Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Sep;173(17):5308–5314. doi: 10.1128/jb.173.17.5308-5314.1991

Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli.

M S McClain 1, I C Blomfield 1, B I Eisenstein 1
PMCID: PMC208240  PMID: 1679430

Abstract

Evidence obtained with an improved in vivo assay of fimbrial phase variation in Escherichia coli supported a revised understanding of the roles of fimB and fimE in the site-specific DNA rearrangement with which they are associated. A previously proposed model argued that fimB and fimE play antagonistic, unidirectional roles in regulating the orientation of the invertible DNA element located immediately upstream of fimA, the gene encoding the major subunit of type 1 fimbriae. This conclusion, though, is based on an in vivo DNA inversion assay using recombinant plasmid substrates under conditions that, among other things, were incapable of detecting recombination of the fim invertible element from the on to the off orientation. Using a modified system that overcome this and several additional technical problems, we confirmed that fimB acts independently of fimE on the invertible element and that the additional presence of fimE results in the preferential rearrangement of the element to the off orientation. It is now demonstrated that fimE can act in the absence of fimB in this recombination to promote inversion primarily from on to off. In contrast to the previous studies, the effect of fimB on a substrate carrying the invertible element in the on orientation could be examined. It was found that fimB mediates DNA inversion from on to off, as well as from off to on, and that, contrary to prior interpretations, the fimB-associated inversion occurs with only minimal orientational preference to the on phase.

Full text

PDF
5308

Images in this article

5310Image
on p.5310
5311Image
on p.5311

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. 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]
  3. Blomfield I. C., McClain M. S., Princ J. A., Calie P. J., Eisenstein B. I. Type 1 fimbriation and fimE mutants of Escherichia coli K-12. J Bacteriol. 1991 Sep;173(17):5298–5307. doi: 10.1128/jb.173.17.5298-5307.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blomfield I. C., Vaughn V., Rest R. F., Eisenstein B. I. Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol. 1991 Jun;5(6):1447–1457. doi: 10.1111/j.1365-2958.1991.tb00791.x. [DOI] [PubMed] [Google Scholar]
  5. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N. Positive selection for loss of tetracycline resistance. J Bacteriol. 1980 Aug;143(2):926–933. doi: 10.1128/jb.143.2.926-933.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brosius J., Holy A. Regulation of ribosomal RNA promoters with a synthetic lac operator. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6929–6933. doi: 10.1073/pnas.81.22.6929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Csonka L. N., Clark A. J. Deletions generated by the transposon Tn10 in the srl recA region of the Escherichia coli K-12 chromosome. Genetics. 1979 Oct;93(2):321–343. doi: 10.1093/genetics/93.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dorman C. J., Higgins C. F. Fimbrial phase variation in Escherichia coli: dependence on integration host factor and homologies with other site-specific recombinases. J Bacteriol. 1987 Aug;169(8):3840–3843. doi: 10.1128/jb.169.8.3840-3843.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eisenstein B. I., Beachey E. H., Ofek I. Influence of sublethal concentrations of antibiotics on the expression of the mannose-specific ligand of Escherichia coli. Infect Immun. 1980 Apr;28(1):154–159. doi: 10.1128/iai.28.1.154-159.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eisenstein B. I., Dodd D. C. Pseudocatabolite repression of type 1 fimbriae of Escherichia coli. J Bacteriol. 1982 Sep;151(3):1560–1567. doi: 10.1128/jb.151.3.1560-1567.1982. [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. Eisenstein B. I., Sweet D. S., Vaughn V., Friedman D. I. Integration host factor is required for the DNA inversion that controls phase variation in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6506–6510. doi: 10.1073/pnas.84.18.6506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freitag C. S., Abraham J. M., Clements J. R., Eisenstein B. I. Genetic analysis of the phase variation control of expression of type 1 fimbriae in Escherichia coli. J Bacteriol. 1985 May;162(2):668–675. doi: 10.1128/jb.162.2.668-675.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Friedman D. I. Integration host factor: a protein for all reasons. Cell. 1988 Nov 18;55(4):545–554. doi: 10.1016/0092-8674(88)90213-9. [DOI] [PubMed] [Google Scholar]
  15. Friedman D. I., Plantefaber L. C., Olson E. J., Carver D., O'Dea M. H., Gellert M. Mutations in the DNA gyrB gene that are temperature sensitive for lambda site-specific recombination, Mu growth, and plasmid maintenance. J Bacteriol. 1984 Feb;157(2):490–497. doi: 10.1128/jb.157.2.490-497.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Higgins C. F., Dorman C. J., Stirling D. A., Waddell L., Booth I. R., May G., Bremer E. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell. 1988 Feb 26;52(4):569–584. doi: 10.1016/0092-8674(88)90470-9. [DOI] [PubMed] [Google Scholar]
  17. Hulton C. S., Seirafi A., Hinton J. C., Sidebotham J. M., Waddell L., Pavitt G. D., Owen-Hughes T., Spassky A., Buc H., Higgins C. F. Histone-like protein H1 (H-NS), DNA supercoiling, and gene expression in bacteria. Cell. 1990 Nov 2;63(3):631–642. doi: 10.1016/0092-8674(90)90458-q. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Klemm P. Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J. 1986 Jun;5(6):1389–1393. doi: 10.1002/j.1460-2075.1986.tb04372.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. May G., Dersch P., Haardt M., Middendorf A., Bremer E. The osmZ (bglY) gene encodes the DNA-binding protein H-NS (H1a), a component of the Escherichia coli K12 nucleoid. Mol Gen Genet. 1990 Oct;224(1):81–90. doi: 10.1007/BF00259454. [DOI] [PubMed] [Google Scholar]
  22. Old D. C., Duguid J. P. Selective outgrowth of fimbriate bacteria in static liquid medium. J Bacteriol. 1970 Aug;103(2):447–456. doi: 10.1128/jb.103.2.447-456.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Orndorff P. E., Falkow S. Identification and characterization of a gene product that regulates type 1 piliation in Escherichia coli. J Bacteriol. 1984 Oct;160(1):61–66. doi: 10.1128/jb.160.1.61-66.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  26. Spears P. A., Schauer D., Orndorff P. E. Metastable regulation of type 1 piliation in Escherichia coli and isolation and characterization of a phenotypically stable mutant. J Bacteriol. 1986 Oct;168(1):179–185. doi: 10.1128/jb.168.1.179-185.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stueber D., Bujard H. Transcription from efficient promoters can interfere with plasmid replication and diminish expression of plasmid specified genes. EMBO J. 1982;1(11):1399–1404. doi: 10.1002/j.1460-2075.1982.tb01329.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES