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Volume 63, Issue 7

Characterization of 17 chaperone-usher fimbriae encoded by reveals strong conservation Free

Abstract

is a Gram-negative enteric bacterium that causes complicated urinary tract infections, particularly in patients with indwelling catheters. Sequencing of clinical isolate HI4320 revealed the presence of 17 predicted chaperone-usher fimbrial operons. We classified these fimbriae into three groups by their genetic relationship to other chaperone-usher fimbriae. Sixteen of these fimbriae are encoded by all seven currently sequenced genomes. The predicted protein sequence of the major structural subunit for 14 of these fimbriae was highly conserved (≥95 % identity), whereas three other structural subunits (Fim3A, UcaA and Fim6A) were variable. Further examination of 58 clinical isolates showed that 14 of the 17 predicted major structural subunit genes of the fimbriae were present in most strains (>85 %). Transcription of the predicted major structural subunit genes for all 17 fimbriae was measured under different culture conditions designed to mimic conditions in the urinary tract. The majority of the fimbrial genes were induced during stationary phase, static culture or colony growth when compared to exponential-phase aerated culture. Major structural subunit proteins for six of these fimbriae were detected using MS of proteins sheared from the surface of broth-cultured , demonstrating that this organism may produce multiple fimbriae within a single culture. The high degree of conservation of fimbriae stands in contrast to uropathogenic and , which exhibit greater variability in their fimbrial repertoires. These findings suggest there may be evolutionary pressure for to maintain a large fimbrial arsenal.

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© 2014 The Authors
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2014-07-01
2024-04-23
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References

  1. Adegbola R. A., Old D. C., Senior B. W. 1983; The adhesins and fimbriae of Proteus mirabilis strains associated with high and low affinity for the urinary tract. J Med Microbiol 16:427–431 [View Article][PubMed]
     [Google Scholar]
  2. Alamuri P., Mobley H. L. 2008; A novel autotransporter of uropathogenic Proteus mirabilis is both a cytotoxin and an agglutinin. Mol Microbiol 68:997–1017 [View Article][PubMed]
     [Google Scholar]
  3. Alamuri P., Löwer M., Hiss J. A., Himpsl S. D., Schneider G., Mobley H. L. 2010; Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis. Infect Immun 78:4882–4894 [View Article][PubMed]
     [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [View Article][PubMed]
     [Google Scholar]
  5. Armbruster C. E., Mobley H. L. T. 2012; Merging mythology and morphology: the multifaceted lifestyle of Proteus mirabilis. Nat Rev Microbiol 10:743–754 [View Article][PubMed]
     [Google Scholar]
  6. Bahrani F. K., Mobley H. L. 1993; Proteus mirabilis MR/P fimbriae: molecular cloning, expression, and nucleotide sequence of the major fimbrial subunit gene. J Bacteriol 175:457–464[PubMed]
     [Google Scholar]
  7. Bahrani F. K., Mobley H. L. T. 1994; Proteus mirabilis MR/P fimbrial operon: genetic organization, nucleotide sequence, and conditions for expression. J Bacteriol 176:3412–3419[PubMed]
     [Google Scholar]
  8. Bahrani F. K., Cook S., Hull R. A., Massad G., Mobley H. L. 1993; Proteus mirabilis fimbriae: N-terminal amino acid sequence of a major fimbrial subunit and nucleotide sequences of the genes from two strains. Infect Immun 61:884–891[PubMed]
     [Google Scholar]
  9. Bahrani F. K., Massad G., Lockatell C. V., Johnson D. E., Russell R. G., Warren J. W., Mobley H. L. 1994; Construction of an MR/P fimbrial mutant of Proteus mirabilis: role in virulence in a mouse model of ascending urinary tract infection. Infect Immun 62:3363–3371[PubMed]
     [Google Scholar]
  10. Belas R., Erskine D., Flaherty D. 1991; Transposon mutagenesis in Proteus mirabilis. J Bacteriol 173:6289–6293[PubMed]
     [Google Scholar]
  11. Belas R., Schneider R., Melch M. 1998; Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J Bacteriol 180:6126–6139[PubMed]
