Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1978 Jan;133(1):158–164. doi: 10.1128/jb.133.1.158-164.1978

Defeat of colicin tolerance in Escherichia coli ompA mutants: evidence for interaction between colicin L-JF246 and the cytoplasmic membrane.

J Foulds, T J Chai
PMCID: PMC221989  PMID: 412831

Abstract

Escherichia coli ompA mutants are tolerant to colicin L-JF246. This tolerance can be overcome by a variety of treatments that have as their target the outer membrane or the peptidoglycan layers of the cell envelope. Thus, increasing the concentration of colicin L, releasing lipopolysaccharide from the outer membrane by treatment of intact cells with ethylenediaminetetracetic acid (EDTA), converting cells to spheroplasts by treatment with lysozyme-EDTA or penicillin, or trypsin, treatment of intact cells will result in an increased colicin sensitivity. These treatments alter the outer membrane of ompA mutants and suggest that the altered outer membrane may allow the penetration of at least a portion of the colicin L molecule to a site of action located within this barrier. To substantiate this, we have demonstrated that membrane vesicles prepared from ompA mutants are sensitive to colicin L and that 14C-labeled colicin L binds rapidly to both the outer and inner membrane fractions of the cell.

Full text

PDF
158

Selected References

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

  1. Ames G. F., Nikaido K. Two-dimensional gel electrophoresis of membrane proteins. Biochemistry. 1976 Feb 10;15(3):616–623. doi: 10.1021/bi00648a026. [DOI] [PubMed] [Google Scholar]
  2. Bachmann B. J., Low K. B., Taylor A. L. Recalibrated linkage map of Escherichia coli K-12. Bacteriol Rev. 1976 Mar;40(1):116–167. doi: 10.1128/br.40.1.116-167.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bhattacharyya P., Wendt L., Whitney E., Silver S. Colicin-tolerant mutants of Escherichia coli: resistance of membranes to colicin E1. Science. 1970 May 22;168(3934):998–1000. doi: 10.1126/science.168.3934.998. [DOI] [PubMed] [Google Scholar]
  4. Boon T. Inactivation of ribosomes in vitro by colicin E 3 . Proc Natl Acad Sci U S A. 1971 Oct;68(10):2421–2425. doi: 10.1073/pnas.68.10.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bowman C. M., Dahlberg J. E., Ikemura T., Konisky J., Nomura M. Specific inactivation of 16S ribosomal RNA induced by colicin E3 in vivo. Proc Natl Acad Sci U S A. 1971 May;68(5):964–968. doi: 10.1073/pnas.68.5.964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bradbeer C., Woodrow M. L., Khalifah L. I. Transport of vitamin B12 in Escherichia coli: common receptor system for vitamin B12 and bacteriophage BF23 on the outer membrane of the cell envelope. J Bacteriol. 1976 Mar;125(3):1032–1039. doi: 10.1128/jb.125.3.1032-1039.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Braun V., Schaller K., Wolff H. A common receptor protein for phage T5 and colicin M in the outer membrane of Escherichia coli B. Biochim Biophys Acta. 1973 Sep 27;323(1):87–97. doi: 10.1016/0005-2736(73)90433-1. [DOI] [PubMed] [Google Scholar]
  8. Chai T. J., Foulds J. Purification of protein A, an outer membrane component missing in Escherichia coli K-12 ompA mutants. Biochim Biophys Acta. 1977 Jul 22;493(1):210–215. doi: 10.1016/0005-2795(77)90274-4. [DOI] [PubMed] [Google Scholar]
  9. Changeux J. P., Thiéry J. On the mode of action of colicins: a model of regulation at the membrane level. J Theor Biol. 1967 Nov;17(2):315–318. doi: 10.1016/0022-5193(67)90175-0. [DOI] [PubMed] [Google Scholar]
  10. Costerton J. W., Ingram J. M., Cheng K. J. Structure and function of the cell envelope of gram-negative bacteria. Bacteriol Rev. 1974 Mar;38(1):87–110. doi: 10.1128/br.38.1.87-110.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davies J. K., Reeves P. Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol. 1975 Jul;123(1):102–117. doi: 10.1128/jb.123.1.102-117.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Davies J. K., Reeves P. Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B. J Bacteriol. 1975 Jul;123(1):96–101. doi: 10.1128/jb.123.1.96-101.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Di Masi D. R., White J. C., Schnaitman C. A., Bradbeer C. Transport of vitamin B12 in Escherichia coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope. J Bacteriol. 1973 Aug;115(2):506–513. doi: 10.1128/jb.115.2.506-513.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Foulds J., Barrett C. Characterization of Escherichia coli mutants tolerant to bacteriocin JF246: two new classes of tolerant mutants. J Bacteriol. 1973 Nov;116(2):885–892. doi: 10.1128/jb.116.2.885-892.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Foulds J. Mode of action of a bacteriocin from Serratia marcescens. J Bacteriol. 1971 Sep;107(3):833–839. doi: 10.1128/jb.107.3.833-839.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Foulds J. Purification and partial characterization of a bacteriocin from Serratia marcescens. J Bacteriol. 1972 Jun;110(3):1001–1009. doi: 10.1128/jb.110.3.1001-1009.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garten W., Henning U. Cell envelope and shape of Escherichia coli K12. Isolation and preliminary characterization of the major ghost-membrane proteins. Eur J Biochem. 1974 Sep 1;47(2):343–352. doi: 10.1111/j.1432-1033.1974.tb03699.x. [DOI] [PubMed] [Google Scholar]
  18. Hancock R. E., Hantke K., Braun V. Iron transport of Escherichia coli K-12: involvement of the colicin B receptor and of a citrate-inducible protein. J Bacteriol. 1976 Sep;127(3):1370–1375. doi: 10.1128/jb.127.3.1370-1375.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hedges A. J. An examination of single-hit and multi-hit hypotheses in relation to the possible kinetics of colicin adsorption. J Theor Biol. 1966 Aug;11(3):383–410. doi: 10.1016/0022-5193(66)90100-7. [DOI] [PubMed] [Google Scholar]
  20. Henning U., Haller I. Mutants of Escherichia coli K12 lacking all 'major' proteins of the outer cell envelope membrane. FEBS Lett. 1975 Jul 15;55(1):161–164. doi: 10.1016/0014-5793(75)80983-5. [DOI] [PubMed] [Google Scholar]
  21. Henning U., Hindennach I., Haller I. The major proteins of the Escherichia coli outer cell envelope membrane: evidence for the structural gene of protein II. FEBS Lett. 1976 Jan 1;61(1):46–48. doi: 10.1016/0014-5793(76)80168-8. [DOI] [PubMed] [Google Scholar]
  22. Konisky J., Liu C. T. Solubilization and partial characterization of the colicin I receptor of Escherichia coli. J Biol Chem. 1974 Feb 10;249(3):835–840. [PubMed] [Google Scholar]
  23. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  24. Luckey M., Wayne R., Neilands J. B. In vitro competition between ferrichrome and phage for the outer membrane T5 receptor complex of Escherichia coli. Biochem Biophys Res Commun. 1975 May 19;64(2):687–693. doi: 10.1016/0006-291x(75)90375-7. [DOI] [PubMed] [Google Scholar]
  25. Manning P. A., Reeves P. Outer membrane of Escherichia coli K-12: TSX mutants (resistant to bacteriophage T6 and colicin K) lack an outer membrane protein. Biochem Biophys Res Commun. 1976 Jul 26;71(2):466–471. doi: 10.1016/0006-291x(76)90810-x. [DOI] [PubMed] [Google Scholar]
  26. Osborn M. J., Gander J. E., Parisi E., Carson J. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem. 1972 Jun 25;247(12):3962–3972. [PubMed] [Google Scholar]
  27. Plate C. A., Luria S. E. Stages in colicin K action, as revealed by the action of trypsin. Proc Natl Acad Sci U S A. 1972 Aug;69(8):2030–2034. doi: 10.1073/pnas.69.8.2030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pugsley A. P., Reeves P. Increased production of the outer membrane receptors for colicins B, D and M by Escherichia coli under iron starvation. Biochem Biophys Res Commun. 1976 Jun 7;70(3):846–853. doi: 10.1016/0006-291x(76)90669-0. [DOI] [PubMed] [Google Scholar]
  29. Sabet S. F., Schnaitman C. A. Localization and solubilization of colicin receptors. J Bacteriol. 1971 Oct;108(1):422–430. doi: 10.1128/jb.108.1.422-430.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schnaitman C. A. Outer membrane proteins of Escherichia coli. 3. Evidence that the major protein of Escherichia coli O111 outer membrane consists of four distinct polypeptide species. J Bacteriol. 1974 May;118(2):442–453. doi: 10.1128/jb.118.2.442-453.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schweizer M., Henning U. Action of a major outer cell envelope membrane protein in conjugation of Escherichia coli K-12. J Bacteriol. 1977 Mar;129(3):1651–1652. doi: 10.1128/jb.129.3.1651-1652.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Skurray R. A., Hancock R. E., Reeves P. Con--mutants: class of mutants in Escherichia coli K-12 lacking a major cell wall protein and defective in conjugation and adsorption of a bacteriophage. J Bacteriol. 1974 Sep;119(3):726–735. doi: 10.1128/jb.119.3.726-735.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  34. Wayne R., Frick K., Neilands J. B. Siderophore protection against colicins M, B, V, and Ia in Escherichia coli. J Bacteriol. 1976 Apr;126(1):7–12. doi: 10.1128/jb.126.1.7-12.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wayne R., Neilands J. B. Evidence for common binding sites for ferrichrome compounds and bacteriophage phi 80 in the cell envelope of Escherichia coli. J Bacteriol. 1975 Feb;121(2):497–503. doi: 10.1128/jb.121.2.497-503.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Weltzien H. U., Jesaitis M. A. The nature of the cilicin K receptor of Escherichia coli Cullen. J Exp Med. 1971 Mar 1;133(3):534–553. doi: 10.1084/jem.133.3.534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Whitney E. N. The tolC locus in Escherichia coli K12. Genetics. 1971 Jan;67(1):39–53. doi: 10.1093/genetics/67.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES