Use of suppression subtractive hybridization to identify genetic differences between differentially virulent genotypes of Paenibacillus larvae, the etiological agent of American Foulbrood of honeybees

Environmental Microbiology Reports

Volumn 1, Issue 4, 2009, Pages 240-250

  Fünfhaus, Anne ^a   Ashiralieva, Ainura ^a,b   Borriss, Rainer ^b   Genersch, Elke ^a  

^a Institute for Bee Research   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APIS MELLIFERA; ENTEROBACTERIACEAE; PAENIBACILLUS; PAENIBACILLUS LARVAE;

EID: 73749085328     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2009.00039.x     Document Type: Article

References (52)

1. Agron, P.G., Macht, M., Radnedge, L., Skowronski, E.W., Miller, W., and Andersen, G.L. (2002) Use of subtractive hybridization for comprehensive surveys of prokaryotic genome differences. FEMS Microbiol Lett 211: 175-182.
2. Akopyants, N.S., Fradkov, A., Diatchenko, L., Hill, J.E., Siebert, P.D., Lukyanov, S.A., et al. (1998) PCR-based subtractive hybridization and differences in gene content among strains of Helicobacter pylori. Proc Natl Acad Sci USA 95: 13108-13113.
3. Alippi, A.M., Reynaldi, F.J., Lopez, A.C., De Giusti, M.R., and Aguilar, O.M. (2004) Molecular epidemiology of Paenibacillus larvae larvae and incidence of American foulbrood in Argentinian honeys from Buenos Aires province. J Apic Res 43: 135-143.
4. Altschul, S.F., Gish, W., Miller, W., Meyers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Amoako, K.K., Goto, Y., Misawa, N., Xu, D.L., and Shinjo, T. (1998) The erythrocyte receptor for Fusobacterium necrophorum hemolysin: phosphatidylcholine as a possible candidate. FEMS Microbiol Lett 168: 65-70.
6. Antunez, K., Piccini, C., Castro-Sowinski, S., Rosado, A.S., Seldin, L., and Zunino, P. (2007) Phenotypic and genotypic characterization of Paenibacillus larvae isolates. Vet Microbiol 124: 178-183.
7. Ashiralieva, A., and Genersch, E. (2006) Reclassification, genotypes, and virulence of Paenibacillus larvae, the etiological agent of American foulbrood in honeybees-a review. Apidologie 37: 411-420.
8. Carpusca, I., Jank, T., and Aktories, K. (2006) Bacillus sphaericus mosquitocidal toxin (MTX) and pierisin: the enigmatic offspring from the family of ADP-ribosyltransferases. Mol Microbiol 62: 621-630.
9. Chantawannakul, P., and Dancer, B.N. (2001) American foulbrood in honey bees. Bee World 82: 168-180.
10. Dancer, B.N., and Chantawannakul, P. (1997) The proteases of American foulbrood scales. J Invertebr Pathol 70: 79-87.
11. Diatchenko, L., Lau, Y., Campbell, A., Chenchik, A., Moqadam, F., Hunag, B., et al. (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93: 6025-6030.
12. Duitman, E.H., Hamoen, L.W., Rembold, M., Venema, G., Seitz, H., Saenger, W., et al. (1999) The mycosubtilin synthetase of Bacillus subtilis ATCC6633: a multifunctional hybrid between a peptide synthetase, an amino transferase, and a fatty acid synthase. Proc Natl Acad Sci USA 96: 13294-13299.
13. Genersch, E., and Otten, C. (2003) The use of repetitive element PCR fingerprinting (rep-PCR) for genetic subtyping of German field isolates of Paenibacillus larvae subsp. larvae. Apidologie 34: 195-206.
14. Genersch, E., Ashiralieva, A., and Fries, I. (2005) Strain-and genotype-specific differences in virulence of Paenibacillus larvae subsp. larvae, the causative agent of American foulbrood disease in honey bees. Appl Environ Microbiol 71: 7551-7555.
15. Genersch, E., Forsgren, E., Pentikäinen, J., Ashiralieva, A., Rauch, S., Kilwinski, J., and Fries, I. (2006) Reclassification of Paenibacillus larvae subsp. pulvifaciens and Paenibacillus larvae subsp. larvae as Paenibacillus larvae without subspecies differentiation. Int J Syst Evol Microbiol 56: 501-511.
16. Grünewald, J., and Marahiel, M.A. (2006) Chemoenzymatic and template-directed synthesis of bioactive macrocyclic peptides. Microbiol Mol Biol Rev 70: 121-146.
17. Hacker, J., and Kaper, J.B. (2000) Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54: 641-679.
18. Hacker, J., Blum-Oehler, G., Muhldorfer, I., and Tschape, H. (1997) Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol Microbiol 23: 1089-1097.
19. Haydak, M.H. (1970) Honey bee nutrition. Annu Rev Entomol 15: 143-156.
20. Heyndrickx, M., Vandemeulebroecke, K., Hoste, B., Janssen, P., Kersters, K., de Vos, P., et al. (1996) Reclassification of Paenibacillus (formerly Bacillus) pulvifaciens (Nakamura 1984) Ash et al. 1994, a later 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 subsp. larvae and P. larvae subsp. pulvifaciens. Int J Syst Bacteriol 46: 270-279.
21. Janke, B., Dobrindt, U., Hacker, J., and Blum-Oehler, G. (2001) A subtractive hybridization analysis of genomic differences between the uropathogenic E. coli strain 536 and the E. coli K-12 strain MG1655. FEMS Microbiol Lett 199: 61-66.
22. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G., Los, T., Lykidis, A., et al. (2002) Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184: 2005-2018.
23. Katznelson, H. (1950) Bacillus pulvifaciens (n. sp.), an organism associated with powdery scale of honeybee larvae. J Bacteriol 59: 153-155.
24. Kilwinski, J., Peters, M., Ashiralieva, A., and Genersch, E. (2004) Proposal to reclassify Paenibacillus larvae subsp. pulvifaciens DSM 3615 (ATCC 49843) as Paenibacillus larvae subsp. larvae. Results of a comparative biochemical and genetic study. Vet Microbiol 104: 31-42.
25. Konz, D., Klens, A., Schörgendorfer, K., and Marahiel, M.A. (1997) The bacitracin biosynthesis operon of Bacillus licheniformis ATCC 10716: molecular characterization of three multi-modular peptide synthetases. Chem Biol 4: 927-937.
26. Loncaric, I., Derakhshifar, I., Oberlerchner, J.T., Köglberger, H., and Moosbeckhofer, R. (2009) Genetic diversity among isolates of Paenibacillus larvae from Austria. J Invertebr Pathol 100: 44-46.
27. Ma, Y., Patel, J., and Parry, R.J. (2000) A novel valanimycinresistance determinant (vlmF) from Streptomyces viridifaciens MG456-hF10. Microbiology 146: 345-352.
28. Marahiel, M.A., Stachelhaus, T., and Mootz, H.D. (1997) Modular peptide synthetases involved in nonribosomal peptide synthesis. Chem Rev 97: 2651-2673.
29. McCleskey, C.S., and Melampy, R.M. (1939) Bactericidal properties of royal jelly of the honeybee. J Econ Entomol 32: 581-587.
30. Ming, L.-J. (2003) Structure and function of metalloantibiotics. Med Res Rev, 23: 697-762.
31. Ming, L.-J., and Epperson, J.D. (2002) Metal binding and structure-activity relationship of the metalloantibiotic peptide bacitracin. J Inorg Biochem 91: 46-58.
32. Mohr, K.I., and Tebbe, C.C. (2006) Diversity and phylotype consistency of bacteria in the guts of three bee species (Apoidea) at an oilseed rape field. Environ Microbiol 8: 258-272.
