Skip to main content

Advertisement

SpringerLink
Log in

Resemblance and divergence: the “new” members of the genus Bordetella

  • Review
  • Published:
Medical Microbiology and Immunology Aims and scope Submit manuscript

Abstract

Bordetella pertussis, the etiological agent of whooping cough, belongs to the bacterial pathogens first described in the so-called golden era of microbiology more than 100 years ago. In the course of the following decades, several other closely related pathogens were described which are nowadays classified in the genus Bordetella together with B. pertussis. These are the human and animal pathogens B. parapertussis, B. bronchiseptica and B. avium which are of high medical or veterinary interest, and which, together with B. pertussis, are referred to as the “classical” Bordetella species. Only in the past 15 years, several additional species were classified in the genus, frequently isolated from patients with underlying disease, animals or from the environment. Very little is known about most of these bacteria. In the present review, the current knowledge about these “new” Bordetella species is briefly summarized.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Locht C, Antoine R, Jacob-Dubuisson F (2001) Bordetella pertussis, molecular pathogenesis under multiple aspects. Curr Opin Microbiol 4:82–89

    Article  PubMed  CAS  Google Scholar 

  2. 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  PubMed  CAS  Google Scholar 

  3. Bjørnstad ON, Harvill ET (2005) Evolution and emergence of Bordetella in humans. Trends Microbiol 13:355–359

    Article  PubMed  Google Scholar 

  4. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, Cerdeño-Tárraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, Holroyd S, Jagels K, Leather S, Moule S, Norberczak H, O’Neil S, Ormond D, Price C, Rabbinowitsch E, Rutter S, Sanders M, Saunders D, Seeger K, Sharp S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Unwin L, Whitehead S, Barrell BG, Maskell DJ (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40

    Article  PubMed  Google Scholar 

  5. Diavatopoulos DA, Cummings CA, Schouls LM, Brinig MM, Relman DA, Mooi FR (2005) Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog 1:e45

    Article  PubMed  Google Scholar 

  6. Gerlach G, von Wintzingerode F, Middendorf B, Gross R (2001) Evolutionary trends in the genus Bordetella. Microbes Infect 3:61–72

    Article  PubMed  CAS  Google Scholar 

  7. von Wintzingerode F, Gerlach G, Schneider B, Gross R (2002) Phylogenetic relationships and virulence evolution in the genus Bordetella. Curr Top Microbiol Immunol 264:177–199

    Google Scholar 

  8. Armstrong SK, Gross R (2007) Metabolism and physiology of Bordetella species. In: Locht C (ed) Bordetella: molecular microbiology. Horizon Scientific Press, Norfolk, UK, pp 165–190

    Google Scholar 

  9. Shrivastava R, Miller JF (2009) Virulence factor secretion and translocation by Bordetella species. Curr Opin Microbiol 12:88–93

    Article  PubMed  CAS  Google Scholar 

  10. Cummings CA, Bootsma HJ, Relman DA, Miller JF (2006) Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J Bacteriol 188:1775–1785

    Article  PubMed  CAS  Google Scholar 

  11. Aricò B, Rappuoli R (1987) Bordetella parapertussis and Bordetella bronchiseptica contain transcriptionally silent pertussis toxin genes. J Bacteriol 169:2847–2853

    PubMed  Google Scholar 

  12. Beier D, Gross R (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9:143–152

    Article  PubMed  CAS  Google Scholar 

  13. Beier D, Gross R (2008) The BvgS/BvgA phosphor lay system of pathogenic Bordetellae: structure, function and evolution. Adv Exp Med Biol 631:149–160

    Article  PubMed  CAS  Google Scholar 

  14. Cotter PA, Jones AM (2003) Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol 11:367–373

    Article  PubMed  CAS  Google Scholar 

  15. Aricó B, Miller JF, Roy C, Stibitz S, Monack D, Falkow S, Gross R, Rappuoli R (1989) Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci USA 86:6671–6675

    Article  PubMed  Google Scholar 

  16. Bock A, Gross R (2002) The unorthodox histidine kinases BvgS and EvgS are responsive to the oxidation status of a quinone electron carrier. Eur J Biochem 269:3479–3484

    Article  PubMed  CAS  Google Scholar 

  17. Harrington AT, Castellanos JA, Ziedalski TM, Clarridge JE 3rd, Cookson BT (2009) Isolation of Bordetella avium and novel Bordetella strain from patients with respiratory disease. Emerg Infect Dis 15:72–74

