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Volume 149, Issue 3

Phase variation in Free

Abstract

is a fastidious, Gram-negative bacterial pathogen of cats and humans. Previous workers have shown that serial passage leads to attenuation of virulence-associated attributes such as expression of pili, invasion of human epithelial cell lines and the stimulation of endothelial cell proliferation. In contrast to the published data, it was found that pilin expression is frequently preserved in organisms which have undergone phase variation . Transition from a slow-growing, dry agar-pitting (DAP) to a faster-growing, smooth non-agar-pitting (SNP) form appears to occur predictably and may reflect competition between two populations growing at different rates. Better survival of the slower-growing (DAP) form may explain its relatively easy retrieval from piliated SNP populations allowed to age on solid media. Pilin expression is associated with auto-agglutination in liquid suspension or broth cultures, and appears to be necessary but not sufficient for expression of the agar-pitting phenotype and for the formation of biofilms. Outer-membrane protein variation is seen in association with phase variation, but lipopolysaccharide expression is preserved in piliated as well as extensively passaged non-piliated isolates. The I/I infrequent restriction site-PCR fingerprint, which has been previously used to discriminate between serotypes Marseille and Houston, is shown to alter with phase variation , and there is evidence that genetic change accompanies these events. The extent of genetic and phenotypic variability of phase-variant has previously been underestimated. It may lead to new insights into the pathogenicity of this organism, and must be considered when interpreting data arising from such studies.

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  • Accepted:
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  • Published Online:
Keyword(s): AP-PCR, arbitrarily primed PCR , DAP, dry agar-pitting , ERIC-PCR, enterobacterial repetitive intergenic consensus PCR , IRS, infrequent restriction site , OMP, outer-membrane protein , S, subculture/passage and SNP, smooth non-agar-pitting
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2003-03-01
2024-04-24
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References

