Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Jun;65(6):2462–2467. doi: 10.1128/iai.65.6.2462-2467.1997

Characterization of Shigella type 1 fimbriae: expression, FimA sequence, and phase variation.

N J Snellings 1, B D Tall 1, M M Venkatesan 1
PMCID: PMC175344  PMID: 9169792

Abstract

This study documents the presence of type 1 fimbriae on Shigella and confirms these mannose-sensitive adherence structures to be bona fide components of the Shigella surface. While laboratory-passaged Shigella strains and lyophilized clinical isolates failed to express type 1 fimbriae, 6 of 20 recent clinical isolates, including 4 Shigella flexneri strains, 1 Shigella boydii strain, and 1 Shigella dysenteriae strain, produced type 1 fimbriae as detected by mannose-sensitive hemagglutination (MSHA) and electron microscopy. Optimal production of a predominantly Fim+ population required serial passage every 48 to 72 h in unshaken brain heart infusion broth at 37 degrees C. Fim+ Shigella cultures were capable of reversibly switching to a non-MSHA, afimbriated phase during serial aerobic cultivation on tryptic soy agar plates. The amino acid sequence of S. flexneri type 1 FimA contained 18 substitutions compared to that of Escherichia coli fimbrillin. Indirect immunoelectron microscopy suggested the presence of both shared and unique epitopes on E. coli and S. flexneri type 1 fimbriae. Random phase variation between fimbriated and afimbriated states in Shigella was accompanied by the genomic rearrangement associated with phase variation in E. coli.