    Article  PubMed  Google Scholar 

  18. Spilker T, Liwienski AA, LiPuma JJ (2008) Identification of Bordetella spp. in respiratory specimens from individuals with cystic fibrosis. Clin Microbiol Infect 14:504–506

    Article  PubMed  CAS  Google Scholar 

  19. Sebaihia M, Preston A, Maskell DJ, Kuzmiak H, Connell TD, King ND, Orndorff PE, Miyamoto DM, Thomson NR, Harris D, Goble A, Lord A, Murphy L, Quail MA, Rutter S, Squares R, Squares S, Woodward J, Parkhill J, Temple LM (2006) Comparison of the genome sequence of the poultry pathogen Bordetella avium with those of B. bronchiseptica, B. pertussis, and B. parapertussis reveals extensive diversity in surface structures associated with host interaction. J Bacteriol 188:6002–6015

    Article  PubMed  CAS  Google Scholar 

  20. Vandamme P, Hommez J, Vancanneyt M, Monsieurs M, Hoste B, Cookson B, Wirsing von König CH, Kersters K, Blackall PJ (1995) Bordetella hinzii sp. nov., isolated from poultry and humans. Int J Syst Bacteriol 45:37–45

    Article  PubMed  CAS  Google Scholar 

  21. Register KB, Sacco RE, Nordholm GE (2003) Comparison of ribotyping and restriction enzyme analysis for inter- and intraspecies discrimination of Bordetella avium and Bordetella hinzii. J Clin Microbiol 41:1512–1519

    Article  PubMed  CAS  Google Scholar 

  22. Register KB, Kunkle RA (2009) Strain-specific virulence of Bordetella hinzii in poultry. Avian Dis 53:50–54

    Article  PubMed  Google Scholar 

  23. Cookson BT, Vandamme P, Carlson LC, Larson AM, Sheffield JV, Kersters K, Spach DH (1994) Bacteremia caused by a novel Bordetella species, “B. hinzii”. J Clin Microbiol 32:2569–2571

    PubMed  CAS  Google Scholar 

  24. Degand N, Carbonnelle E, Dauphin B, Beretti JL, Le Bourgeois M, Sermet-Gaudelus I, Segonds C, Berche P, Nassif X, Ferroni A (2008) Matrix-assisted laser desorption ionization-time of flight mass spectrometry for identification of nonfermenting gram-negative bacilli isolated from cystic fibrosis patients. J Clin Microbiol 46:3361–3367

    Article  PubMed  CAS  Google Scholar 

  25. Hristov AC, Auwaerter PG, Romagnoli M, Carroll KC (2008) Bordetella hinzii septicemia in association with Epstein-Barr virus viremia and an Epstein-Barr virus-associated diffuse large B-cell lymphoma. Diagn Microbiol Infect Dis 61:484–486

    Article  PubMed  CAS  Google Scholar 

  26. Fry NK, Duncan J, Edwards MT, Tilley RE, Chitnavis D, Harman R, Hammerton H, Dainton L (2007) A UK clinical isolate of Bordetella hinzii from a patient with myelodysplastic syndrome. J Med Microbiol 56:1700–1703

    Article  PubMed  Google Scholar 

  27. Hayashimoto N, Yasuda M, Goto K, Takakura A, Itoh T (2008) Study of a Bordetella hinzii isolate from a laboratory mouse. Comp Med 58:440–446

    PubMed  CAS  Google Scholar 

  28. Gerlach G, Janzen S, Beier D, Gross R (2004) Functional characterization of the BvgAS two-component system of Bordetella holmesii. Microbiology 150:3715–3729

    Article  PubMed  CAS  Google Scholar 

  29. Donato GM, Hsia HL, Green CS, Hewlett E (2005) Adenylate cyclase toxin (ACT) from Bordetella hinzii: characterization and differences from ACT of Bordetella pertussis. J Bacteriol 187:7579–7588

    Article  PubMed  CAS  Google Scholar 

  30. Tang YW, Hopkins MK, Kolbert CP, Hartley PA, Severance PJ, Persing DH (1998) Bordetella holmesii-like organisms associated with septicemia, endocarditis, and respiratory failure. Clin Infect Dis 26(2):389–392