     [Google Scholar]
  12. Bijlsma I. G. W., van Dijk L., Kusters J. G., Gaastra W. 1995; Nucleotide sequences of two fimbrial major subunit genes, pmpA and ucaA, from canine-uropathogenic Proteus mirabilis strains. Microbiology 141:1349–1357 [View Article][PubMed]
     [Google Scholar]
  13. Blomfield I. C., McClain M. S., Princ J. A., Calie P. J., Eisenstein B. I. 1991; Type 1 fimbriation and fimE mutants of Escherichia coli K-12. J Bacteriol 173:5298–5307[PubMed]
     [Google Scholar]
  14. Chaudhuri R. R., Loman N. J., Snyder L. A. S., Bailey C. M., Stekel D. J., Pallen M. J. 2008; xBASE2: a comprehensive resource for comparative bacterial genomics. Nucleic Acids Res 36:DatabaseD543–D546 [View Article][PubMed]
     [Google Scholar]
  15. Cook S. W., Mody N., Valle J., Hull R. 1995; Molecular cloning of Proteus mirabilis uroepithelial cell adherence (uca) genes. Infect Immun 63:2082–2086[PubMed]
     [Google Scholar]
  16. Cotto-Rios X. M., Békés M., Chapman J., Ueberheide B., Huang T. T. 2012; Deubiquitinases as a signaling target of oxidative stress. Cell Reports 2:1475–1484 [View Article][PubMed]
     [Google Scholar]
  17. DeFrances C. J., Lucas C. A., Buie V. C., Golosinskiy A. 2008 2006 National Hospital Discharge Survey National Health Statistics Reports, no. 5 Hyattsville, MD: National Center for Health Statistics;[PubMed]
     [Google Scholar]
  18. Foxman B. 2003; Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis Mon 49:53–70 [View Article][PubMed]
     [Google Scholar]
  19. Gaastra W., van Oosterom R. A., Pieters E. W., Bergmans H. E., van Dijk L., Agnes A., ter Huurne H. M. 1996; Isolation and characterisation of dog uropathogenic Proteus mirabilis strains. Vet Microbiol 48:57–71 [View Article][PubMed]
     [Google Scholar]
  20. Gibbs K. A., Urbanowski M. L., Greenberg E. P. 2008; Genetic determinants of self identity and social recognition in bacteria. Science 321:256–259 [View Article][PubMed]
     [Google Scholar]
  21. Griffith D. P., Musher D. M., Itin C. 1976; Urease. The primary cause of infection-induced urinary stones. Invest Urol 13:346–350[PubMed]
     [Google Scholar]
  22. Hannan T. J., Totsika M., Mansfield K. J., Moore K. H., Schembri M. A., Hultgren S. J. 2012; Host-pathogen checkpoints and population bottlenecks in persistent and intracellular uropathogenic Escherichia coli bladder infection. FEMS Microbiol Rev 36:616–648 [View Article][PubMed]
     [Google Scholar]
  23. Himpsl S. D., Lockatell C. V., Hebel J. R., Johnson D. E., Mobley H. L. 2008; Identification of virulence determinants in uropathogenic Proteus mirabilis using signature-tagged mutagenesis. J Med Microbiol 57:1068–1078 [View Article][PubMed]
     [Google Scholar]
  24. Hung D. L., Knight S. D., Woods R. M., Pinkner J. S., Hultgren S. J. 1996; Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15:3792–3805[PubMed]
     [Google Scholar]
  25. Jansen A. M., Lockatell V., Johnson D. E., Mobley H. L. 2004; Mannose-resistant Proteus-like fimbriae are produced by most Proteus mirabilis strains infecting the urinary tract, dictate the in vivo localization of bacteria, and contribute to biofilm formation. Infect Immun 72:7294–7305 [View Article][PubMed]
     [Google Scholar]
  26. Källenius G., Svenson S. B., Hultberg H., Möllby R., Helin I., Cedergren B., Winberg J. 1981; Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet 318:1369–1372 [View Article][PubMed]
     [Google Scholar]
  27. Khalid M. I. H., Teh L. K., Lee L. S., Zakaria Z. A., Salleh M. Z. 2013; Genome sequence of Proteus mirabilis strain PR03, isolated from a local hospital in Malaysia. Genome Announc 1:e00327-13 [View Article][PubMed]
     [Google Scholar]
  28. Klemm P., Christiansen G., Kreft B., Marre R., Bergmans H. 1994; Reciprocal exchange of minor components of type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities. J Bacteriol 176:2227–2234[PubMed]
     [Google Scholar]
  29. Klemm P., Jørgensen B. J., Kreft B., Christiansen G. 1995; The export systems of type 1 and F1C fimbriae are interchangeable but work in parental pairs. J Bacteriol 177:621–627[PubMed]
