Evidence for horizontal gene transfer of two antigenically distinct O antigens in Bordetella bronchiseptica

Infection and Immunity

Volumn 77, Issue 8, 2009, Pages 3249-3257

  Buboltz, Anne M ^a   Nicholson, Tracy L ^b   Karanikas, Alexia T ^a   Preston, Andrew ^c   Harvill, Eric T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b NATIONAL ANIMAL DISEASE CENTER   (United States)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

O ANTIGEN;

ANIMAL EXPERIMENT; ARTICLE; BORDETELLA BRONCHISEPTICA; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; GENE EXPRESSION; GENE SEGREGATION; GENE TRANSFER; IN VIVO STUDY; MOUSE; NONHUMAN; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BORDETELLA BRONCHISEPTICA; BORDETELLA INFECTIONS; CLUSTER ANALYSIS; COMPARATIVE GENOMIC HYBRIDIZATION; DNA FINGERPRINTING; DNA, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENOTYPE; MICE; MICE, INBRED C57BL; O ANTIGENS; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 67651204664     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01448-08     Document Type: Article

References (43)

1. Allen, A., and D. Maskell. 1996. The identification, cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordetella pertussis. Mol. Microbiol. 19:37-52.
2. Allen, A. G., R. M. Thomas, J. T. Cadisch, and D. J. Maskell. 1998. Molecular and functional analysis of the lipopolysaccharide biosynthesis locus wlb from Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Mol. Microbiol. 29:27-8.
3. Anderson, R. M. 1995. Evolutionary pressures in the spread and persistence of infectious agents in vertebrate populations. Parasitology. 111(Suppl.):S15-S31.
4. Bjornstad, O. N., and E. T. Harvill. 2005. Evolution and emergence of Bordetella in humans. Trends Microbiol. 13:355-359.
5. Brinig, M. M., C. A. Cummings, G. N. Sanden, P. Stefanelli, A. Lawrence, and D. A. Relman. 2006. Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J. Bacteriol. 188:2375-2382.
6. Buboltz, A. M., T. L. Nicholson, M. R. Parette, S. E. Hester, J. Parkhill, and E. T. Harvill. 2008. Replacement of adenylate cyclase toxin in a lineage of Bordetella bronchiseptica. J. Bacteriol. 190:5502-5511.
7. Buboltz, A. M., T. L. Nicholson, L. S. Weyrich, and E. T. Harvill. Role of the type III secretion system in a hypervirulent lineage of Bordetella bronchiseptica. Infect. Immun., in press.
8. Burns, V. C., E. J. Pishko, A. Preston, D. J. Maskell, and E. T. Harvill. 2003. Role of Bordetella O antigen in respiratory tract infection. Infect. Immun. 71:86-94.
9. Cotter, P. A., and J. F. Miller. 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62:3381-3390.
10. Diavatopoulos, D. A., C. A. Cummings, L. M. Schouls, M. M. Brinig, D. A. Relman, and F. R. Mooi. 2005. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 1:e45.
11. Goebel, E. M., D. N. Wolfe, K. Elder, S. Stibitz, and E. T. Harvill. 2008. O antigen protects Bordetella parapertussis from complement. Infect. Immun. 76:1774-1780.
12. Gog, J. R., and B. T. Grenfell. 2002. Dynamics and selection of many-strain pathogens. Proc. Natl. Acad. Sci. USA 99:17209-17214.
13. Gonzalez-Fraga, S., M. Pichel, N. Binsztein, J. A. Johnson, J. G. Morris, Jr., and O. C. Stine. 2008. Lateral gene transfer of O1 serogroup encoding genes of Vibrio cholerae. FEMS Microbiol. Lett. 286:32-38.
14. Gueirard, P., K. Le Blay, A. Le Coustumier, R. Chaby, and N. Guiso. 1998. Variation in Bordetella bronchiseptica lipopolysaccharide during human infection. FEMS Microbiol. Lett. 162:331-337.
15. Gupta, S., and R. M. Anderson. 1999. Population structure of pathogens: the role of immune selection. Parasitol. Today 15:497-501.
16. Gupta, S., and M. C. Maiden. 2001. Exploring the evolution of diversity in pathogen populations. Trends Microbiol. 9:181-185.
17. Harvill, E. T., A. Preston, P. A. Cotter, A. G. Allen, D. J. Maskell, and J. F. Miller. 2000. Multiple roles for Bordetella lipopolysaccharide molecules during respiratory tract infection. Infect. Immun. 68:6720-6728.
18. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
19. Kingsley, R. A., and A. J. Baumler. 2000. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36:1006-1014.
20. Kirimanjeswara, G. S., P. B. Mann, and E. T. Harvill. 2003. Role of antibodies in immunity to Bordetella infections. Infect. Immun. 71:1719-1724.
21. Kirimanjeswara, G. S., P. B. Mann, M. Pilione, M. J. Kennett, and E. T. Harvill. 2005. The complex mechanism of antibody-mediated clearance of Bordetella from the lungs requires TLR4. J. Immunol. 175:7504-7511.
