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

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.

[1]  K. Krogfelt,et al.  Type 1 Fimbriae of Escherichia coli , 2020 .

[2]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[3]  T. Whittam,et al.  Clonal relationships among bloodstream isolates of Escherichia coli , 1995, Infection and immunity.

[4]  P. Klemm.  Fimbriae Adhesion, Genetics, Biogenesis, and Vaccines , 1994 .

[5]  R. Marre,et al.  Reciprocal exchange of minor components of type 1 and F1C fimbriae results in hybrid organelles with changed receptor specificities , 1994, Journal of bacteriology.

[6]  S. Clegg,et al.  Type 1 fimbrial shafts of Escherichia coli and Klebsiella pneumoniae influence sugar-binding specificities of their FimH adhesins , 1994, Infection and immunity.

[7]  I. Ofek,et al.  Bacterial Adhesion to Cells and Tissues , 1994, Springer US.

[8]  E. Sokurenko,et al.  FimH family of type 1 fimbrial adhesins: functional heterogeneity due to minor sequence variations among fimH genes , 1994, Journal of bacteriology.

[9]  S. Hultgren,et al.  Neutrophil activation by nascent FimH subunits of type 1 fimbriae purified from the periplasm of Escherichia coli. , 1993, The Journal of biological chemistry.

[10]  A. Siitonen.  Escherichia coli in fecal flora of healthy adults: serotypes, P and type 1C fimbriae, non-P mannose-resistant adhesins, and hemolytic activity. , 1992, The Journal of infectious diseases.

[11]  M. S. McClain,et al.  Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli , 1991, Journal of bacteriology.

[12]  M. S. McClain,et al.  Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants , 1991, Molecular microbiology.

[13]  S. Harris,et al.  Isolation and characterization of mutants with lesions affecting pellicle formation and erythrocyte agglutination by type 1 piliated Escherichia coli , 1990, Journal of bacteriology.

[14]  S. Hull,et al.  Frequency and organization of pap homologous DNA in relation to clinical origin of uropathogenic Escherichia coli. , 1990, The Journal of infectious diseases.

[15]  P. Klemm,et al.  Regulation of the phase switch controlling expression of type 1 fimbriae in Escherichia coli , 1989, Molecular microbiology.

[16]  S. Mårild,et al.  Special virulence of the Escherichia coli O1:K1:H7 clone in acute pyelonephritis. , 1989, The Journal of pediatrics.

[17]  B. Levin,et al.  Distribution of the P-associated-pilus (pap) region among Escherichia coli from natural sources: evidence for horizontal gene transfer , 1989, Infection and immunity.

[18]  E. Beachey,et al.  Conservation of the D-mannose-adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae , 1988, Nature.

[19]  M. Hanson,et al.  Purification of the Escherichia coli type 1 pilin and minor pilus proteins and partial characterization of the adhesin protein , 1988, Journal of bacteriology.

[20]  E. Beachey,et al.  Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products , 1987, Journal of bacteriology.

[21]  N. Firon,et al.  Aromatic alpha-glycosides of mannose are powerful inhibitors of the adherence of type 1 fimbriated Escherichia coli to yeast and intestinal epithelial cells , 1987, Infection and immunity.

[22]  L. Maurer,et al.  Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili , 1987, Journal of bacteriology.

[23]  E. Beachey,et al.  The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit , 1986, Journal of bacteriology.

[24]  J. Abraham,et al.  An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[25]  S. Falkow,et al.  Organization and expression of genes responsible for type 1 piliation in Escherichia coli , 1984, Journal of bacteriology.

[26]  R. Gibbons.  Microbial Ecology Adherent Interactions Which May Affect Microbial Ecology in the Mouth , 1984, Journal of dental research.

[27]  N. Firon,et al.  Carbohydrate specificity of the surface lectins of Escherichia coli, Klebsiella pneumoniae, and Salmonella typhimurium. , 1983, Carbohydrate research.

[28]  S. Falkow,et al.  Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate , 1981, Infection and immunity.

[29]  E. Beachey,et al.  Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. , 1981, The Journal of infectious diseases.

[30]  E. Beachey,et al.  Mannose Binding and Epithelial Cell Adherence of Escherichia coli , 1978, Infection and immunity.

[31]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[32]  N. Sharon,et al.  Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors , 1977, Nature.

[33]  D. Old.  Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. , 1972, Journal of general microbiology.

[34]  C. Brinton.  The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. , 1965, Transactions of the New York Academy of Sciences.

[35]  I. Smith,et al.  Non-flagellar filamentous appendages (fimbriae) and haemagglutinating activity in Bacterium coli. , 1955, The Journal of pathology and bacteriology.

[36]  D. Hasty,et al.  [41] Bacterial adhesion measured by growth of adherent organisms , 1995 .

[37]  K. Krogfelt,et al.  Escherichia coli F-18 phase locked 'on' for expression of type 1 fimbriae is a poor colonizer of the streptomycin-treated mouse large intestine. , 1993, Microbial pathogenesis.

[38]  Jeffrey H. Miller.  Experiments in molecular genetics , 1972 .