33. Neuendorf, S., Hedtke, K., Tangen, G., and Genersch, E. (2004) Biochemical characterization of different genotypes of Paenibacillus larvae subsp. larvae, a honey bee bacterial pathogen. Microbiology 150: 2381-2390.
34. Ongena, M., and Jacques, P. (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16: 115-125.
35. Peters, M., Kilwinski, J., Beringhoff, A., Reckling, D., and Genersch, E. (2006) American foulbrood of the honey bee: occurrence and distribution of different genotypes of Paenibacillus larvae in the administrative district of Arnsberg (North Rhine-Westphalia). J Vet Med 100-104.
36. Qin, X., Evans, J.D., Aronstein, K.A., Murray, K.D., andWeinstock, G.M. (2006) Genome sequence of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 15: 715-718.
37. Rauch, S., Ashiralieva, A., Hedtke, K., and Genersch, E. (2009) Negative correlation between individual-insect-level virulence and colony-level virulence of Paenibacillus larvae, the etiological agent of American foulbrood of honeybees. Appl Environ Microbiol 75: 3344-3347.
38. Reckseidler, S.L., DeShazer, D., Sokol, P.A., and Woods, D.E. (2001) Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect Immun 69: 34-44.
39. Schirmer, J., Just, I., and Aktories, K. (2002) The ADPribosylating mosquitocidal toxin from Bacillus sphaericus-proteolytic activiation, enzyme activity, and cytotoxic effects. J Biol Chem 277: 11941-11948.
40. Shapiro-Ilan, D.I., Fuxa, J.R., Lacey, L.A., Onstad, D.W., and Kaya, H.K. (2005) Definitions of pathogenicity and virulence in invertebrate pathology. J Invertebr Pathol 88: 1-7.
41. Thanabalu, T., Hindley, J., Jackson-Yap, J., and Berry, C. (1991) Cloning, sequencing, and expression of a gene encoding a 100-kilodalton mosquitocidal toxin from Bacillus sphaericus SSII-1. J Bacteriol 173: 2776-2785.
42. Thanabalu, T., Hindley, J., and Berry, C. (1992) Proteolytic processing of the mosquitocidal toxin from Bacillus sphaericus SSII-1. J Bacteriol 174: 5051-5056.
43. Thomas, S.R., and Elkinton, J.S. (2004) Pathogenicity and virulence. J Invertebr Pathol 85: 146-151.
44. Tsuge, K., Akiyama, T., and Shoda, M. (2000) Cloning, sequencing, and characterization of the iturin a operon. J Bacteriol 183: 6265-6273.
45. Versalovic, J., Schneider, M., de Bruijn, F.J., and Lupski, J.R. (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol Cell Biol 5: 25-40.
46. Willey, J.M., and van der Donk, W.A. (2007) Lantibiotics: peptides of diverse structure and function. Annu Rev Microbiol 61: 477-501.
47. Winstanley, C. (2002) Spot the difference: applications of subtractive hybridization to the study of bacterial pathogens. J Med Microbiol 51: 459-467.
48. Woodrow, A.W. (1942) Susceptibility of honeybee larvae to individual inoculations with spores of Bacillus larvae. J Econ Entomol 35: 892-895.
49. Woodrow, A.W., and Holst, E.C. (1942) The mechanism of colony resistance to American foulbrood. J Econ Entomol 35: 327-330.
50. Yue, D., Nordhoff, M., Wieler, L.H., and Genersch, E. (2008) 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). Environ Microbiol 10: 1612-1620.
51. Zander, E. (1951) Die Brutkrankheiten und ihre Bekämpfung. In Handbuch der Bienenkunde. Zander, E. (ed.). Stuttgart: Eugen Ulmer Stuttgart, p. 21.
52. Zhang, Y.L., Ong, C.T., and Leung, K.Y. (2000) Molecular analysis of genetic differences between virulent and avirulent strains of Aeromonas hydrophila isolated from diseased fish. Microbiology 146: 999-1009.