    Article  PubMed  CAS  Google Scholar 

  31. Weyant RS, Hollis DG, Weaver RE, Amin MF, Steigerwalt AG, O’Connor SP, Whitney AM, Daneshvar MI, Moss CW, Brenner DJ (1995) Bordetella holmesii sp.nov., a new gram-negative species associated with septicemia. J Clin Microbiol 33:1–7

    PubMed  CAS  Google Scholar 

  32. Mazengia E, Silva EA, Peppe JA, Timperi R, George H (2000) Recovery of Bordetella holmesii from patients with pertussis-like symptoms: use of pulsed-field gel electrophoresis to characterize circulating strains. J Clin Microbiol 38:2330–2333

    PubMed  CAS  Google Scholar 

  33. Yih WK, Silva EA, Ida J, Harrington N, Lett SM, George H (1999) Bordetella holmesii-like organisms isolated from Massachusetts patients with pertussis-like symptoms. Emerg Infect Dis 5:441–443

    Article  PubMed  CAS  Google Scholar 

  34. Antila M, He Q, de Jong C, Aarts I, Verbakel H, Bruisten S, Keller S, Haanperä M, Mäkinen J, Eerola E, Viljanen MK, Mertsola J, van der Zee A (2006) Bordetella holmesii DNA is not detected in nasopharyngeal swabs from Finnish and Dutch patients with suspected pertussis. J Med Microbiol 55:1043–1051

    Article  PubMed  CAS  Google Scholar 

  35. Njamkepo E, Delisle F, Hagege I, Gerbaud G, Guiso N (2000) Bordetella holmesii isolated from a patient with sickle cell anemia: analysis and comparison with other Bordetella holmesii isolates. Clin Microbiol Infect 6:131–136

    Article  PubMed  CAS  Google Scholar 

  36. Shepard CW, Daneshvar MI, Kaiser RM, Ashford DA, Lonsway D, Patel JB, Morey RE, Jordan JG, Weyant RS, Fischer M (2004) Bordetella holmesii bacteremia: a newly recognized clinical entity among asplenic patients. Clin Infect Dis 38:799–804

    Article  PubMed  Google Scholar 

  37. McCavit TL, Grube S, Revell P, Quinn CT (2008) Bordetella holmesii bacteremia in sickle cell disease. Pediatr Blood Cancer 51:814–816

    Article  PubMed  Google Scholar 

  38. Monnier S, Therby A, Couzon B, Doucet-Populaire F, Greder-Belan A (2009) Bordetella holmesii bacteremia in a 26-year-old patient with sickle cell disease. Med Mal Infect. doi:10.1016/j.medmal.2009.06.002

  39. Loeffelholz MJ, Thompson CJ, Long KS, Gilchrist MJ (2000) Detection of Bordetella holmesii using Bordetella pertussis IS481 PCR assay. J Clin Microbiol 38:467

    PubMed  CAS  Google Scholar 

  40. Probert WS, Ely J, Schrader K, Atwell J, Nossoff A, Kwan S (2008) Identification and evaluation of new target sequences for specific detection of Bordetella pertussis by real-time PCR. J Clin Microbiol 46:3228–3231

    Article  PubMed  CAS  Google Scholar 

  41. Tatti KM, Wu KH, Tondella ML, Cassiday PK, Cortese MM, Wilkins PP, Sanden GN (2008) Development and evaluation of dual-target real-time polymerase chain reaction assays to detect Bordetella spp. Diagn Microbiol Infect Dis 61:264–272

    Article  PubMed  CAS  Google Scholar 

  42. Muyldermans G, Soetens O, Antoine M, Bruisten S, Vincart B, Doucet-Populaire F, Fry NK, Olcén P, Scheftel JM, Senterre JM, van der Zee A, Riffelmann M, Piérard D, Lauwers S (2005) External quality assessment for molecular detection of Bordetella pertussis in European laboratories. J Clin Microbiol 43:30–35

    Article  PubMed  CAS  Google Scholar 

  43. Vielemeyer O, Crouch JY, Edberg SC, Howe JG (2004) Identification of Bordetella pertussis in a critically ill human immunodeficiency virus-infected patient by direct genotypical analysis of Gram-stained material and discrimination from B. holmesii by using a unique recA gene restriction enzyme site. J Clin Microbiol 42:847–849

    Article  PubMed  CAS  Google Scholar 

  44. Reischl U, Lehn N, Sanden GN, Loeffelholz MJ (2001) Real-time PCR assay targeting IS481 of Bordetella pertussis and molecular basis for detecting Bordetella holmesii. J Clin Microbiol 39:1963–1966

    Article  PubMed  CAS  Google Scholar 

  45. Diavatopoulos DA, Cummings CA, van der Heide HG, van Gent M, Liew S, Relman DA, Mooi FR (2006) Characterization of a highly conserved island in the otherwise divergent Bordetella holmesii and Bordetella pertussis genomes. J Bacteriol 188:8385–8394

    Article  PubMed  CAS  Google Scholar 

  46. Brickman TJ, Hanawa T, Anderson MT, Suhadolc RJ, Armstrong SK (2008) Differential expression of Bordetella pertussis iron transport system genes during infection. Mol Microbiol 70:3–14

    Article  PubMed  CAS  Google Scholar 

  47. Register KB, Ducey TF, Brockmeier SL, Dyer DW (2001) Reduced virulence of a Bordetella bronchiseptica siderophore mutant in neonatal swine. Infect Immun 69:2137–2143

    Article  PubMed  CAS  Google Scholar 

  48. Link S, Schmitt K, Beier D, Gross R (2007) Identification and regulation of expression of a gene encoding a filamentous hemagglutinin-related protein in Bordetella holmesii. BMC Microbiol 7:100

    Article  PubMed  Google Scholar 

  49. Merkel TJ, Boucher PE, Stibitz S, Grippe VK (2003) Analysis of bvgR expression in Bordetella pertussis. J Bacteriol 185:6902–6912

    Article  PubMed  CAS  Google Scholar 

  50. Monack DM, Arico B, Rappuoli R, Falkow S (1989) Phase variants of Bordetella bronchiseptica arise by spontaneous deletions in the vir locus. Mol Microbiol 3:1719–1728

    Article  PubMed  CAS  Google Scholar 

  51. Boucher PE, Maris AE, Yang MS, Stibitz S (2003) The response regulator BvgA and RNA polymerase alpha subunit C-terminal domain bind simultaneously to different faces of the same segment of promoter DNA. Mol Cell 11:163–173

    Article  PubMed  CAS  Google Scholar 

  52. Horvat A, Gross R (2009) Molecular characterization of the BvgA response regulator of Bordetella holmesii. Microbiol Res 164:243–252

    Article  PubMed  CAS  Google Scholar 

  53. Hodak H, Jacob-Dubuisson F (2007) Current challenges in auto transport and two-partner protein secretion pathways. Res Microbiol 158:631–637

    Article  PubMed  CAS  Google Scholar 

  54. Vandamme P, Heyndrickx M, Vancanneyt M, Hoste B, De Vos P, Falsen E, Kersters K, Hinz KH (1996) Bordetella trematum sp. nov., isolated from wounds and ear infections in humans, and reassessment of Alcaligenes denitrificans Rüger and Tan 1983. Int J Syst Bacteriol 46:849–858

    Article  PubMed  CAS  Google Scholar 

  55. Daxboeck F, Goerzer E, Apfalter P, Nehr M, Krause R (2004) Isolation of Bordetella trematum from a diabetic leg ulcer. Diabet Med 21:1247–1248

    Article  PubMed  CAS  Google Scholar 

  56. Ko KS, Peck KR, Oh WS, Lee NY, Lee JH, Song JH (2005) New species of Bordetella, Bordetella ansorpii sp. nov., isolated from the purulent exudate of an epidermal cyst. J Clin Microbiol 43:2516–2519

    Article  PubMed  CAS  Google Scholar 

  57. Fry NK, Duncan J, Malnick H, Cockcroft PM (2007) The first UK isolate of ‘Bordetella ansorpii’ from an immunocompromised patient. J Med Microbiol 56:993–995

    Article  PubMed  CAS  Google Scholar 

  58. von Wintzingerode F, Schattke A, Siddiqui RA, Rösick U, Göbel UB, Gross R (2001) Bordetella petrii sp. nov., isolated from an anaerobic bioreactor, and emended description of the genus Bordetella. Int J Syst Evol Microbiol 51:1257–1265

    Google Scholar 

  59. Bianchi F, Careri M, Mustat L, Malcevschi A, Musci M (2005) Bioremediation of toluene and naphthalene: development and validation of a GC-FID method for their monitoring. Ann Chim 95:515–524

