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. 1995 Jul;177(13):3680–3686. doi: 10.1128/jb.177.13.3680-3686.1995

Quantitative differences in adhesiveness of type 1 fimbriated Escherichia coli due to structural differences in fimH genes.

E V Sokurenko 1, H S Courtney 1, J Maslow 1, A Siitonen 1, D L Hasty 1
PMCID: PMC177083  PMID: 7601831

Abstract

Type 1 fimbriae are heteropolymeric surface organelles responsible for the D-mannose-sensitive (MS) adhesion of Escherichia coli. We recently reported that variation of receptor specificity of type 1 fimbriae can result solely from minor alterations in the structure of the gene for the FimH adhesin subunit. To further study the relationship between allelic variation of the fimH gene and adhesive properties of type 1 fimbriae, the fimH genes from five additional strains were cloned and used to complement the FimH deletion in E. coli KB18. When the parental and recombinant strains were tested for adhesion to immobilized mannan, a wide quantitative range in the ability of bacteria to adhere was noted. The differences in adhesion do not appear to be due to differences in the levels of fimbriation or relative levels of incorporation of FimH, because these parameters were similar in low-adhesion and high-adhesion strains. The nucleotide sequence for each of the fimH genes was determined. Analysis of deduced FimH sequences allowed identification of two sequence homology groups, based on the presence of Asn-70 and Ser-78 or Ser-70 and Asn-78 residues. The consensus sequences for each group conferred very low adhesion activity, and this low-adhesion phenotype predominated among a group of 43 fecal isolates. Strains isolated from a different host niche, the urinary tract, expressed type 1 fimbriae that conferred an increased level of adhesion. The results presented here strongly suggest that the quantitative variations in MS adhesion are due primarily to structural differences in the FimH adhesin. The observed differences in MS adhesion among populations of E. coli isolated from different host niches call attention to the possibility that phenotypic variants of FimH may play a functional role in populations dynamics.

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Selected References

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  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. Abraham S. N., Goguen J. D., Sun D., Klemm P., Beachey E. H. Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products. J Bacteriol. 1987 Dec;169(12):5530–5536. doi: 10.1128/jb.169.12.5530-5536.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Abraham S. N., Sun D., Dale J. B., Beachey E. H. Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature. 1988 Dec 15;336(6200):682–684. doi: 10.1038/336682a0. [DOI] [PubMed] [Google Scholar]
  4. BRINTON C. C., Jr Non-flagellar appendages of bacteria. Nature. 1959 Mar 21;183(4664):782–786. doi: 10.1038/183782a0. [DOI] [PubMed] [Google Scholar]
  5. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [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. 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]
  8. DUGUID J. P., SMITH I. W., DEMPSTER G., EDMUNDS P. N. Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. J Pathol Bacteriol. 1955 Oct;70(2):335–348. doi: 10.1002/path.1700700210. [DOI] [PubMed] [Google Scholar]
  9. Firon N., Ashkenazi S., Mirelman D., Ofek I., Sharon N. Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells. Infect Immun. 1987 Feb;55(2):472–476. doi: 10.1128/iai.55.2.472-476.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Firon N., Ofek I., Sharon N. Carbohydrate specificity of the surface lectins of Escherichia coli, Klebsiella pneumoniae, and Salmonella typhimurium. Carbohydr Res. 1983 Aug 16;120:235–249. doi: 10.1016/0008-6215(83)88019-7. [DOI] [PubMed] [Google Scholar]
  11. Gibbons R. J. Adherent interactions which may affect microbial ecology in the mouth. J Dent Res. 1984 Mar;63(3):378–385. doi: 10.1177/00220345840630030401. [DOI] [PubMed] [Google Scholar]
  12. Hanson M. S., Brinton C. C., Jr Identification and characterization of E. coli type-1 pilus tip adhesion protein. Nature. 1988 Mar 17;332(6161):265–268. doi: 10.1038/332265a0. [DOI] [PubMed] [Google Scholar]
  13. Hanson M. S., Hempel J., Brinton C. C., Jr Purification of the Escherichia coli type 1 pilin and minor pilus proteins and partial characterization of the adhesin protein. J Bacteriol. 1988 Aug;170(8):3350–3358. doi: 10.1128/jb.170.8.3350-3358.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harris S. L., Elliott D. A., Blake M. C., Must L. M., Messenger M., Orndorff P. E. Isolation and characterization of mutants with lesions affecting pellicle formation and erythrocyte agglutination by type 1 piliated Escherichia coli. J Bacteriol. 1990 Nov;172(11):6411–6418. doi: 10.1128/jb.172.11.6411-6418.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun. 1981 Sep;33(3):933–938. doi: 10.1128/iai.33.3.933-938.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Klemm P., Christiansen G., Kreft B., Marre R., Bergmans H. Reciprocal exchange of minor components of type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities. J Bacteriol. 1994 Apr;176(8):2227–2234. doi: 10.1128/jb.176.8.2227-2234.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Klemm P., Christiansen G. Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae. Mol Gen Genet. 1987 Jul;208(3):439–445. doi: 10.1007/BF00328136. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Krogfelt K. A., Bergmans H., Klemm P. Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae. Infect Immun. 1990 Jun;58(6):1995–1998. doi: 10.1128/iai.58.6.1995-1998.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Madison B., Ofek I., Clegg S., Abraham S. N. Type 1 fimbrial shafts of Escherichia coli and Klebsiella pneumoniae influence sugar-binding specificities of their FimH adhesins. Infect Immun. 1994 Mar;62(3):843–848. doi: 10.1128/iai.62.3.843-848.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Maslow J. N., Mulligan M. E., Adams K. S., Justis J. C., Arbeit R. D. Bacterial adhesins and host factors: role in the development and outcome of Escherichia coli bacteremia. Clin Infect Dis. 1993 Jul;17(1):89–97. doi: 10.1093/clinids/17.1.89. [DOI] [PubMed] [Google Scholar]
  22. Maurer L., Orndorff P. E. Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili. J Bacteriol. 1987 Feb;169(2):640–645. doi: 10.1128/jb.169.2.640-645.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. McCormick B. A., Klemm P., Krogfelt K. A., Burghoff R. L., Pallesen L., Laux D. C., Cohen P. S. Escherichia coli F-18 phase locked 'on' for expression of type 1 fimbriae is a poor colonizer of the streptomycin-treated mouse large intestine. Microb Pathog. 1993 Jan;14(1):33–43. doi: 10.1006/mpat.1993.1004. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Mårild S., Jodal U., Orskov I., Orskov F., Svanborg Edén C. Special virulence of the Escherichia coli O1:K1:H7 clone in acute pyelonephritis. J Pediatr. 1989 Jul;115(1):40–45. doi: 10.1016/s0022-3476(89)80326-9. [DOI] [PubMed] [Google Scholar]
  27. Ofek I., Beachey E. H. Mannose binding and epithelial cell adherence of Escherichia coli. Infect Immun. 1978 Oct;22(1):247–254. doi: 10.1128/iai.22.1.247-254.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ofek I., Mirelman D., Sharon N. Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature. 1977 Feb 17;265(5595):623–625. doi: 10.1038/265623a0. [DOI] [PubMed] [Google Scholar]
  29. Old D. C. Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol. 1972 Jun;71(1):149–157. doi: 10.1099/00221287-71-1-149. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. Pallesen L., Madsen O., Klemm P. Regulation of the phase switch controlling expression of type 1 fimbriae in Escherichia coli. Mol Microbiol. 1989 Jul;3(7):925–931. doi: 10.1111/j.1365-2958.1989.tb00242.x. [DOI] [PubMed] [Google Scholar]
  32. Plos K., Carter T., Hull S., Hull R., Svanborg Edén C. Frequency and organization of pap homologous DNA in relation to clinical origin of uropathogenic Escherichia coli. J Infect Dis. 1990 Mar;161(3):518–524. doi: 10.1093/infdis/161.3.518. [DOI] [PubMed] [Google Scholar]
  33. Plos K., Hull S. I., Hull R. A., Levin B. R., Orskov I., Orskov F., Svanborg-Edén C. Distribution of the P-associated-pilus (pap) region among Escherichia coli from natural sources: evidence for horizontal gene transfer. Infect Immun. 1989 May;57(5):1604–1611. doi: 10.1128/iai.57.5.1604-1611.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Siitonen A. Escherichia coli in fecal flora of healthy adults: serotypes, P and type 1C fimbriae, non-P mannose-resistant adhesins, and hemolytic activity. J Infect Dis. 1992 Nov;166(5):1058–1065. doi: 10.1093/infdis/166.5.1058. [DOI] [PubMed] [Google Scholar]
  36. Sokurenko E. V., Courtney H. S., Ohman D. E., Klemm P., Hasty D. L. FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes. J Bacteriol. 1994 Feb;176(3):748–755. doi: 10.1128/jb.176.3.748-755.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sokurenko E. V., McMackin V. A., Hasty D. L. Bacterial adhesion measured by growth of adherent organisms. Methods Enzymol. 1995;253:519–528. doi: 10.1016/s0076-6879(95)53043-6. [DOI] [PubMed] [Google Scholar]
  38. Tewari R., MacGregor J. I., Ikeda T., Little J. R., Hultgren S. J., Abraham S. N. Neutrophil activation by nascent FimH subunits of type 1 fimbriae purified from the periplasm of Escherichia coli. J Biol Chem. 1993 Feb 5;268(4):3009–3015. [PubMed] [Google Scholar]

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