Skip to main content

Advertisement

Log in

Heterogeneity of Bordetella bronchiseptica adenylate cyclase (cyaA) RTX domain

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Bordetella bronchiseptica is a widespread pathogen, with a broad host range, occasionally including humans. Diverse virulence factors (adhesins, toxins) allow its adaptation to its host, but this property of the adenylate cyclase (cyaA) toxin is not well understood. In this study, we analyzed the repeats-in-toxin domain of B. bronchiseptica cyaA with PCR, followed by restriction fragment length analysis. Of ninety-two B. bronchiseptica strains collected from different hosts and geographic regions, 72 (78.3 %) carried cyaA and four RFLP types (A–D) were established using NarI and SalI. However, in 20 strains, cyaA was replaced with a peptide transport protein operon. A phylogenetic tree based on partial nucleotide sequences of cyaA revealed that group 2 contains strains of specifically human origin, whereas subgroup 1a contains all but one of the strains from pigs. The human strains showed many PCR–RFLP and sequence variants, confirming the clonal population structure of B. bronchiseptica.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akerley BJ, Monack DM, Falkow S, Miller JF (1992) The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J Bacteriol 174:980–990

    CAS  PubMed Central  PubMed  Google Scholar 

  • Betsou F, Seismiro O, Danchin A, Guiso N (1995) Cloning and sequence of Bordetella bronchiseptica adenylate cyclase-hemolysin-encoding gene: comparison with the Bordetella pertussis gene. Gene 162:165–166

    Article  CAS  PubMed  Google Scholar 

  • Buboltz AM, Nicholson TL, Parette MR, Hester SE, Parkhill J, Harvill ET (2008) Replacement of adenylate cyclase toxin in a lineage of Bordetella bronchiseptica. J Bacteriol 190:5502–5511

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carbonetti NH (2010) Pertussis toxin and adenylate cyclase toxin: key virulence factors of Bordetella pertussis and cell biology tools. Future Microbiol 5:455–469

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chenal-Francisque V, Caro V, Boursaux-Eude C, Guiso N (2009) Genomic analysis of the adenylate cyclase-hemolysin C-terminal region of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Res Microbiol 160:330–336

    Article  CAS  PubMed  Google Scholar 

  • Cotter PA, Miller JF (2001) Bordetella. In: Groisman EA (ed) Principles of bacterial pathogenesis. Academic Press, San Diego, pp 619–674

    Chapter  Google Scholar 

  • El-Azami-El-Idrissi M, Bauche C, Loucka J, Osicka R, Sebo P, Ladant D, Leclerc C (2003) Interaction of Bordetella pertussis adenylate cyclase with CD11b/CD18: role of toxin acylation and identification of the main integrin interaction domain. J Biol Chem 278:38514–38521

    Article  CAS  PubMed  Google Scholar 

  • Glaser P, Ladant D, Sezer O, Pichot F, Ullmann A, Danchin A (1988) The calmodulin-sensitive adenylate cyclase of Bordetella pertussis: cloning and expression in Escherichia coli. Mol Microbiol 2:19–30

    Article  CAS  PubMed  Google Scholar 

  • González GM, Rosales ME, Morales GB, Crespo JAM (2006) Isolation and characterisation of Bordetella bronchiseptica strains from canine origin. Vet Mexico 37:313–325

    Google Scholar 

  • Goodnow RA (1980) Biology of Bordetella bronchiseptica. Microbiol Rev 44:722–738

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid S 41:95–98

    CAS  Google Scholar 

  • Harvill ET, Cotter PA, Yuk MH, Miller JF (1999) Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect Immun 67:1493–1500

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hewlett EL, Donato GM (2007) Bordetella toxins. In: Locht C (ed) Bordetella molecular microbiology. Horizon Bioscience, Norfolk, UK, pp 97–118

  • Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  PubMed  Google Scholar 

  • Hozbor D, Fouque F, Guiso N (1999) Detection of Bordetella bronchiseptica by the polymerase chain reaction. Res Microbiol 150:333–341

    Article  CAS  PubMed  Google Scholar 

  • Khayer B, Rónai Z, Wehmann E, Magyar T (2011) Detection of urease-negative Bordetella bronchiseptica from the field. Acta Vet Hung 59:289–293

    Article  CAS  PubMed  Google Scholar 

  • Khelef N, Zychlinsky A, Guiso N (1993) Bordetella pertussis induces apoptosis in macrophages: role of adenylate cyclase-hemolysin. Infect Immun 61:4064–4071

    CAS  PubMed Central  PubMed  Google Scholar 

  • Magyar T, Lax AJ (2002) Atrophic rhinitis. In: Brogden KA, Guthmiller JM (eds) Polymicrobial diseases. ASM Press, Washington, pp 169–197

    Chapter  Google Scholar 

  • Mattoo S, Cherry JD (2005) Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. Clin Microbiol Rev 18:326–382

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mattoo S, Foreman-Wykert AK, Cotter PA, Miller JF (2001) Mechanisms of Bordetella pathogenesis. Front Biosci 6:E168–E186

    Article  CAS  PubMed  Google Scholar 

  • Park J, Zhang Y, Buboltz AM et al (2012) Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens. BMC Genomics 13:545

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parkhill J, Sebaihia M, Preston A et al (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40

    Article  PubMed  Google Scholar 

  • Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M (2008) Cyclic AMP: master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39:127–132

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stępniewska K, Markowska-Daniel I (2010) Evaluation of PCR test for detection of dermonecrotoxin of Bordetella bronchiseptica. Bull Vet I Pulawy 54:495–499

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vojtova J, Kamanova J, Sebo P (2006a) Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr Opin Microbiol 9:69–75

    Article  CAS  PubMed  Google Scholar 

  • Vojtova J, Kofronova O, Sebo P, Beneda O (2006b) Bordetella adenylate cyclase toxin induces a cascade of morphological changes of sheep erythrocytes and localizes into clusters in erythrocyte membranes. Microsc Res Tech 69:119–129

    Article  CAS  PubMed  Google Scholar 

  • Wernli D, Emonet S, Schrenzel J, Harbarth S (2011) Evaluation of eight cases of confirmed Bordetella bronchiseptica infection and colonization over a 15-year period. Clin Microbiol Infect 17:201–203

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Hungarian Scientific Research Fund (OTKA, K83332). We thank Prof. Alistair Lax (Microbiology Department of King’s College, London, UK) and Karen B. Register (National Animal Disease Center, USDA, Ames, IA, USA) for providing strains.

Conflict of interest

The authors have no conflicts of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Enikő Wehmann.

Additional information

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wehmann, E., Khayer, B. & Magyar, T. Heterogeneity of Bordetella bronchiseptica adenylate cyclase (cyaA) RTX domain. Arch Microbiol 197, 105–112 (2015). https://doi.org/10.1007/s00203-014-1068-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-014-1068-x

Keywords

Navigation