Genetic diversity among strains of avian, bovine, ovine and porcine origin from England and Wales by comparative sequence analysis of the 16S rRNA gene Free

Abstract

Genetic diversity among 86 isolates was investigated by comparative sequence analysis of a 1468 bp fragment of the 16S rRNA gene. The strains included 79 field isolates recovered from birds (poultry) (22), cattle (21), pigs (26) and sheep (10) within England and Wales, four Asian isolates associated with bovine haemorrhagic septicaemia, and the type strains of the three subspecies of . Dulcitol and sorbitol fermentation patterns were also determined to establish correlations between subspecies status and phylogenetic relatedness. Nineteen 16S rRNA types were identified, but these were clustered into two distinct phylogenetic lineages, A and B. Sequences within lineages A and B had a mean number of nucleotide differences of 21·12±3·90. Isolates within lineage A were associated with birds, cattle, pigs and sheep, whereas those belonging to lineage B were recovered from birds and a cat. Eighty-seven per cent of the isolates were classified as subsp. by dulcitol and sorbitol fermentation patterns, but these have diverse 16S rRNA gene sequences that were represented in both lineages A and B. Avian subsp. isolates were associated exclusively with lineage B, but bovine subsp. isolates were present in lineage A. subsp. isolates of avian, bovine and porcine origin represent a homogeneous group within lineage A, but they have the same 16S rRNA type as certain subsp. isolates. These findings provide strong support for the view that dulcitol and sorbitol fermentation patterns are inaccurate indicators of genetic relatedness among strains. Avian capsular type B isolates and capsular type B and E isolates associated with haemorrhagic septicaemia of cattle and water buffaloes are closely related and form a distinct cluster within lineage A. The current subspecies nomenclature of neither accurately reflects the 16S rRNA-based phylogenetic relationships among isolates nor does it adequately encompass the full range of diversity within the species. The study provides a 16S rRNA-based evolutionary framework that will form the basis of further studies into the genetic diversity of and will also help in the reclassification of the species.

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2004-12-01
2024-03-28
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References

  1. Aalbaek, B., Eriksen, L., Rimler, R. B., Leifsson, P. S., Basse, A., Christiansen, T. & Eriksen, E.(1999). Typing of Pasteurella multocida from haemorrhagic septicaemia in Danish fallow deer (Dama dama). APMIS 107, 913–920.[CrossRef] [Google Scholar]
  2. Amonsin, A., Wellehan, J. F. X., Li, L. L., Laber, J. & Kapur, V.(2002). DNA fingerprinting of Pasteurella multocida recovered from avian sources. J Clin Microbiol 40, 3025–3031.[CrossRef] [Google Scholar]
  3. Blackall, P. J., Pahoff, J. L., Marks, D., Fegan, N. & Morrow, C. J.(1995). Characterisation of Pasteurella multocida isolated from fowl cholera outbreaks on turkey farms. Aust Vet J 72, 135–138.[CrossRef] [Google Scholar]
  4. Blackall, P. J., Fegan, N., Chew, G. T. I. & Hampson, D. J.(1998). Population structure and diversity of avian isolates of Pasteurella multocida from Australia. Microbiology 144, 279–289.[CrossRef] [Google Scholar]
  5. Blackall, P. J., Fegan, N., Pahoff, J. L. & 8 other authors(2000). The molecular epidemiology of four outbreaks of porcine pasteurellosis. Vet Microbiol 72, 111–120.[CrossRef] [Google Scholar]
  6. Bowles, R. E., Pahoff, J. L., Smith, B. N. & Blackall, P. J.(2000). Ribotype diversity of porcine Pasteurella multocida from Australia. Aust Vet J 78, 630–635.[CrossRef] [Google Scholar]
  7. Carpenter, T. E., Snipes, K. P., Kasten, R. W., Hird, D. W. & Hirsh, D. C.(1991). Molecular epidemiology of Pasteurella multocida in turkeys. Am J Vet Res 52, 1345–1349. [Google Scholar]
  8. Carter, G. R. & de Alwis, M. C. L.(1989). Haemorrhagic septicaemia. In Pasteurella and Pasteurellosis, pp. 131–160. Edited by C. F. Adlam & J. M. Rutter. London: Academic Press.
  9. Chanter, N. & Rutter, J. M.(1989). Pasteurellosis in pigs and the determinants of virulence of toxigenic Pasteurella multocida. In Pasteurella and Pasteurellosis, pp. 161–195. Edited by C. F. Adlam & J. M. Rutter. London: Academic Press.
  10. Christensen, H., Angen, O., Olsen, J. E. & Bisgaard, M.(2004). Revised description and classification of atypical isolates of Pasteurella multocida from bovine lungs based on genotypic characterization to include variants previously classified as biovar 2 of Pasteurella canis and Pasteurella avium. Microbiology 150, 1757–1767.[CrossRef] [Google Scholar]
  11. Christiansen, K. H., Carpenter, T. E., Snipes, K. P. & Hird, D. W.(1992). Transmission of Pasteurella multocida on California turkey premises in 1988–89. Avian Dis 36, 262–271.[CrossRef] [Google Scholar]
  12. Dabo, S. M., Debey, B. M., Montelongo, M. & Confer, A. W.(1999). Genomic DNA restriction site heterogeneity in bovine Pasteurella multocida serogroup A isolates detected with an rRNA probe. J Med Microbiol 48, 279–286.[CrossRef] [Google Scholar]
  13. Davies, R. L., Paster, B. J. & Dewhirst, F. E.(1996). Phylogenetic relationships and diversity within the Pasteurella haemolytica complex based on 16S rRNA sequence comparison and outer membrane protein and lipopolysaccharide analysis. Int J Syst Bacteriol 46, 736–744.[CrossRef] [Google Scholar]
  14. Davies, R. L., MacCorquodale, R., Baillie, S. & Caffrey, B.(2003a). Characterization and comparison of Pasteurella multocida strains associated with porcine pneumonia and atrophic rhinitis. J Med Microbiol 52, 59–67.[CrossRef] [Google Scholar]
  15. Davies, R. L., MacCorquodale, R. & Caffrey, B.(2003b). Diversity of avian Pasteurella multocida strains based on capsular PCR typing and variation of the OmpA and OmpH outer membrane proteins. Vet Microbiol 91, 169–182.[CrossRef] [Google Scholar]
  16. Davies, R. L., Watson, P. J. & Caffrey, B.(2003c). Comparative analyses of Pasteurella multocida strains associated with the ovine respiratory and vaginal tracts. Vet Rec 152, 7–10.[CrossRef] [Google Scholar]
  17. Davies, R. L., MacCorquodale, R. & Reilly, S.(2004). Characterisation of bovine strains of Pasteurella multocida and comparison with isolates of avian, ovine and porcine origin. Vet Microbiol 99, 145–158.[CrossRef] [Google Scholar]
  18. Dewhirst, F. E., Paster, B. J., Olsen, I. & Fraser, G. J.(1992). Phylogeny of 54 representative strains of species in the family Pasteurellaceae as determined by comparison of 16S rRNA sequences. J Bacteriol 174, 2002–2013. [Google Scholar]
  19. Frank, G. H.(1989). Pasteurellosis of cattle. In Pasteurella and Pasteurellosis, pp. 197–222. Edited by C. F. Adlam & J. M. Rutter. London: Academic Press.
  20. Gardner, I. A., Kasten, R., Eamens, G. J., Snipes, K. P. & Anderson, R. J.(1994). Molecular fingerprinting of Pasteurella multocida associated with progressive atrophic rhinitis in swine herds. J Vet Diagn Invest 6, 442–447.[CrossRef] [Google Scholar]
  21. Gunawardana, G. A., Townsend, K. M. & Frost, A. J.(2000). Molecular characterisation of avian Pasteurella multocida isolates from Australia and Vietnam by REP-PCR and PFGE. Vet Microbiol 72, 97–109.[CrossRef] [Google Scholar]
  22. Holm, M. & Tarnvik, A.(2000). Hospitalization due to Pasteurella multocida-infected animal bite wounds: correlation with inadequate primary antibiotic medication. Scand J Infect Dis 32, 181–183.[CrossRef] [Google Scholar]
  23. Korczak, B., Christensen, H., Emler, S., Frey, J. & Kuhnert, P.(2004). Phylogeny of the family Pasteurellaceae based on rpoB sequences. Int J Syst Evol Microbiol 54, 1393–1399.[CrossRef] [Google Scholar]
  24. Krametter, R., Hassan, J., Mayrhofer, E. & Baumgartner, W.(2004). Atrophic rhinitis in sheep in Austria. Vet Rec 154, 147–148.[CrossRef] [Google Scholar]
  25. Kuhnert, P., Boerlin, P., Emler, S., Krawinkler, M. & Frey, J.(2000). Phylogenetic analysis of Pasteurella multocida subspecies and molecular identification of feline P. multocida subsp. septica by 16S rRNA gene sequencing. Int J Med Microbiol 290, 599–604.[CrossRef] [Google Scholar]
  26. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M.(2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.[CrossRef] [Google Scholar]
  27. Lu, Y. S., Afendis, S. J. & Pakes, S. P.(1988). Identification of immunogenic outer membrane proteins of Pasteurella multocida 3 : A in rabbits. Infect Immun 56, 1532–1537. [Google Scholar]
  28. Miflin, J. K. & Blackall, P. J.(2001). Development of a 23S rRNA-based PCR assay for the identification of Pasteurella multocida. Lett Appl Microbiol 33, 216–221.[CrossRef] [Google Scholar]
  29. Muhairwa, A. P., Christensen, J. P. & Bisgaard, M.(2001). Relationships among Pasteurellaceae isolated from free ranging chickens and their animal contacts as determined by quantitative phenotyping, ribotyping and REA-typing. Vet Microbiol 78, 119–137.[CrossRef] [Google Scholar]
  30. Mutters, R., Ihm, P., Pohl, S., Frederiksen, W. & Mannheim, W.(1985). Reclassification of the genus Pasteurella Trevisan 1887 on the basis of deoxyribonucleic acid homology, with proposals for the new species Pasteurella dagmatis, Pasteurella canis, Pasteurella stomatis, Pasteurella anatis, and Pasteurella langaa. Int J Syst Bacteriol 35, 309–322.[CrossRef] [Google Scholar]
  31. Olsen, I., Dewhirst, F. E., Paster, B. J. & Busse, H. J.(2003). Family Pasteurellaceae Pohl 1981, 382VP. In Bergey's Manual of Systematic Bacteriology. Edited by D. J. Brenner, N. R. Krieg, J. T. Staley & G. M. Garrity. New York: Springer.
  32. Petersen, K. D., Christensen, J. P. & Bisgaard, M.(1998). Phenotypic and genotypic diversity of organisms previously classified as maltose positive Pasteurella multocida. Zentbl Bakteriol 288, 1–12.[CrossRef] [Google Scholar]
  33. Petersen, K. D., Christensen, H., Bisgaard, M. & Olsen, J. E.(2001). Genetic diversity of Pasteurella multocida fowl cholera isolates as demonstrated by ribotyping and 16S rRNA and partial atpD sequence comparisons. Microbiology 147, 2739–2748. [Google Scholar]
  34. Rhoades, K. R. & Rimler, R. B.(1987). Capsular groups of Pasteurella multocida isolated from avian hosts. Avian Dis 31, 895–898.[CrossRef] [Google Scholar]
  35. Rhoades, K. R. & Rimler, R. B.(1989). Fowl cholera. In Pasteurella and Pasteurellosis, pp. 95–113. Edited by C. F. Adlam & J. M. Rutter. London: Academic Press.
  36. Rimler, R. B.(2000). Restriction endonuclease analysis using HhaI and HpaII to discriminate among group B Pasteurella multocida associated with haemorrhagic septicaemia. J Med Microbiol 49, 81–87. [Google Scholar]
  37. Rimler, R. B. & Brogden, K. A.(1986).Pasteurella multocida isolated from rabbits and swine: serologic types and toxin production. Am J Vet Res 47, 730–737. [Google Scholar]
  38. Rimler, R. B. & Glisson, J. R.(1997). Fowl cholera. In Diseases of Poultry, pp. 143–159. Edited by B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald & Y. M. Saif. Ames: Iowa State University Press.
  39. Rimler, R. B. & Rhoades, K. R.(1989).Pasteurella multocida. In Pasteurella and Pasteurellosis, pp. 37–73. Edited by C. F. Adlam & J. M. Rutter. London: Academic Press.
  40. Rimler, R. B., Rhoades, K. R. & Jones, T. O.(1987). Serological and immunological study of Pasteurella multocida strains that produced septicaemia in fallow deer. Vet Rec 121, 300–301.[CrossRef] [Google Scholar]
  41. Sacchi, C. T., Whitney, A. M., Reeves, M. W., Mayer, L. W. & Popovic, T.(2002). Sequence diversity of Neisseria meningitidis 16S rRNA genes and use of 16S rRNA gene sequencing as a molecular subtyping tool. J Clin Microbiol 40, 4520–4527.[CrossRef] [Google Scholar]
  42. Schouls, L. M., Schot, C. S. & Jacobs, J. A.(2003). Horizontal transfer of segments of the 16S rRNA genes between species of the Streptococcus anginosus group. J Bacteriol 185, 7241–7246.[CrossRef] [Google Scholar]
  43. Snipes, K. P., Hirsh, D. C., Kasten, R. W., Hansen, L. M., Hird, D. W., Carpenter, T. E. & McCapes, R. H.(1989). Use of an rRNA probe and restriction endonuclease analysis to fingerprint Pasteurella multocida isolated from turkeys and wildlife. J Clin Microbiol 27, 1847–1853. [Google Scholar]
  44. Watson, P. J. & Davies, R. L.(2002). Outbreak of Pasteurella multocida septicaemia in neonatal lambs. Vet Rec 151, 420–422.[CrossRef] [Google Scholar]
  45. Westling, K., Bygdeman, S., Engkvist, O. & Jorup-Ronstrom, C.(2000).Pasteurella multocida infection following cat bites in humans. J Infect 40, 97–98.[CrossRef] [Google Scholar]
  46. Wilson, M. A., Morgan, M. J. & Barger, G. E.(1993). Comparison of DNA fingerprinting and serotyping for identification of avian Pasteurella multocida isolates. J Clin Microbiol 31, 255–259. [Google Scholar]
  47. Wilson, M. A., Duncan, R. M., Nordholm, G. E. & Berlowski, B. M.(1995).Pasteurella multocida isolated from wild birds of North America: a serotype and DNA fingerprint study of isolates from 1978 to 1993. Avian Dis 39, 587–593.[CrossRef] [Google Scholar]
  48. Zhao, G., Pijoan, C., Murtaugh, M. P. & Molitor, T. W.(1992). Use of restriction endonuclease analysis and ribotyping to study epidemiology of Pasteurella multocida in closed swine herds. Infect Immun 60, 1401–1405. [Google Scholar]
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