    Article  PubMed  CAS  Google Scholar 

  60. Wang F, Grundmann S, Schmid M, Dörfler U, Roherer S, Charles Munch J, Hartmann A, Jiang X, Schroll R (2007) Isolation and characterization of 1, 2, 4-trichlorobenzene mineralizing Bordetella sp. and its bioremediation potential in soil. Chemosphere 67:896–902

    Article  PubMed  CAS  Google Scholar 

  61. Yuan SY, Su LM, Chang BV (2009) Biodegradation of phenanthrene and pyrene in compost-amended soil. J Environ Sci Health A Tox Hazard Subst Environ Eng 44:648–653

    PubMed  CAS  Google Scholar 

  62. Chowdhury SP, Schmid M, Hartmann A, Tripathi AK (2007) Identification of diazotrophs in the culturable bacterial community associated with roots of Lasiurus sindicus, a perennial grass of Thar Desert, India. Microb Ecol 54:82–90

    Article  PubMed  Google Scholar 

  63. Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P, Lopez J (2005) A molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 28:242–264

    Article  PubMed  CAS  Google Scholar 

  64. Fry NK, Duncan J, Malnick H, Warner M, Smith AJ, Jackson MS, Ayoub A (2005) Bordetella petrii clinical isolate. Emerg Infect Dis 11:1131–1133

    PubMed  Google Scholar 

  65. Stark D, Riley LA, Harkness J, Marriott D (2007) Bordetella petrii from a clinical sample in Australia: isolation and molecular identification. J Med Microbiol 56:435–437

    Article  PubMed  CAS  Google Scholar 

  66. Moissenet D, Bingen E, Arlet G, Vu-Thien H (2005) Use of 16S rRNA gene sequencing for identification of “Pseudomonas-like” isolates from sputum of patients with cystic fibrosis. Pathol Biol (Paris) 53:500–502

    CAS  Google Scholar 

  67. Gross R, Guzman CA, Sebaihia M, dos Santos VA, Pieper DH, Koebnik R, Lechner M, Bartels D, Buhrmester J, Choudhuri JV, Ebensen T, Gaigalat L, Herrmann S, Khachane AN, Larisch C, Link S, Linke B, Meyer F, Mormann S, Nakunst D, Rückert C, Schneiker-Bekel S, Schulze K, Vorhölter FJ, Yevsa T, Engle JT, Goldman WE, Pühler A, Göbel UB, Goesmann A, Blöcker H, Kaiser O, Martinez-Arias R (2008) The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 9:449

    Article  PubMed  Google Scholar 

  68. Cotter PA, DiRita VJ (2000) Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54:519–565

    Article  PubMed  CAS  Google Scholar 

  69. van der Meer JR, Sentchilo V (2003) Genomic islands and the evolution of catabolic pathways in bacteria. Curr Opin Biotechnol 14:248–254

    Article  PubMed  Google Scholar 

  70. Lechner M, Schmitt K, Bauer S, Hot D, Hubans C, Levillain E, Locht C, Lemoine Y, Gross R (2009) Genomic island excisions in Bordetella petrii. BMC Microbiol 9:141

    Article  PubMed  Google Scholar 

  71. Almuzara M, Limansky A, Ballerini V, Galanternik L, Famiglietti A, Vay C (2010) In vitro susceptibility of Achromobacter spp. isolates: comparison of disk diffusion, Etest and agar dilution methods. Int J Antimicrob Agents 35:68–71

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dagmar Beier for critically reading of the manuscript. Work of the authors was supported by the Deutsche Forschungsgemeinschaft through Sonderforschungsbereich 479.

Author information

Authors and Affiliations

  1. Lehrstuhl für Mikrobiologie, Biozentrum, Universität Würzburg, Am Hubland, D-97074, Würzburg, Germany

    Roy Gross, Kristina Keidel & Karin Schmitt

Authors
  1. Roy Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristina Keidel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin Schmitt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roy Gross.

Additional information

This article is published as part of a Special Issue on Pathogen Variation and Host Response in Infectious Disease.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gross, R., Keidel, K. & Schmitt, K. Resemblance and divergence: the “new” members of the genus Bordetella . Med Microbiol Immunol 199, 155–163 (2010). https://doi.org/10.1007/s00430-010-0148-z

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00430-010-0148-z

Keywords

Search

Navigation