  1. Anderson B, Scotchlas D, Jones D, Johnson A, Tzianabos T., Baumstark B. 1997; Analysis of a 36-kilodalton protein (PapA) associated with the bacteriophage particle of Bartonella henselae . DNA Cell Biol 16:1223–1229
     [Google Scholar]
  2. Anderson B. E., Neuman M. A. 1997; Bartonella spp. as emerging human pathogens. Clin Microbiol Rev 10:203–219
     [Google Scholar]
  3. Anderson B. E, Goldsmith C, Johnson A, Padmalayam I., Baumstark B. 1994; Bacteriophage-like particle of Rochalimaea henselae . Mol Microbiol 13:67–73
     [Google Scholar]
  4. Arvand M, Wendt C, Regnath T, Ullrich R., Hahn H. 1998; Characterisation of Bartonella henselae isolated from bacillary angiomatosis lesions in a human immunodeficiency virus-infected patient in Germany. Clin Infect Dis 26:1296–1299
     [Google Scholar]
  5. Arvand M, Klose A. J, Schwartz-Porsche D, Hahn H., Wendt C. 2001; Genetic variability and prevalence of Bartonella henselae in cats in Berlin, Germany, and analysis of its genetic relatedness to a strain from Berlin that is pathogenic for humans. J Clin Microbiol 39:743–746
     [Google Scholar]
  6. Batterman H. J, Peek J. A, Loutit J. S, Falkow S., Tompkins L. S. 1995; Bartonella henselae and Bartonella quintana adherence to and entry into cultured human epithelial cells. Infect Immun 63:4553–4556
     [Google Scholar]
  7. Bergmans A. M. C, Schellekens J. F. P, van Embden J. D. A., Schouls L. M. 1996; Predominance of two Bartonella henselae variants among cat-scratch disease patients in the Netherlands. J Clin Microbiol 34:254–260
     [Google Scholar]
  8. Birtles R. J., Raoult D. 1996; Comparison of partial citrate synthase gene ( gltA ) sequences for phylogenetic analysis of Bartonella species. Int J Syst Bacteriol 46:891–897
     [Google Scholar]
  9. Branley J, Wolfson C, Waters P, Gottlieb T., Bradbury R. 1996; Prevalence of Bartonella henselae bacteraemia, the causative agent of cat-scratch disease, in an Australian cat population. Pathology 28:262–265
     [Google Scholar]
  10. Brayton K. A, Knowles D. P, McGuire T. C., Palmer G. H. 2001; Efficient use of a small genome to generate antigenic diversity in tick-borne ehrlichial pathogens. Proc Natl Acad Sci U S A 98:4130–4135
     [Google Scholar]
  11. Burgess A. W. O., Anderson B. E. 1998; Outer membrane proteins of Bartonella henselae and their interaction with human endothelial cells. Microb Pathog 25:157–164
     [Google Scholar]
  12. Chang C. C, Chomel B. B, Kasten R. W, Tappero J. W, Sanchez M. A., Koehler J. E. 2002; Molecular epidemiology of Bartonella henselae infection in human immunodeficiency virus-infected patients and their cat contacts, using pulsed-field gel electrophoresis and genotyping. J Infect Dis 186:1733–1739
     [Google Scholar]
  13. Chomel B. B, Abbott R. C, Kasten R. W, Floyd-Hawkins K. A, Kass P. H, Glasier C. A, Pedersen N. C., Koehler J. E. 1995; Bartonella henselae prevalence in domestic cats in California: risk factors and association between bacteremia and antibody titers. J Clin Microbiol 33:2445–2450
     [Google Scholar]
  14. Dehio C, Meyer M, Berger J, Schwarz H., Lanz C. 1997; Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 110:2141–2154
     [Google Scholar]
  15. Dillon B, Valenzuela J, Don R, Blanckenberg D, Wigney D. I, Malik R, Morris A. J, Robson J. M., Iredell J. 2002; Limited diversity within human isolates of Bartonella henselae . J Clin Microbiol 40:4691–4699
     [Google Scholar]
  16. Drancourt M, Birtles R, Chaumentin G, Vandenesch F, Etienne J., Raoult D. 1996; New serotype of Bartonella henselae in endocarditis and cat-scratch disease. Lancet 347:441–443
     [Google Scholar]
  17. Foley J. E, Chomel B, Kikuchi Y, Yamamoto K., Pedersen N. C. 1998; Seroprevalence of Bartonella henselae in cattery cats: association with cattery hygiene and flea infestation. Vet Quart 20:1–5
     [Google Scholar]
  18. Fumarola D, Pece S, Fumarulo R, Petruzzelli R, Greco B, Giuliani G, Maffione A. B., Jirillo E. 1994; Downregulation of human polymorphonuclear cell activities exerted by microorganisms belonging to the alpha-2 subgroup of Proteobacteria ( Afipia felis and Rochalimaea henselae ). Immunopharmacol Immunotoxicol 16:449–461
     [Google Scholar]
  19. Gally D. L, Bogan J. A, Eisenstein B. I., Blomfield I. C. 1993; Environmental regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12: effects of temperature and media. J Bacteriol 175:6186–6193
     [Google Scholar]
  20. Handley S. A., Regnery R. L. 2000; Differentiation of pathogenic Bartonella species by infrequent restriction site PCR. J Clin Microbiol 38:3010–3015
     [Google Scholar]
  21. Henderson I. R, Owen P., Nataro J. P. 1999; Molecular switches – the ON and OFF of bacterial phase variation. Mol Microbiol 33:919–932
     [Google Scholar]
  22. Hitchcock P. J., Brown T. M. 1983; Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154:269–277
     [Google Scholar]
  23. Jackson L. A, Perkins B. A., Wenger J. D. 1993; Cat scratch disease in the United States: an analysis of three national databases. Am J Public Health 83:1707–1711
     [Google Scholar]
  24. Joseph A. K, Wood C. W, Robson J. M, Paul S. L., Morris A. J. 1997; Bartonella henselae bacteraemia in domestic cats from Auckland. NZ Vet J 45:185–187
     [Google Scholar]
  25. Kempf V. A, Volkmann B, Schaller M, Sander C. A, Alitalo K, Riess T., Autenrieth I. B. 2001; Evidence of a leading role for VEGF in Bartonella henselae -induced endothelial cell proliferations. Cell Microbiol 3:623–632
     [Google Scholar]
  26. Koehler J. E, Glaser C. A., Tappero J. W. 1994; Rochalimaea henselae infection. A new zoonosis with the domestic cat as reservoir. JAMA 271:531–535
     [Google Scholar]
  27. La Scola B., Raoult D. 1999; Culture of Bartonella quintana and Bartonella henselae from human samples: a 5-year experience; (1993 to 1998 J Clin Microbiol 37:1899–1905
     [Google Scholar]
  28. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
     [Google Scholar]
  29. Lugtenberg B, Meijers J, Peters R, van der Hoek P., van Alphen L. 1975; Electrophoretic resolution of the ‘major outer membrane protein’ of Escherichia coli K12 into four bands. FEBS Lett 58:254–258
     [Google Scholar]
  30. Matar G. M, Swaminathan B, Hunter S. B, Slater L. N., Welch D. F. 1993; Polymerase chain reaction-based restriction fragment length polymorphism analysis of a fragment of the ribosomal operon from Rochalimaea species for subtyping. J Clin Microbiol 31:1730–1740
     [Google Scholar]
  31. Morona R, Macpherson D. F, Van Den Bosch L, Carlin N. I. A., Manning P. A. 1995; Lipopolysaccharide with an altered O-antigen produced in Escherichia coli K-12 harbouring mutated, cloned Shigella flexneri rfb genes. Mol Microbiol 18:209–223
     [Google Scholar]
  32. O'Reilly K. L, Bauer R. W, Freeland R. L, Foil L. D, Hughes K. J, Rohde K. R, Roy A. F, Stout R. W., Triche P. C. 1999; Acute clinical disease in cats following infection with a pathogenic strain of Bartonella henselae (LSU16). Infect Immun 67:3066–3072
     [Google Scholar]
  33. Pratt L. A., Kolter R. 1999; Genetic analyses of bacterial biofilm formation. Curr Opin Microbiol 2:598–603
     [Google Scholar]
  34. Prescott L. M, Harley J. P., Klein D. A. 1996; Isolation of pure cultures. In Microbiology pp  108–109 Boston, MD: WCB Publishers;
     [Google Scholar]
  35. Regnery R. L, Anderson B. E, Clarridge J. E. 3rd, Rodriguez-Barradas M. C, Jones D. C., Carr J. H. 1992; Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient. J Clin Microbiol 30:265–274
     [Google Scholar]
  36. Relman D. A. 1998; Are all Bartonella henselae strains created equal?. Clin Infect Dis 26:1300–1301
     [Google Scholar]
  37. Riffard S, Lo Presti F, Vandenesch F, Forey F, Reyrolle M., Etienne J. 1998; Comparative analysis of infrequent-restriction-site PCR and pulsed-field gel electrophoresis for epidemiological typing of Legionella pneumophila serogroup 1 strains. J Clin Microbiol 36:161–167
     [Google Scholar]
  38. Sander A, Ruess M, Bereswill S, Schuppler M., Steinbrueckner B. 1998; Comparison of different DNA fingerprinting techniques for molecular typing of Bartonella henselae isolates. J Clin Microbiol 36:2973–2981
     [Google Scholar]
  39. Sander A, Posselt M, Bohm N, Ruess M., Altwegg M. 1999; Detection of Bartonella henselae DNA by two different PCR assays and determination of the genotypes of strains involved in histologically defined cat scratch disease. J Clin Microbiol 37:993–997
     [Google Scholar]
  40. Schwartzman W. A, Nesbit C. A., Jo Baron E. 1993; Development and evaluation of a blood-free medium for determining growth curves and optimising growth of Rochalimaea henselae . J Clin Microbiol 31:1882–1885
     [Google Scholar]
  41. Slater L. N, Welch D. F, Hensel D., Coody D. 1990; A newly recognised fastidious gram-negative pathogen as a cause of fever and bacteremia. N Engl J Med 323:1587–1593
     [Google Scholar]
  42. Tennent J., Mattick J. S. 1994; Type 4 fimbriae. In Fimbriae: Aspects of Adhesion, Genetics, Biogenesis and Vaccines pp  2–93 Edited by Klemm P. Boca Raton, FL: CRC Press;
     [Google Scholar]
  43. Tsai C., Frasch C. E. 1982; A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119:115–119
     [Google Scholar]
  44. Voss E., Attridge S. R. 1993; In vitro production of toxin-coregulated pili by Vibrio cholerae El Tor. Microb Pathog 15:255–268
     [Google Scholar]
  45. Watnick P. I, Fullner K. J., Kolter R. 1999; A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 118:3606–3609
     [Google Scholar]
  46. Welch D. F, Pickett D. A, Slater L. N, Steigerwalt A. G., Brenner D. J. 1992; Rochalimaea henselae sp. nov., a cause of septicemia, bacillary angiomatosis, and parenchymal bacillary peliosis. J Clin Microbiol 30:275–280
     [Google Scholar]
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Phase variation in Bartonella henselae
Microbiology 149, 621 (2003); https://doi.org/10.1099/mic.0.26014-0
/content/journal/micro/10.1099/mic.0.26014-0
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