22. Koelle, K., M. Pascual, and M. Yunus. 2006. Serotype cycles in cholera dynamics. Proc. Biol. Sci. 273:2879-2886.
23. Kubler-Kielb, J., E. Vinogradov, G. Ben-Menachem, V. Pozsgay, J. B. Robbins, and R. Schneerson. 2008. Saccharide/protein conjugate vaccines for Bordetella species: preparation of saccharide, development of new conjugation procedures, and physico-chemical and immunological characterization of the conjugates. Vaccine 26:3587-3593.
24. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
25. Longini, I. M., Jr., M. Yunus, K. Zaman, A. K. Siddique, R. B. Sack, and A. Nizam. 2002. Epidemic and endemic cholera trends over a 33-year period in Bangladesh. J. Infect. Dis. 186:246-251.
26. Mattoo, S., and J. D. Cherry. 2005. Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin. Microbiol. Rev. 18:326-382.
27. Mooi, F. R., and E. M. Bik. 1997. The evolution of epidemic Vibrio cholerae strains. Trends Microbiol. 5:161-165.
28. Murray, G. L., S. R. Attridge, and R. Morona. 2006. Altering the length of the lipopolysaccharide O antigen has an impact on the interaction of Salmonella enterica serovar Typhimurium with macrophages and complement. J. Bacteriol. 188:2735-2739.
29. Myc, A., J. Buck, J. Gonin, B. Reynolds, U. Hammerling, and D. Emanuel. 1997. The level of lipopolysaccharide-binding protein is significantly increased in plasma in patients with the systemic inflammatory response syndrome. Clin. Diagn. Lab. Immunol. 4:113-116.
30. Nicholson, T. L. 2007. Construction and validation of a first-generation Bordetella bronchiseptica long-oligonucleotide microarray by transcriptional profiling the Bvg regulon. BMC Genomics 8:-220.
31. Parkhill, J., M. Sebaihia, A. Preston, L. D. Murphy, N. Thomson, D. E. Harris, M. T. Holden, C. M. Churcher, S. D. Bentley, K. L. Mungall, A. M. Cerdeno-Tarraga, L. Temple, K. James, B. Harris, M. A. Quail, M. Achtman, R. Atkin, S. Baker, D. Basham, N. Bason, I. Cherevach, T. Chillingworth, M. Collins, A. Cronin, P. Davis, J. Doggett, T. Feltwell, A. Goble, N. Hamlin, H. Hauser, S. Holroyd, K. Jagels, S. Leather, S. Moule, H. Norberczak, S. O'Neil, D. Ormond, C. Price, E. Rabbinowitsch, S. Rutter, M. Sanders, D. Saunders, K. Seeger, S. Sharp, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, L. Unwin, S. Whitehead, B. G. Barrell, and D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:32-40.
32. Plotkin, J. B., J. Dushoff, and S. A. Levin. 2002. Hemagglutinin sequence clusters and the antigenic evolution of influenza A virus. Proc. Natl. Acad. Sci. USA 99:6263-6268.
33. Preston, A., A. G. Allen, J. Cadisch, R. Thomas, K. Stevens, C. M. Churcher, K. L. Badcock, J. Parkhill, B. Barrell, and D. J. Maskell. 1999. Genetic basis for lipopolysaccharide O-antigen biosynthesis in bordetellae. Infect. Immun. 67:3763-3767.
34. Preston, A., and D. Maskell. 2001. The molecular genetics and role in infection of lipopolysaccharide biosynthesis in the Bordetellae. J. Endotoxin Res. 7:251-261.
35. Preston, A., J. Parkhill, and D. J. Maskell. 2004. The bordetellae: lessons from genomics. Nat. Rev. Microbiol. 2:379-390.
36. Preston, A., B. O. Petersen, J. O. Duus, J. Kubler-Kielb, G. Ben-Menachem, J. Li, and E. Vinogradov. 2006. Complete structures of Bordetella bronchiseptica and Bordetella parapertussis lipopolysaccharides. J. Biol. Chem. 281:18135-18144.
37. Reeves, P. 1993. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet. 9:17-22.
38. Reeves, P. 1995. Role of O-antigen variation in the immune response. Trends Microbiol. 3:381-386.
39. Stenutz, R., A. Weintraub, and G. Widmalm. 2006. The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol. Rev. 30:382-403.
40. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
41. Vinogradov, E., M. S. Peppler, and M. B. Perry. 2000. The structure of the nonreducing terminal groups in the O-specific polysaccharides from two strains of Bordetella bronchiseptica. Eur. J. Biochem. 267:7230-7237.
42. Wolfe, D. N., E. M. Goebel, O. N. Bjornstad, O. Restif, and E. T. Harvill. 2007. The O antigen enables Bordetella parapertussis to avoid Bordetella pertussis-induced immunity. Infect. Immun. 75:4972-4979.
43. Wolfe, D. N., G. S. Kirimanjeswara, E. M. Goebel, and E. T. Harvill. 2007. Comparative role of immunoglobulin A in protective immunity against the bordetellae. Infect. Immun. 75:4416-4422.