     [Google Scholar]
  30. Klevens R. M., Edwards J. R., Richards C. L. Jr, Horan T. C., Gaynes R. P., Pollock D. A., Cardo D. M. 2007; Estimating health care-associated infections and deaths in U.S. hospitals, 2002. Public Health Rep 122:160–166[PubMed]
     [Google Scholar]
  31. Lane M. C., Mobley H. L. 2007; Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72:19–25 [View Article][PubMed]
     [Google Scholar]
  32. Lane M. C., Li X., Pearson M. M., Simms A. N., Mobley H. L. 2009; Oxygen-limiting conditions enrich for fimbriate cells of uropathogenic Proteus mirabilis and Escherichia coli. J Bacteriol 191:1382–1392 [View Article][PubMed]
     [Google Scholar]
  33. Litwin M. S., Saigal C. S. 2007 Urologic Diseases in America Washington, D.C.: Government Printing Office;
     [Google Scholar]
  34. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ method. Methods 25:402–408 [View Article][PubMed]
     [Google Scholar]
  35. Massad G., Bahrani F. K., Mobley H. L. 1994a; Proteus mirabilis fimbriae: identification, isolation, and characterization of a new ambient-temperature fimbria. Infect Immun 62:1989–1994[PubMed]
     [Google Scholar]
  36. Massad G., Lockatell C. V., Johnson D. E., Mobley H. L. 1994b; Proteus mirabilis fimbriae: construction of an isogenic pmfA mutant and analysis of virulence in a CBA mouse model of ascending urinary tract infection. Infect Immun 62:536–542[PubMed]
     [Google Scholar]
  37. Massad G., Fulkerson J. F. Jr, Watson D. C., Mobley H. L. 1996; Proteus mirabilis ambient-temperature fimbriae: cloning and nucleotide sequence of the aft gene cluster. Infect Immun 64:4390–4395[PubMed]
     [Google Scholar]
  38. Mobley H. L., Island M. D., Hausinger R. P. 1995; Molecular biology of microbial ureases. Microbiol Rev 59:451–480[PubMed]
     [Google Scholar]
  39. Mobley H. L. T., Donnenberg M. S., Hagan E. C. 2009; Uropathogenic Escherichia coli. In EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology Edited by Böck A., Curtiss R. III, Kaper J. B., Karp P. D., Neidhardt F. C., Nyström T., Slauch J. M., Squires C. L., Ussery D. Washington, D.C.: American Society for Microbiology;
     [Google Scholar]
  40. Nielubowicz G. R., Mobley H. L. 2010; Host-pathogen interactions in urinary tract infection. Nat Rev Urol 7:430–441 [View Article][PubMed]
     [Google Scholar]
  41. Nuccio S. P., Bäumler A. J. 2007; Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71:551–575 [View Article][PubMed]
     [Google Scholar]
  42. O'Hara C. M., Brenner F. W., Miller J. M. 2000; Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev 13:534–546 [View Article][PubMed]
     [Google Scholar]
  43. Old D. C., Adegbola R. A. 1982; Haemagglutinins and fimbriae of Morganella, Proteus and Providencia. J Med Microbiol 15:551–564 [View Article][PubMed]
     [Google Scholar]
  44. Old D. C., Duguid J. P. 1970; Selective outgrowth of fimbriate bacteria in static liquid medium. J Bacteriol 103:447–456[PubMed]
     [Google Scholar]
  45. Pearson M. M., Mobley H. L. 2008; Repression of motility during fimbrial expression: identification of 14 mrpJ gene paralogues in Proteus mirabilis. Mol Microbiol 69:548–558 [View Article][PubMed]
     [Google Scholar]
  46. Pearson M. M., Sebaihia M., Churcher C., Quail M. A., Seshasayee A. S., Luscombe N. M., Abdellah Z., Arrosmith C., Atkin B.& other authors ( 2008; Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol 190:4027–4037 [View Article][PubMed]
     [Google Scholar]
  47. Pellegrino R., Scavone P., Umpiérrez A., Maskell D. J., Zunino P. 2013; Proteus mirabilis uroepithelial cell adhesin (UCA) fimbria plays a role in the colonization of the urinary tract. Pathog Dis 67:104–107 [View Article][PubMed]
     [Google Scholar]
  48. Roberts J. A., Fussell E. N., Kaack M. B. 1990; Bacterial adherence to urethral catheters. J Urol 144:264–269[PubMed]
     [Google Scholar]
  49. Schembri M. A., Klemm P. 2001; Biofilm formation in a hydrodynamic environment by novel fimh variants and ramifications for virulence. Infect Immun 69:1322–1328 [View Article][PubMed]
     [Google Scholar]
  50. Simerville J. A., Maxted W. C., Pahira J. J. 2005; Urinalysis: a comprehensive review. Am Fam Physician 71:1153–1162[PubMed]
     [Google Scholar]
  51. Sokurenko E. V., Courtney H. S., Maslow J., Siitonen A., Hasty D. L. 1995; Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes. J Bacteriol 177:3680–3686[PubMed]
     [Google Scholar]
  52. Sokurenko E. V., Chesnokova V., Doyle R. J., Hasty D. L. 1997; Diversity of the Escherichia coli type 1 fimbrial lectin. Differential binding to mannosides and uroepithelial cells. J Biol Chem 272:17880–17886 [View Article][PubMed]
     [Google Scholar]
  53. Sokurenko E. V., Chesnokova V., Dykhuizen D. E., Ofek I., Wu X. R., Krogfelt K. A., Struve C., Schembri M. A., Hasty D. L. 1998; Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci U S A 95:8922–8926 [View Article][PubMed]
     [Google Scholar]
  54. Spurbeck R. R., Stapleton A. E., Johnson J. R., Walk S. T., Hooton T. M., Mobley H. L. T. 2011; Fimbrial profiles predict virulence of uropathogenic Escherichia coli strains: contribution of Ygi and Yad fimbriae. Infect Immun 79:4753–4763 [View Article][PubMed]
     [Google Scholar]
  55. Sullivan N. L., Septer A. N., Fields A. T., Wenren L. M., Gibbs K. A. 2013; The complete genome sequence of Proteus mirabilis strain BB2000 reveals differences from the P. mirabilis reference strain. Genome Announc 1:e00024-13 [View Article][PubMed]
     [Google Scholar]
  56. Tambyah P. A. 2004; Catheter-associated urinary tract infections: diagnosis and prophylaxis. Int J Antimicrob Agents 24:Suppl. 1S44–S48 [View Article][PubMed]
     [Google Scholar]
  57. Tambyah P. A., Maki D. G. 2000; Catheter-associated urinary tract infection is rarely symptomatic: a prospective study of 1,497 catheterized patients. Arch Intern Med 160:678–682[PubMed]
     [Google Scholar]
  58. Tanabe M., Kanehisa M. 2012; Using the KEGG database resource. Curr Protoc Bioinformatics 38:1.12.1–1.12.43[PubMed]
     [Google Scholar]
  59. Tolson D. L., Barrigar D. L., McLean R. J., Altman E. 1995; Expression of a nonagglutinating fimbria by Proteus mirabilis. Infect Immun 63:1127–1129[PubMed]
     [Google Scholar]
  60. Townsend S. M., Kramer N. E., Edwards R., Baker S., Hamlin N., Simmonds M., Stevens K., Maloy S., Parkhill J.& other authors ( 2001; Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun 69:2894–2901 [View Article][PubMed]
     [Google Scholar]
  61. Warren J. W., Tenney J. H., Hoopes J. M., Muncie H. L., Anthony W. C. 1982; A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J Infect Dis 146:719–723 [View Article][PubMed]
     [Google Scholar]
  62. Wray S. K., Hull S. I., Cook R. G., Barrish J., Hull R. A. 1986; Identification and characterization of a uroepithelial cell adhesin from a uropathogenic isolate of Proteus mirabilis. Infect Immun 54:43–49[PubMed]
     [Google Scholar]
  63. Wurpel D. J., Beatson S. A., Totsika M., Petty N. K., Schembri M. A. 2013; Chaperone-usher fimbriae of Escherichia coli. PLoS ONE 8:e52835 [View Article][PubMed]
     [Google Scholar]
  64. Zunino P., Geymonat L., Allen A. G., Legnani-Fajardo C., Maskell D. J. 2000; Virulence of a Proteus mirabilis ATF isogenic mutant is not impaired in a mouse model of ascending urinary tract infection. FEMS Immunol Med Microbiol 29:137–143 [View Article][PubMed]
     [Google Scholar]
  65. Zunino P., Sosa V., Allen A. G., Preston A., Schlapp G., Maskell D. J. 2003; Proteus mirabilis fimbriae (PMF) are important for both bladder and kidney colonization in mice. Microbiology 149:3231–3237 [View Article][PubMed]
     [Google Scholar]
  66. Zunino P., Sosa V., Schlapp G., Allen A. G., Preston A., Maskell D. J. 2007; Mannose-resistant Proteus-like and P. mirabilis fimbriae have specific and additive roles in P. mirabilis urinary tract infections. FEMS Immunol Med Microbiol 51:125–133 [View Article][PubMed]
     [Google Scholar]
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Characterization of 17 chaperone-usher fimbriae encoded by Proteus mirabilis reveals strong conservation
J. Med. Microbiol. 63, 911 (2014); https://doi.org/10.1099/jmm.0.069971-0
/content/journal/jmm/10.1099/jmm.0.069971-0
/content/journal/jmm/10.1099/jmm.0.069971-0
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