. J. Reynaldi, and M. R. De Giusti, “In vitro and in vivo susceptibility of the honeybee bacterial pathogen Paenibacillus larvae subs P. larvae to the antibiotic tylosin,” Veterinary Microbiology, vol. 109, no. 1-2, pp. 47–55, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Heyndrickx, K. Vandemeulebroecke, B. Hoste et al., “Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later subjective synonym of Paenibacillus (formerly Bacillus) larvae (White 1906) Ash et al. 1994, as a subspecies of P. larvae, with emended descriptions of P. larvae as P. larvae subs P. larvae and P. larvae subsp. pulvifaciens,” International Journal of Systematic Bacteriology, vol. 46, no. 1, pp. 270–279, 1996. View at Google Scholar · View at Scopus
  5. W. Dobbelaere, D. C. De Graaf, W. Reybroeck, E. Desmedt, J. E. Peeters, and F. J. Jacobs, “Disinfection of wooden structures contaminated with Paenibacillus larvae subs P. larvae spores,” Journal of Applied Microbiology, vol. 91, no. 2, pp. 212–216, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Antúnez, B. D'Alessandro, C. Piccini, E. Corbella, and P. Zunino, “Paenibacillus larvae larvae spores in honey samples from Uruguay: a nationwide survey,” Journal of Invertebrate Pathology, vol. 86, no. 1-2, pp. 56–58, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Kilwinski, M. Peters, A. Ashiralieva, and E. Genersch, “Proposal to reclassify Paenibacillus larvae subsp. pulvifaciens DSM 3615 (ATCC 49843) as Paenibacillus larvae subs P. larvae. Results of a comparative biochemical and genetic study,” Veterinary Microbiology, vol. 104, no. 1-2, pp. 31–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Hamdi, A. Balloi, J. Essanaa et al., “Gut microbiome dysbiosis and honeybee health,” Journal of Applied Entomology, vol. 135, no. 7, pp. 524–533, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Crotti, A. Balloi, C. Hamdi et al., “Microbial symbionts: a resource for the management of insect-related problems,” Microbial Biotechnology, vol. 5, no. 3, pp. 307–317, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. D. C. De Graaf, P. De Vos, M. Heyndrickx, S. Van Trappen, N. Peiren, and F. J. Jacobs, “Identification of Paenibacillus larvae to the subspecies level: an obstacle for AFB diagnosis,” Journal of Invertebrate Pathology, vol. 91, no. 2, pp. 115–123, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. T. S. Thompson, S. F. Pernal, D. K. Noot, A. P. Melathopoulos, and J. P. van den Heever, “Degradation of incurred tylosin to desmycosin-Implications for residue analysis of honey,” Analytica Chimica Acta, vol. 586, no. 1-2, pp. 304–311, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. A. M. Alippi and O. M. Aguilar, “Characterization of isolates of Paenibacillus larvae subsp. larvae from diverse geographical origin by the polymerase chain reaction and BOX primers,” Journal of Invertebrate Pathology, vol. 72, no. 1, pp. 21–27, 1998. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Genersch and C. Otten, “The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subs P. larvae,” Apidologie, vol. 34, no. 3, pp. 195–206, 2003. View at Google Scholar · View at Scopus
  14. S. Neuendorf, K. Hedtke, G. Tangen, and E. Genersch, “Biochemical characterization of different genotypes of Paenibacillus larvae subs P. larvae, a honey bee bacterial pathogen,” Microbiology, vol. 150, no. 7, pp. 2381–2390, 2004. View at Google Scholar · View at Scopus
  15. I. Loncaric, I. Derakhshifar, J. T. Oberlerchner, H. Köglberger, and R. Moosbeckhofer, “Genetic diversity among isolates of Paenibacillus larvae from Austria,” Journal of Invertebrate Pathology, vol. 100, no. 1, pp. 44–46, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. J. D. Evans, “Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae,” Journal of Invertebrate Pathology, vol. 85, no. 2, pp. 105–111, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. P. H. De Rycke, J. J. Joubert, S. H. Hosseinian, and F. J. Jacobs, “The possible role of Varroa destructor in the spreading of American foulbrood among apiaries,” Experimental and Applied Acarology, vol. 27, no. 4, pp. 313–318, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. M. O. Schäfer, W. Ritter, J. Pettis, and P. Neumann, “Small hive beetles, Aethina tumida, are vectors of Paenibacillus larvae,” Apidologie, vol. 41, no. 1, pp. 14–20, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. E. W. Davidson, “Ultrastructure of American foulbrood disease pathogenesis in larvae of the worker honey bee, Apis mellifera,” Journal of Invertebrate Pathology, vol. 21, no. 1, pp. 53–61, 1973. View at Google Scholar · View at Scopus
  20. D. Yue, M. Nordhoff, L. H. Wieler, and E. Genersch, “Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera),” Environmental Microbiology, vol. 10, no. 6, pp. 1612–1620, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. B. N. Dancer and P. Chantawannakul, “The proteases of American Foulbrood scales,” Journal of Invertebrate Pathology, vol. 70, no. 2, pp. 79–87, 1997. View at Google Scholar · View at Scopus
  22. K. Antúnez, M. Anido, D. Arredondo, J. D. Evans, and P. Zunino, “Paenibacillus larvae enolase as a virulence factor in honeybee larvae infection,” Veterinary Microbiology, vol. 147, no. 1-2, pp. 83–89, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. L. Poppinga, B. Janesch, A. Funfhaus et al., “Identification and functional analysis of the S-layer protein SplA of Paenibacillus larvae, the causative agent of American Foulbrood of honey bees,” PLOS Pathogens, vol. 8, no. 5, Article ID e1002716, 2012. View at Publisher · View at Google Scholar
  24. E. Genersch, A. Ashiralieva, and I. Fries, “Strain- and genotype-specific differences in virulence of Paenibacillus larvae subs P. larvae, a bacterial pathogen causing American foulbrood disease in honeybees,” Applied and Environmental Microbiology, vol. 71, no. 11, pp. 7551–7555, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. H. Hussein, “A review of beekeeping in Arab countries,” Bee World, vol. 81, no. 2, pp. 56–71, 2000. View at Google Scholar · View at Scopus
  26. N. Gallai, J.-M. Salles, J. Settele, and B. E. Vaissière, “Economic valuation of the vulnerability of world agriculture confronted with pollinator decline,” Ecological Economics, vol. 68, no. 3, pp. 810–821, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. R. E. Gordon, W. C. Haynes, and C. H. N. Pang, The Genus Bacillus, Handbook No. 427, United States Department of Agriculture, Washington, DC, USA, 1973.
  28. P. H. A. Sneath and R. R. Sokal, Numerical Taxonomy: The Principles and Practice of Numerical Classification, Freeman WH and Co., San Francisco, Calif, USA, 1973.
  29. A. Cherif, S. Borin, A. Rizzi, H. Ouzari, A. Boudabous, and D. Daffonchio, “Characterization of a repetitive element polymorphism-polymerase chain reaction chromosomal marker that discriminates Bacillus anthracis from related species,” Journal of Applied Microbiology, vol. 93, no. 3, pp. 456–462, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. B. Chouaia, P. Rossi, M. Montagna et al., “Molecular evidence for multiple infections as revealed by typing of asaia bacterial symbionts of four mosquito species,” Applied and Environmental Microbiology, vol. 76, no. 22, pp. 7444–7450, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Velezmoro, E. Ramos, C. García, and D. Zúñiga, “Genotypic identification of Bacillus sp. isolated from canned white asparagus (Asparagus officinalis) during the production/processing chain in northern Peru,” Annals of Microbiology, vol. 62, no. 3, pp. 1207–1217, 2012. View at Google Scholar
  32. W. L. Kovach, MVSP-A Multivariate Statistical Package for Windows, ver. 3.1. Kovach, Computing Services, Pentraeth, Wales, UK, 1998.
  33. S. F. Altschul, W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, “Basic local alignment search tool,” Journal of Molecular Biology, vol. 215, no. 3, pp. 403–410, 1990. View at Publisher · View at Google Scholar · View at Scopus
  34. J. D. Thompson, D. G. Higgins, and T. J. Gibson, “CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice,” Nucleic Acids Research, vol. 22, no. 22, pp. 4673–4680, 1994. View at Google Scholar · View at Scopus
  35. T. H. Jukes and C. R. Cantor, “Evolution of protein molecules,” in Mammalian Protein Metabolism, N. Munro, Ed., pp. 21–132, Academic Press, New York, NY, USA, 1969. View at Google Scholar
  36. N. Saitou and M. Nei, “The neighbor-joining method: a new method for reconstructing phylogenetic trees,” Molecular Biology and Evolution, vol. 4, no. 4, pp. 406–425, 1987. View at Google Scholar · View at Scopus
  37. K. Tamura, J. Dudley, M. Nei, and S. Kumar, “MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0,” Molecular Biology and Evolution, vol. 24, no. 8, pp. 1596–1599, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. B. Ettoumi, N. Raddadispi, S. Borin, D. Daffonchio, A. Boudabous, and A. Cherif, “Diversity and phylogeny of culturable spore-forming Bacilli isolated from marine sediments,” Journal of Basic Microbiology, vol. 49, no. 1, pp. S13–S23, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Forsgren, T. C. Olofsson, A. Vásquez, and I. Fries, “Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae,” Apidologie, vol. 41, no. 1, pp. 99–108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. Y.-S. C. Peng, E. Mussen, A. Fong, M. A. Montague, and T. Tyler, “Effects of chlortetracycline of honey bee worker larvae reared in vitro,” Journal of Invertebrate Pathology, vol. 60, no. 2, pp. 127–133, 1992. View at Publisher · View at Google Scholar · View at Scopus
  41. P. Aupinel, D. Fortini, H. Dufour et al., “Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae,” Bulletin of Insectology, vol. 58, no. 2, pp. 107–111, 2005. View at Google Scholar · View at Scopus
  42. N. Millar, “Biology statistics made simple using excel,” School Science Review, vol. 83, no. 303, pp. 23–24, 2001. View at Google Scholar
  43. S. Rauch, A. Ashiralieva, K. Hedtke, and E. Genersch, “Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of american foulbrood of honeybees,” Applied and Environmental Microbiology, vol. 75, no. 10, pp. 3344–3347, 2009. View at Publisher · View at Google Scholar · View at Scopus