Skip to main content
SpringerLink
Log in

Functional and structural homology among regulatory cistrons of pili-adhesin determinants in Escherichia coli

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

Expression of the digalactoside-binding Pap pili involves two trans-acting regulatory genes, papB and papI. Using pap-lac operon fusions and DNA hybridization probes derived from pap DNA we tested whether or not other pili-adhesin determinants from different Escherichia coli strains encode homologs to the pap regulatory genes. Digalactoside-specific clones of serotypes F72 and F11 complemented papB and papI mutants of the Pap (serotype F13) clone and DNA hybridization analysis showed that the clones are homologous in the DNA sequences encoding the two regulatory genes. Similar results were obtained with an S-pili determinant which mediates binding to sialic acid-containing receptors and the findings suggest that the regulatory regions may be more conserved than other genes in different pili-adhesin gene clusters. Determinants for type 1-pili (mannose-specific binding) and for pili associated with enterotoxigenic E. coli (K88, K99, CFAI, CFAII) did not appear to contain DNA sequences homologous to papB or papI. E. coli strain J96, which was the origin of the pap DNA, was found to carry two additional copies of papB-papI homologous sequences in the chromosome. In strains expressing more than one kind of pili the trans-active gene products thereby may allow for regulatory interaction between separate pili-adhesin gene systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Båga M, Göransson M, Normark S, Uhlin BE (1985) Transcriptional activation of a Pap pilus virulence operon from uropathogenic Escherichia coli. EMBO J 4:3887–3893

    Google Scholar 

  • Båga M, Göransson M, Normark S, Uhlin BE (1988) Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell 52:197–206

    Google Scholar 

  • Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300

    Google Scholar 

  • Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW (1977) Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95–113

    Google Scholar 

  • Boyer HW, Roulland-Dussoix D (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41:459–472

    Google Scholar 

  • Brinton CC (1959) Non-flagellar appendages of bacteria. Nature 183:782–786

    Google Scholar 

  • Casadaban MJ, Cohen SN (1980) Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol 138:179–207

    Google Scholar 

  • Chang ACY, Cohen SN (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic plasmid. J Bacteriol 134:1141–1156

    Google Scholar 

  • Clegg S (1982) Cloning of genes determining the production of mannose-resistant fimbriae in a uropathogenic strain of Escherichia coli belonging to serogroup O6. Infect Immun 38:739–744

    Google Scholar 

  • Duguid JP, Smith W, Dempster G, Edmunds PN (1955) Non flagellar filamentous appendages (fimbriae) and hemagglutinating activity in bacterium coli. J Pathol Bacteriol 70:335–348

    Google Scholar 

  • Evans DG, Silver RP, Evans DJ Jr, Chase DG, Gorbach SL (1975) Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect Immun 12:656–667

    Google Scholar 

  • Gaastra W, Klemm P, De Graaf FK (1983) The nucleotide sequence of the K88ad protein subunit of porcine enterotoxigenic Escherichia coli. FEMS Microbiol Lett 18:177–183

    Google Scholar 

  • Göransson M, Uhlin BE (1984) Environmental temperature regulates transcription of a virulence pili operon in E. coli. EMBO J 3:2885–2888

    Google Scholar 

  • Hacker J, Schmidt G, Hughes C, Knapp S, Marget M, Goebel W (1985) Cloning and characterization of genes involved in production of mannose-resistant, neuraminidase-susceptible (X) fimbriae from a uropathogenic O6:K15:H31 Escherichia coli strain. Infect Immun 47:434–440

    Google Scholar 

  • Hull RA, Gill RE, Hsu P, Minshew BH, Falkow S (1981) Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun 33:933–938

    Google Scholar 

  • Hull S, Clegg S, Svanborg-Edén C, Hull R (1985) Multiple forms of genes in pyelonephritogenic Escherichia coli encoding adhesins binding globoseries glycolipid receptors. Infect Immun 47:80–83

    Google Scholar 

  • Hull R, Bieler S, Falkow S, Hull S (1986) Chromosomal map position of genes encoding P adhesins in uropathogenic Escherichia coli. Infect Immun 51:693–695

    Google Scholar 

  • Klemm P (1986) Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J 5:1389–1393

    Google Scholar 

  • Klemm P, Orskov I, Orskov F (1982) F7 and type 1-like fimbriae from three Escherichia coli strains isolated from urinary tract infections: Protein chemical and immunological aspects. Infect Immun 36:462–468

    Google Scholar 

  • Lindahl M, Faris A, Wadström T, Hjerten S (1981) A new test based on “salting out” to measure relative hydrophobicity of bacterial cells. Biochim Biophys Acta 677:471–476

    Google Scholar 

  • Lund B, Lindberg FP, Båga M, Normark S (1985) Globosidespecific adhesions of uropathogenic Escherichia coli are encoded by similar trans-complementable gene clusters. J Bacteriol 162:1293–1301

    Google Scholar 

  • Lund B, Lindberg F, Marklund B-I, Normark S (1987) The PapG protein is the α-D-galactopyranosyl-(1–4)-β-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci UsA 84:5898–5902

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Miller J (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Mooi FR, DeGraaf FK (1985) Molecular biology of fimbriae of enterotoxigenic Escherichia coli. Curr Top Microbiol Immunol 118:119–138

    Google Scholar 

  • Norgren M, Normark S, Lark D, O'Hanley P, Schoolnik G, Falkow S, Svanborg-Edén C, Båga M, Uhlin BE (1984) Mutations in E. coli cistrons affecting adhesion to human cells do not abolish Pap pili fiber formation. EMBO J 3:1159–1165

    Google Scholar 

  • Normark S, Båga M, Göransson M, Lindberg FP, Lund B, Norgren M, Uhlin BE (1986) Genetics and biogenesis of Escherichia coli adhesins. In: Mirelman D (ed) Microbial lectins and agglutinins: Properties and biological activity. John Wiley and Sons, New York, pp 113–143

    Google Scholar 

  • Orndorff PE, Falkow S (1984) Organization and expression of genes responsible for type 1 piliation in Escherichia coli. J Bacteriol 159:736–744

    Google Scholar 

  • Ott M, Schmoll T, Goebel W, Van Die I, Hacker J (1987) Comparison of the genetic determinant coding for the S-fimbrial adhesin (sfa) of Escherichia coli to other chromosomally encoded fimbrial determinants. Infect Immun 55:1940–1943

    Google Scholar 

  • Rhen M, Knowles J, Penttilä ME, Sarvas M, Korhonen TK (1983) P fimbriae of Escherichia coli: Molecular cloning of DNA fragments containing the structural genes. FEMS Microbiol Lett 19:119–123

    Google Scholar 

  • Rhen M, Väisänen-Rhen V, Pere A, Korhonen TK (1985) Complementation and regulatory interaction between two cloned fimbrial gene clusters of Escherichia coli strain KS71. Mol Gen Genet 200:60–64

    Google Scholar 

  • Roosendaal E, Boots M, De Graaf FK (1987) Two novel genes, fanA and fanB, involved in the biogenesis of K99 fimbriae. Nucleic Acids Res 15:5973–5984

    Google Scholar 

  • Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517

    Google Scholar 

  • Uhlin BE, Båga M, Göransson M, Lindberg FP, Lund B, Norgren M, Normark S (1985) Genes determining adhesin formation in uropathogenic Escherichia coli. Curr Top Microbiol Immunol 118:163–178

    Google Scholar 

  • Van Die I, Van Den Hondel C, Hamstra J-H, Hoekstra W, Bergmans H (1983) Studies on the fimbriae of an Escherichia coli O6:K2:H1:F7 strain: molecular cloning of a DNA fragment encoding a fimbrial antigen responsible for mannose-resistant hemagglutination of human erythrocytes. FEMS Microbiol Lett 19:77–82

    Google Scholar 

  • Van Die I, Van Megen I, Zuidweg E, Hoekstra W, De Ree H, Van Den Bosch H, Bergmans H (1986) Functional relationship among the gene clusters encoding F71, F72, F9, and F11 fimbriae of human uropathogenic Escherichia coli. J Bacteriol 167:407–410

    Google Scholar 

  • Van Embden JDA, De Graaf FK, Schouls LM, Teppema JS (1980) Cloning and expression of a deoxyribonucleic acid fragment that encodes for the adhesive antigen K99. Infect Immun 29:1125–1133

    Google Scholar 

  • Vogel HJ, Bonner DM (1956) Acetylornithinase of Escherichia coli: Partial purification and some propeties. J Biol Chem 218:97–106

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, University of Umeå, S-90187, Umeå, Sweden

    Mikael Göransson, Kristina Forsman & Bernt Eric Uhlin

Authors
  1. Mikael Göransson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristina Forsman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bernt Eric Uhlin
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by H. Hennecke

Rights and permissions

Reprints and permissions

About this article

Cite this article

Göransson, M., Forsman, K. & Uhlin, B.E. Functional and structural homology among regulatory cistrons of pili-adhesin determinants in Escherichia coli . Mol Gen Genet 212, 412–417 (1988). https://doi.org/10.1007/BF00330844

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00330844

Key words

Search

Navigation