Full Text

The Full Text of this article is available as a PDF (698.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abraham J. M., Freitag C. S., Clements J. R., Eisenstein B. I. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5724–5727. doi: 10.1073/pnas.82.17.5724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adegbola R. A., Old D. C. Antigenic relationships among type-1 fimbriae of Enterobacteriaceae revealed by immuno-electronmicroscopy. J Med Microbiol. 1987 Aug;24(1):21–28. doi: 10.1099/00222615-24-1-21. [DOI] [PubMed] [Google Scholar]
  3. Aronson M., Medalia O., Schori L., Mirelman D., Sharon N., Ofek I. Prevention of colonization of the urinary tract of mice with Escherichia coli by blocking of bacterial adherence with methyl alpha-D-mannopyranoside. J Infect Dis. 1979 Mar;139(3):329–332. doi: 10.1093/infdis/139.3.329. [DOI] [PubMed] [Google Scholar]
  4. Bloch C. A., Orndorff P. E. Impaired colonization by and full invasiveness of Escherichia coli K1 bearing a site-directed mutation in the type 1 pilin gene. Infect Immun. 1990 Jan;58(1):275–278. doi: 10.1128/iai.58.1.275-278.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bloch C. A., Stocker B. A., Orndorff P. E. A key role for type 1 pili in enterobacterial communicability. Mol Microbiol. 1992 Mar;6(6):697–701. doi: 10.1111/j.1365-2958.1992.tb01518.x. [DOI] [PubMed] [Google Scholar]
  6. Blomfield I. C., McClain M. S., Eisenstein B. I. Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants. Mol Microbiol. 1991 Jun;5(6):1439–1445. doi: 10.1111/j.1365-2958.1991.tb00790.x. [DOI] [PubMed] [Google Scholar]
  7. Blum G., Falbo V., Caprioli A., Hacker J. Gene clusters encoding the cytotoxic necrotizing factor type 1, Prs-fimbriae and alpha-hemolysin form the pathogenicity island II of the uropathogenic Escherichia coli strain J96. FEMS Microbiol Lett. 1995 Feb 15;126(2):189–195. doi: 10.1111/j.1574-6968.1995.tb07415.x. [DOI] [PubMed] [Google Scholar]
  8. Blyn L. B., Braaten B. A., White-Ziegler C. A., Rolfson D. H., Low D. A. Phase-variation of pyelonephritis-associated pili in Escherichia coli: evidence for transcriptional regulation. EMBO J. 1989 Feb;8(2):613–620. doi: 10.1002/j.1460-2075.1989.tb03416.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brinton C. C., Jr The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans N Y Acad Sci. 1965 Jun;27(8):1003–1054. doi: 10.1111/j.2164-0947.1965.tb02342.x. [DOI] [PubMed] [Google Scholar]
  10. Buchanan K., Falkow S., Hull R. A., Hull S. I. Frequency among Enterobacteriaceae of the DNA sequences encoding type 1 pili. J Bacteriol. 1985 May;162(2):799–803. doi: 10.1128/jb.162.2.799-803.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eisenstein B. I. Phase variation of type 1 fimbriae in Escherichia coli is under transcriptional control. Science. 1981 Oct 16;214(4518):337–339. doi: 10.1126/science.6116279. [DOI] [PubMed] [Google Scholar]
  12. Hagberg L., Jodal U., Korhonen T. K., Lidin-Janson G., Lindberg U., Svanborg Edén C. Adhesion, hemagglutination, and virulence of Escherichia coli causing urinary tract infections. Infect Immun. 1981 Feb;31(2):564–570. doi: 10.1128/iai.31.2.564-570.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hale T. L. Genetic basis of virulence in Shigella species. Microbiol Rev. 1991 Jun;55(2):206–224. doi: 10.1128/mr.55.2.206-224.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hultgren S. J., Porter T. N., Schaeffer A. J., Duncan J. L. Role of type 1 pili and effects of phase variation on lower urinary tract infections produced by Escherichia coli. Infect Immun. 1985 Nov;50(2):370–377. doi: 10.1128/iai.50.2.370-377.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson J. R. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991 Jan;4(1):80–128. doi: 10.1128/cmr.4.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Keith B. R., Maurer L., Spears P. A., Orndorff P. E. Receptor-binding function of type 1 pili effects bladder colonization by a clinical isolate of Escherichia coli. Infect Immun. 1986 Sep;53(3):693–696. doi: 10.1128/iai.53.3.693-696.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klemm P., Jørgensen B. J., van Die I., de Ree H., Bergmans H. The fim genes responsible for synthesis of type 1 fimbriae in Escherichia coli, cloning and genetic organization. Mol Gen Genet. 1985;199(3):410–414. doi: 10.1007/BF00330751. [DOI] [PubMed] [Google Scholar]
  18. McClain M. S., Blomfield I. C., Eisenstein B. I. Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli. J Bacteriol. 1991 Sep;173(17):5308–5314. doi: 10.1128/jb.173.17.5308-5314.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Minion F. C., Abraham S. N., Beachey E. H., Goguen J. D. The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit. J Bacteriol. 1986 Mar;165(3):1033–1036. doi: 10.1128/jb.165.3.1033-1036.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Orndorff P. E., Falkow S. Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J Bacteriol. 1984 Aug;159(2):736–744. doi: 10.1128/jb.159.2.736-744.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Orskov I., Ferencz A., Orskov F. Tamm-Horsfall protein or uromucoid is the normal urinary slime that traps type 1 fimbriated Escherichia coli. Lancet. 1980 Apr 19;1(8173):887–887. doi: 10.1016/s0140-6736(80)91396-3. [DOI] [PubMed] [Google Scholar]
  22. Orskov I., Orskov F. Serologic classification of fimbriae. Curr Top Microbiol Immunol. 1990;151:71–90. [PubMed] [Google Scholar]
  23. Ottow J. C. Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol. 1975;29:79–108. doi: 10.1146/annurev.mi.29.100175.000455. [DOI] [PubMed] [Google Scholar]
  24. Parsot C. Shigella flexneri: genetics of entry and intercellular dissemination in epithelial cells. Curr Top Microbiol Immunol. 1994;192:217–241. doi: 10.1007/978-3-642-78624-2_10. [DOI] [PubMed] [Google Scholar]
  25. Qadri F., Haq S., Ciznár I. Hemagglutinating properties of Shigella dysenteriae type 1 and other Shigella species. Infect Immun. 1989 Sep;57(9):2909–2911. doi: 10.1128/iai.57.9.2909-2911.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rahaman M. M., Khan M. M., Aziz K. M., Islam M. S., Kibriya A. K. An outbreak of dysentery caused by Shigella dysenteriae type 1 on a coral island in the Bay of Bengal. J Infect Dis. 1975 Jul;132(1):15–19. doi: 10.1093/infdis/132.1.15. [DOI] [PubMed] [Google Scholar]
  27. Sekizaki T., Ito H., Asawa T., Nonomura I. DNA sequence of type 1 fimbrin, Fpul1, gene from a chicken pathogenic Escherichia coli serotype O78. J Vet Med Sci. 1993 Jun;55(3):395–400. doi: 10.1292/jvms.55.395. [DOI] [PubMed] [Google Scholar]
  28. Utsunomiya A., Naito T., Ehara M., Ichinose Y., Hamamoto A. Studies on novel pili from Shigella flexneri. I. Detection of pili and hemagglutination activity. Microbiol Immunol. 1992;36(8):803–813. doi: 10.1111/j.1348-0421.1992.tb02082.x. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES