Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1985 May;162(2):668–675. doi: 10.1128/jb.162.2.668-675.1985

Genetic analysis of the phase variation control of expression of type 1 fimbriae in Escherichia coli.

C S Freitag, J M Abraham, J R Clements, B I Eisenstein
PMCID: PMC218902  PMID: 2859269

Abstract

Expression of type 1 fimbriae in Escherichia coli exhibits phase variation, whereby individual cells can alternate between states of organelle expression (Fim+) and nonexpression (Fim-). Strains with a fimD-lac operon fusion, in which lac, rather than fimD, expression is under the control of the fimD promoter, undergo Lac+ in equilibrium Lac- phase variation, instead. After positioning a lambda prophage adjacent to the operon fusion, we were able to isolate specialized lambda phage carrying both the fimD-lac fusion and the phase variation control region. Introduction of such phage into an Fim+ strain resulted in construction of a strain with a double, independently switching phenotype (Fim+ in equilibrium Fim- and Lac+ in equilibrium Lac-), demonstrating that the region controlling phase variation is contiguous with the fimD-lac operon fusion and is cis acting. When the specialized lambda phage was propagated on a delta lac delta fim strain, phase variation occurred within the plaques, confirming that the phase variation control region is carried on the specialized transducing phage. All lysogens acquired the Lac+ in equilibrium Lac- phenotype, except for two nonswitching Lac+ recombinants, which acquired Lac+ in equilibrium Lac- phase variation only by trans complementation with fim. Phase variation of type 1 fimbriae, therefore, appears to involve both a cis-active element, which is cloned on a specialized lambda phage, and a trans-active permissive factor, which is not present on the phage, but rather must be supplied by the recipient strain in the transduction.

Full text

PDF
669

Images in this article

Selected References

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

  1. 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]
  2. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bar-Shavit Z., Ofek I., Goldman R., Mirelman D., Sharon N. Mannose residues on phagocytes as receptors for the attachment of Escherichia coli and Salmonella typhi. Biochem Biophys Res Commun. 1977 Sep 9;78(1):455–460. doi: 10.1016/0006-291x(77)91276-1. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Campbell A., Berg D. E., Botstein D., Lederberg E. M., Novick R. P., Starlinger P., Szybalski W. Nomenclature of transposable elements in prokaryotes. Gene. 1979 Mar;5(3):197–206. doi: 10.1016/0378-1119(79)90078-7. [DOI] [PubMed] [Google Scholar]
  6. Casadaban M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. doi: 10.1016/0022-2836(76)90119-4. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Eisenstein B. I., Clements J. R., Dodd D. C. Isolation and characterization of a monoclonal antibody directed against type 1 fimbriae organelles from Escherichia coli. Infect Immun. 1983 Oct;42(1):333–340. doi: 10.1128/iai.42.1.333-340.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eisenstein B. I. Operon fusion of the phase variation switch. A virulence factor in Escherichia coli. Infection. 1982;10(2):112–115. doi: 10.1007/BF01816739. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Freitag C. S., Eisenstein B. I. Genetic mapping and transcriptional orientation of the fimD gene. J Bacteriol. 1983 Dec;156(3):1052–1058. doi: 10.1128/jb.156.3.1052-1058.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Iino T., Kutsukake K. Trans-acting genes of bacteriophages P1 and Mu mediate inversion of a specific DNA segment involved in flagellar phase variation of Salmonella. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):11–16. doi: 10.1101/sqb.1981.045.01.004. [DOI] [PubMed] [Google Scholar]
  13. Kamp D., Kahmann R. The relationship of two invertible segments in bacteriophage Mu and Salmonella typhimurium DNA. Mol Gen Genet. 1981;184(3):564–566. doi: 10.1007/BF00352543. [DOI] [PubMed] [Google Scholar]
  14. Kleckner N., Barker D. F., Ross D. G., Botstein D. Properties of the translocatable tetracycline-resistance element Tn10 in Escherichia coli and bacteriophage lambda. Genetics. 1978 Nov;90(3):427–461. doi: 10.1093/genetics/90.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lorence M. C., Rupert C. S. Convenient construction of recA deletion derivatives of Escherichia coli. J Bacteriol. 1983 Oct;156(1):458–459. doi: 10.1128/jb.156.1.458-459.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maloy S. R., Nunn W. D. Selection for loss of tetracycline resistance by Escherichia coli. J Bacteriol. 1981 Feb;145(2):1110–1111. doi: 10.1128/jb.145.2.1110-1111.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Meyer T. F., Billyard E., Haas R., Storzbach S., So M. Pilus genes of Neisseria gonorrheae: chromosomal organization and DNA sequence. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6110–6114. doi: 10.1073/pnas.81.19.6110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Meyer T. F., Mlawer N., So M. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell. 1982 Aug;30(1):45–52. doi: 10.1016/0092-8674(82)90010-1. [DOI] [PubMed] [Google Scholar]
  19. 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]
  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. Plasterk R. H., Brinkman A., van de Putte P. DNA inversions in the chromosome of Escherichia coli and in bacteriophage Mu: relationship to other site-specific recombination systems. Proc Natl Acad Sci U S A. 1983 Sep;80(17):5355–5358. doi: 10.1073/pnas.80.17.5355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Plasterk R. H., Van de Putte P. Genetic switches by DNA inversions in prokaryotes. Biochim Biophys Acta. 1984 Jun 16;782(2):111–119. doi: 10.1016/0167-4781(84)90013-7. [DOI] [PubMed] [Google Scholar]
  23. Salit I. E., Gotschlich E. C. Type I Escherichia coli pili: characterization of binding to monkey kidney cells. J Exp Med. 1977 Nov 1;146(5):1182–1194. doi: 10.1084/jem.146.5.1182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Silverman M., Simon M. Phase variation: genetic analysis of switching mutants. Cell. 1980 Apr;19(4):845–854. doi: 10.1016/0092-8674(80)90075-6. [DOI] [PubMed] [Google Scholar]
  25. Stern A., Nickel P., Meyer T. F., So M. Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonococcal pilus gene. Cell. 1984 Jun;37(2):447–456. doi: 10.1016/0092-8674(84)90375-1. [DOI] [PubMed] [Google Scholar]
  26. Szekely E., Simon M. Homology between the invertible deoxyribonucleic acid sequence that controls flagellar-phase variation in Salmonella sp. and deoxyribonucleic acid sequences in other organisms. J Bacteriol. 1981 Dec;148(3):829–836. doi: 10.1128/jb.148.3.829-836.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Zieg J., Hilmen M., Simon M. Regulation of gene expression by site-specific inversion. Cell. 1978 Sep;15(1):237–244. doi: 10.1016/0092-8674(78)90098-3. [DOI] [PubMed] [Google Scholar]
  28. van de Putte P., Plasterk R., Kuijpers A. A Mu gin complementing function and an invertible DNA region in Escherichia coli K-12 are situated on the genetic element e14. J Bacteriol. 1984 May;158(2):517–522. doi: 10.1128/jb.158.2.517-522.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES