1887

Microbiology Society logo

Volume 157, Issue 1

Evidence for a common gene pool and frequent recombinational exchange of the operon in , and Free

Abstract

The operon was sequenced in 42 representative isolates of (32), (6) and (4). A total of 27 and 20 alleles were identified whilst the operon was represented by 28 unique alleles that could be assigned to seven classes. There were 1566 (34.8 % variation) polymorphic nucleotide sites and 482 (32.1 % variation) variable inferred amino acid positions among the 42 sequences. The operons of serotype A2 isolates are, with one exception, substantially more diverse than those of the other serotypes and most likely have a different ancestral origin. The phylogeny has been severely disrupted by numerous small- and large-scale intragenic recombination events. In addition, assortative (entire gene) recombination events, involving either the entire operon or the individual and genes, have played a major role in shaping structure and it's distribution in the three species. Our findings indicate that a common gene pool exists for in , and . In particular, , and ovine isolates share a large portion of the gene, and this probably reflects selection for a conserved TbpA protein that provides effective iron uptake in sheep. Bovine and ovine serotype A2 lineages have very different alleles. Bovine-like alleles have been partially, or completely, replaced by ovine-like alleles in ovine serotype A2 isolates, suggesting that different transferrin receptors are required by serotype A2 isolates for optimum iron uptake in cattle and sheep. Conversely, the alleles of bovine-pathogenic serotype A1 and A6 isolates are very similar to those of closely related ovine isolates, suggesting a recent and common evolutionary origin.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): ET, electrophoretic type
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.041236-0
2011-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/1/123.html?itemId=/content/journal/micro/10.1099/mic.0.041236-0&mimeType=html&fmt=ahah

References

  1. Angen O., Mutters R., Caugant D. A., Olsen J. E., Bisgaard M. 1999; Taxonomic relationships of the [ Pasteurella ] haemolytica complex as evaluated by DNA–DNA hybridizations and 16s rRNA sequencing with proposal of Mannheimia haemolytica gen. nov., comb. nov., Mannheimia granulomatis comb. nov., Mannheimia glucosida sp. nov., Mannheimia ruminalis sp. nov. and Mannheimia varigena sp. nov. Int J Syst Bacteriol 49:67–86
     [Google Scholar]
  2. Bennett J. S., Thompson E. A., Kriz P., Jolley K. A., Maiden M. C. J. 2009; A common gene pool for the Neisseria FetA antigen. Int J Med Microbiol 299:133–139
     [Google Scholar]
  3. Bentley S. D., Vernikos G. S., Snyder L. A. S. 2007; Meningococcal genetic variation mechanisms viewed through comparative analysis of serogroup C strain FAM18. PLoS Genet 3:e23
     [Google Scholar]
  4. Blackall P. J., Bojesen A. M., Christensen H., Bisgaard M. 2007; Reclassification of [ Pasteurella ] trehalosi as Bibersteinia trehalosi gen. nov., comb. nov. Int J Syst Evol Microbiol 57:666–674
     [Google Scholar]
  5. Brehony C., Wilson D. J., Maiden M. C. J. 2009; Variation of the factor H-binding protein of Neisseria meningitidis . Microbiology 155:4155–4169
     [Google Scholar]
  6. Buchanan S. K., Smith B. S., Venkatramani L., Xia D., Esser L., Palnitkar M., Chakraborty R., van der Helm D., Deisenhofer J. 1999; Crystal structure of the outer membrane active transporter FepA from Escherichia coli . Nat Struct Biol 6:56–63
     [Google Scholar]
  7. Cornelissen C. N. 2003; Transferrin-iron uptake by Gram-negative bacteria. Front Biosci 8:d836–d847
     [Google Scholar]
  8. Cornelissen C. N., Anderson J. E., Sparling P. F. 1997; Characterization of the diversity and the transferrin-binding domain of gonococcal transferrin-binding protein 2. Infect Immun 65:822–828
     [Google Scholar]
  9. Cornelissen C. N., Anderson J. E., Boulton I. C., Sparling P. F. 2000; Antigenic and sequence diversity in gonococcal transferrin-binding protein A (TbpA. Infect Immun 68:4725–4735
     [Google Scholar]
  10. Davies R. L., Donachie W. 1996; Intra-specific diversity and host specificity within Pasteurella haemolytica based on variation of capsular polysaccharide, lipopolysaccharide and outer-membrane proteins. Microbiology 142:1895–1907
     [Google Scholar]
  11. Davies R. L., Lee I. 2004; Sequence diversity and molecular evolution of the heat-modifiable outer membrane protein gene ( ompA ) of Mannheimia ( Pasteurella ) haemolytica Mannheimia glucosida , and Pasteurella trehalosi . J Bacteriol 186:5741–5752
     [Google Scholar]
  12. Davies R. L., Quirie M. 1996; Intra-specific diversity within Pasteurella trehalosi based on variation of capsular polysaccharide, lipopolysaccharide and outer-membrane proteins. Microbiology 142:551–560
     [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
     [Google Scholar]
  14. Davies R. L., Arkinsaw S., Selander R. K. 1997a; Evolutionary genetics of Pasteurella haemolytica isolates recovered from cattle and sheep. Infect Immun 65:3585–3593
     [Google Scholar]
  15. Davies R. L., Arkinsaw S., Selander R. K. 1997b; Genetic relationships among Pasteurella trehalosi isolates based on multilocus enzyme electrophoresis. Microbiology 143:2841–2849
     [Google Scholar]
  16. Davies R. L., Whittam T. S., Selander R. K. 2001; Sequence diversity and molecular evolution of the leukotoxin ( lktA ) gene in bovine and ovine strains of Mannheimia Pasteurella ) haemolytica . J Bacteriol 183:1394–1404
     [Google Scholar]
  17. Davies R. L., Campbell S., Whittam T. S. 2002; Mosaic structure and molecular evolution of the leukotoxin operon ( lktCABD ) in Mannheimia ( Pasteurella ) haemolytica Mannheimia glucosida and Pasteurella trehalosi . J Bacteriol 184:266–277
     [Google Scholar]
  18. Derrick J. P., Urwin R., Suker J., Feavers I. M., Maiden M. C. J. 1999; Structural and evolutionary inference from molecular variation in Neisseria porins. Infect Immun 67:2406–2413
     [Google Scholar]
  19. Didelot X., Falush D. 2007; Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251–1266
     [Google Scholar]
  20. Frank G. H. 1989; Pasteurellosis of cattle. In: Pasteurella. Edited by Adlam C. F., Rutter J. M. Pasteurellosis pp 197–222 London: Academic Press;
     [Google Scholar]
  21. Gilmour N. J. L., Gilmour J. S. 1989; Pasteurellosis of sheep. In Pasteurella. Edited by Adlam C. F., Rutter J. M. Pasteurellosis pp 223–261 London: Academic Press;
     [Google Scholar]
  22. Gilmour N. J. L., Donachie W., Sutherland A. D., Gilmour J. S., Jones G. E., Quirie M. 1991; Vaccine containing iron-regulated proteins of Pasteurella haemolytica A2 enhances protection against experimental pasteurellosis in lambs. Vaccine 9:137–140
     [Google Scholar]
  23. Gioia J., Qin X., Jiang H., Clinkenbeard K., Lo R., Liu Y., Fox G. E., Yerrapragada S., McLeod M. P. other authors 2006; The genome sequence of Mannheimia haemolytica A1: insights into virulence, natural competence, and Pasteurellaceae phylogeny. J Bacteriol 188:7257–7266
     [Google Scholar]
  24. Harrison O. B., Maiden M. C. J., Rokbi B. 2008; Distribution of transferrin binding protein B gene ( tbpB ) variants among Neisseria species. BMC Microbiol 8:66
     [Google Scholar]
  25. Huson D. H., Bryant D. 2006; Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267
     [Google Scholar]
  26. Kuhnert P., Korczak B. M. 2006; Prediction of whole-genome DNA–DNA similarity, determination of G+C content and phylogenetic analysis within the family Pasteurellaceae by multilocus sequence analysis (MLSA. Microbiology 152:2537–2548
     [Google Scholar]
  27. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17:1244–1245
     [Google Scholar]
  28. Lee I. 2004; Molecular evolution of Mannheimia (Pasteurella) haemolytica, Mannheimia glucosida and Pasteurella trehalosi and characterization of temperate bacteriophages . PhD thesis University of Glasgow; Glasgow:
     [Google Scholar]
  29. Linz B., Schenker M., Zhu P., Achtman M. 2000; Frequent interspecific genetic exchange between commensal Neisseriae and Neisseria meningitidis . Mol Microbiol 36:1049–1058
     [Google Scholar]
  30. Moraes T. F., Yu R. H., Strynadka N. C. J., Schryvers A. B. 2009; Insights into the bacterial transferrin receptor: the structure of transferrin-binding protein B from Actinobacillus pleuropneumoniae . Mol Cell 35:523–533
     [Google Scholar]
  31. Ogunnariwo J. A., Schryvers A. B. 1990; Iron acquisition in Pasteurella haemolytica : Expression and identification of a bovine-specific transferrin receptor. Infect Immun 58:2091–2097
     [Google Scholar]
  32. Ogunnariwo J. A., Schryvers A. B. 1996; Rapid identification and cloning of bacterial transferrin and lactoferrin receptor protein genes. J Bacteriol 178:7326–7328
     [Google Scholar]
  33. Ogunnariwo J. A., Woo T. K. W., Lo R. Y. C., Gonzalez G. C., Schryvers A. B. 1997; Characterization of the Pasteurella haemolytica transferrin receptor genes and the recombinant receptor proteins. Microb Pathog 23:273–284
     [Google Scholar]
  34. Potter A. A., Schryvers A. B., Ogunnariwo J. A., Hutchins W. A., Lo R. Y. C., Watts T. 1999; Protective capacity of the Pasteurella haemolytica transferrin-binding proteins TbpA and TbpB in cattle. Microb Pathog 27:197–206
     [Google Scholar]
  35. Rokbi B., Mazarin V., Maitre-Wilmotte G., Quentin-Millet M. J. 1993; Identification of two major families of transferrin receptors among Neisseria meningitidis strains based on antigenic and genomic features. FEMS Microbiol Lett 110:51–57
     [Google Scholar]
  36. Rokbi B., Maitre-Wilmotte G., Mazarin V., Fourrichon L., Lissolo L., Quentin-Millet M. J. 1995; Variable sequences in a mosaic-like domain of meningococcal Tbp2 encode immunoreactive epitopes. FEMS Microbiol Lett 132:277–283
     [Google Scholar]
  37. Rokbi B., Mignon M., Maitre-Wilmotte G., Lissolo L., Danve B., Caugant D. A., Quentin-Millet M. J. 1997; Evaluation of recombinant transferrin-binding protein B variants from Neisseria meningitidis for their ability to induce cross-reactive and bactericidal antibodies against a genetically diverse collection of serogroup B strains. Infect Immun 65:55–63
     [Google Scholar]
  38. Rokbi B., Renauld-Mongenie G., Mignon M., Danve B., Poncet D., Chabanel C., Caugant D. A., Quentin-Millet M. J. 2000; Allelic diversity of the two transferrin binding protein B gene isotypes among a collection of Neisseria meningitidis strains representative of serogroup B disease: Implication for the composition of a recombinant TbpB-based vaccine. Infect Immun 68:4938–4947
     [Google Scholar]
  39. Sneath P. H. A., Stevens M. 1990; Actinobacillus rossii sp. nov., Actinobacillus seminis sp. nov., nom. rev., Pasteurella bettii sp. nov., Pasteurella lymphangitidis sp. nov., Pasteurella mairi sp. nov., and Pasteurella trehalosi sp. nov. Int J Syst Bacteriol 40148–153
     [Google Scholar]
  40. Yu R.-H., Schryvers A. B. 1994; Transferrin receptors on ruminant pathogens vary in their interactions with the C-lobe and N-lobe of ruminant transferrins. Can J Microbiol 40:532–540
     [Google Scholar]
  41. Yu R.-H., Gray-Owen S. D., Ogunnariwo J., Schryvers A. B. 1992; Interaction of ruminant transferrins with transferrin receptors in bovine isolates of Pasteurella haemolytica and Haemophilus somnus . Infect Immun 60:2992–2994
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.041236-0
Loading
Evidence for a common gene pool and frequent recombinational exchange of the tbpBA operon in Mannheimia haemolytica, Mannheimia glucosida and Bibersteinia trehalosi
Microbiology 157, 123 (2011); https://doi.org/10.1099/mic.0.041236-0
/content/journal/micro/10.1099/mic.0.041236-0
/content/journal/micro/10.1099/mic.0.041236-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error