Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Aug;159(2):555–563. doi: 10.1128/jb.159.2.555-563.1984

Regulation of outer membrane protein synthesis in Escherichia coli K-12: deletion of ompC affects expression of the OmpF protein.

C A Schnaitman, G A McDonald
PMCID: PMC215679  PMID: 6086576

Abstract

A chromosomal deletion beginning at a Tn10 located ca. 8 kilobases upstream from the ompC structural gene and extending through the 2.6-kilobase HindIII fragment carrying the ompC was isolated. The 2.6-kilobase ompC fragment was cloned into lambda 540 to obtain phage lambda 540C1. When the deletion mutant was lysogenized with lambda 540C1, the resulting strain produced normal levels of OmpC protein, and expression of this protein was regulated by osmolarity, carbon source, and the lc gene of phage PA-2, indicating that the cloned fragment contained all of the information required for regulated expression of ompC. The strain carrying the deletion was partially constitutive for expression of OmpF protein, whereas the lambda 540C1 lysogen of this strain and other strains with mutations in ompC repressed OmpF synthesis under conditions which lead to high-level expression of OmpC protein. Strains which are diploid or triploid for ompC show strong inhibition of synthesis of OmpF protein. We conclude that a regulatory element located upstream from the ompC coding sequence inhibits translation of OmpF protein under conditions which favor OmpC expression. Since ompF is known to repress transcription of ompC, we propose that these two genes constitute a closed regulatory loop which acts to amplify regulatory signals which control expression of these proteins.

Full text

PDF
555

Images in this article

Selected References

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

  1. Alphen W. V., Lugtenberg B. Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol. 1977 Aug;131(2):623–630. doi: 10.1128/jb.131.2.623-630.1977. [DOI] [PMC free article] [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. Bassford P. J., Jr, Diedrich D. L., Schnaitman C. L., Reeves P. Outer membrane proteins of Escherichia coli. VI. Protein alteration in bacteriophage-resistant mutants. J Bacteriol. 1977 Aug;131(2):608–622. doi: 10.1128/jb.131.2.608-622.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clément J. M., Hofnung M. Gene sequence of the lambda receptor, an outer membrane protein of E. coli K12. Cell. 1981 Dec;27(3 Pt 2):507–514. doi: 10.1016/0092-8674(81)90392-5. [DOI] [PubMed] [Google Scholar]
  5. Diedrich D. L., Fralick J. A. Relationship between the OmpC and LamB proteins of Escherichia coli and its influence on the protein mass of the outer membrane. J Bacteriol. 1982 Jan;149(1):156–160. doi: 10.1128/jb.149.1.156-160.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fralick J. A., Diedrich D. L. Studies on the expression of outer membrane protein 2 in escherichia coli. Mol Gen Genet. 1982;188(1):139–142. doi: 10.1007/BF00333008. [DOI] [PubMed] [Google Scholar]
  7. Garrett S., Taylor R. K., Silhavy T. J. Isolation and characterization of chain-terminating nonsense mutations in a porin regulator gene, envZ. J Bacteriol. 1983 Oct;156(1):62–69. doi: 10.1128/jb.156.1.62-69.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hall M. N., Silhavy T. J. Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol. 1981 Sep 5;151(1):1–15. doi: 10.1016/0022-2836(81)90218-7. [DOI] [PubMed] [Google Scholar]
  9. Hall M. N., Silhavy T. J. The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K12. J Mol Biol. 1981 Feb 15;146(1):23–43. doi: 10.1016/0022-2836(81)90364-8. [DOI] [PubMed] [Google Scholar]
  10. Hall M. N., Silhavy T. J. Transcriptional regulation of Escherichia coli K-12 major outer membrane protein 1b. J Bacteriol. 1979 Nov;140(2):342–350. doi: 10.1128/jb.140.2.342-350.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Inokuchi K., Mutoh N., Matsuyama S., Mizushima S. Primary structure of the ompF gene that codes for a major outer membrane protein of Escherichia coli K-12. Nucleic Acids Res. 1982 Nov 11;10(21):6957–6968. doi: 10.1093/nar/10.21.6957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kaiser K. The origin of Q-independent derivatives of phage lambda. Mol Gen Genet. 1980;179(3):547–554. doi: 10.1007/BF00271744. [DOI] [PubMed] [Google Scholar]
  13. Lee D. R., Schnaitman C. A., Pugsley A. P. Chemical heterogeneity of major outer membrane pore proteins of Escherichia coli. J Bacteriol. 1979 Jun;138(3):861–870. doi: 10.1128/jb.138.3.861-870.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Mizuno T., Chou M. Y., Inouye M. A comparative study on the genes for three porins of the Escherichia coli outer membrane. DNA sequence of the osmoregulated ompC gene. J Biol Chem. 1983 Jun 10;258(11):6932–6940. [PubMed] [Google Scholar]
  16. Mizuno T., Chou M. Y., Inouye M. A unique mechanism regulating gene expression: translational inhibition by a complementary RNA transcript (micRNA). Proc Natl Acad Sci U S A. 1984 Apr;81(7):1966–1970. doi: 10.1073/pnas.81.7.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mizuno T., Wurtzel E. T., Inouye M. Osmoregulation of gene expression. II. DNA sequence of the envZ gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem. 1982 Nov 25;257(22):13692–13698. [PubMed] [Google Scholar]
  18. Morona R., Reeves P. The tolC locus of Escherichia coli affects the expression of three major outer membrane proteins. J Bacteriol. 1982 Jun;150(3):1016–1023. doi: 10.1128/jb.150.3.1016-1023.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Murray K., Murray N. E. Phage lambda receptor chromosomes for DNA fragments made with restriction endonuclease III of Haemophilus influenzae and restriction endonuclease I of Escherichia coli. J Mol Biol. 1975 Nov 5;98(3):551–564. doi: 10.1016/s0022-2836(75)80086-6. [DOI] [PubMed] [Google Scholar]
  20. Overbeeke N., Bergmans H., van Mansfeld F., Lugtenberg B. Complete nucleotide sequence of phoE, the structural gene for the phosphate limitation inducible outer membrane pore protein of Escherichia coli K12. J Mol Biol. 1983 Feb 5;163(4):513–532. doi: 10.1016/0022-2836(83)90110-9. [DOI] [PubMed] [Google Scholar]
  21. Ozawa Y., Mizushima S. Regulation of outer membrane porin protein synthesis in Escherichia coli K-12: ompF regulates the expression of ompC. J Bacteriol. 1983 May;154(2):669–675. doi: 10.1128/jb.154.2.669-675.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pugsley A. P., Littmann-Louth D., Schnaitman C. A. Chromosomal location of the attachment site for the PA-2 prophage in Escherichia coli K-12. J Virol. 1979 Feb;29(2):808–810. doi: 10.1128/jvi.29.2.808-810.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pugsley A. P., Schnaitman C. A. Identification of three genes controlling production of new outer membrane pore proteins in Escherichia coli K-12. J Bacteriol. 1978 Sep;135(3):1118–1129. doi: 10.1128/jb.135.3.1118-1129.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pugsley A. P., Schnaitman C. A. Outer membrane proteins of Escherichia coli. VII. Evidence that bacteriophage-directed protein 2 functions as a pore. J Bacteriol. 1978 Mar;133(3):1181–1189. doi: 10.1128/jb.133.3.1181-1189.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schnaitman C., Smith D., de Salsas M. F. Temperate Bacteriophage Which Causes the Production of a New Major Outer Membrane Protein by Escherichia coli. J Virol. 1975 May;15(5):1121–1130. doi: 10.1128/jvi.15.5.1121-1130.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sutcliffe J., Blumenthal R., Walter A., Foulds J. Escherichia coli outer membrane protein K is a porin. J Bacteriol. 1983 Nov;156(2):867–872. doi: 10.1128/jb.156.2.867-872.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Taylor R. K., Hall M. N., Enquist L., Silhavy T. J. Identification of OmpR: a positive regulatory protein controlling expression of the major outer membrane matrix porin proteins of Escherichia coli K-12. J Bacteriol. 1981 Jul;147(1):255–258. doi: 10.1128/jb.147.1.255-258.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES