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. 1979 Aug;139(2):468–477. doi: 10.1128/jb.139.2.468-477.1979

Chromosomal location and expression of the structural gene for major outer membrane protein Ia of Escherichia coli K-12 and of the homologous gene of Salmonella typhimurium.

T Sato, T Yura
PMCID: PMC216892  PMID: 378974

Abstract

The gene determining the structure of a major outer membrane protein of Escherichia coli, protein Ia, has been located between serC and pyrD, at the min 21 region of the linkage map. This is based on the isolation and characterization of E. coli-Salmonella typhimurium intergeneric hybrids as well as analyses of a mutation (ompF2) affecting the formation of protein Ia. When the serC region of the S. typhimurium chromosome was transduced by phage P1 into E. coli, two classes of transductants were obtained; one produced protein Ia like the parental strain of E. coli, whereas the other produced not protein Ia but a pair of outer membrane proteins structurally related to 35K protein, one of the major outer membrane proteins of S. typhimurium. Furthermore, a strain of S. typhimurium harboring an F' plasmid which carries the ompF region of the E. coli chromosome was found to produce a protein indistinguishable from protein Ia, beside the outer membrane proteins characteristic to the parental Salmonella strain. These results suggest that the structural genes for protein Ia (E. coli) and for 35K protein (S. typhimurium) are homologous to each other and are located at the ompF region of the respective chromosome. The bearing of these findings on the genetic control of protein Ia formation is discussed.

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Selected References

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  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. Ames G. F., Spudich E. N., Nikaido H. Protein composition of the outer membrane of Salmonella typhimurium: effect of lipopolysaccharide mutations. J Bacteriol. 1974 Feb;117(2):406–416. doi: 10.1128/jb.117.2.406-416.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  6. Chai T. J., Foulds J. Escherichia coli K-12 tolF mutants: alterations in protein composition of the outer membrane. J Bacteriol. 1977 May;130(2):781–786. doi: 10.1128/jb.130.2.781-786.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
  8. Datta D. B., Arden B., Henning U. Major proteins of the Escherichia coli outer cell envelope membrane as bacteriophage receptors. J Bacteriol. 1977 Sep;131(3):821–829. doi: 10.1128/jb.131.3.821-829.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Datta D. B., Krämer C., Henning U. Diploidy for a structural gene specifying a major protein of the outer cell envelope membrane from Escherichia coli K-12. J Bacteriol. 1976 Dec;128(3):834–841. doi: 10.1128/jb.128.3.834-841.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. DiRienzo J. M., Nakamura K., Inouye M. The outer membrane proteins of Gram-negative bacteria: biosynthesis, assembly, and functions. Annu Rev Biochem. 1978;47:481–532. doi: 10.1146/annurev.bi.47.070178.002405. [DOI] [PubMed] [Google Scholar]
  12. Foulds J. TolF locus in Escherichia coli: chromosomal location and relationship to loci cmlB and tolD. J Bacteriol. 1976 Nov;128(2):604–608. doi: 10.1128/jb.128.2.604-608.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hasegawa Y., Yamada H., Mizushima S. Interactions of outer membrane proteins O-8 and O-9 with peptidoglycan sacculus of Escherichia coli K-12. J Biochem. 1976 Dec;80(6):1401–1409. doi: 10.1093/oxfordjournals.jbchem.a131413. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hindennach I., Henning U. The major proteins of the Excherichia coli outer cell envelope membrane. Preparative isolation of all major membrane proteins. Eur J Biochem. 1975 Nov 1;59(1):207–213. doi: 10.1111/j.1432-1033.1975.tb02443.x. [DOI] [PubMed] [Google Scholar]
  16. Horiuchi T., Sato T., Nagata T. DNA degradation in an amber mutant of Escherichia coli K12 affecting DNA ligase and viability. J Mol Biol. 1975 Jun 25;95(2):271–287. doi: 10.1016/0022-2836(75)90395-2. [DOI] [PubMed] [Google Scholar]
  17. Ichihara S., Mizushima S. Characterization of major outer membrane proteins O-8 and O-9 of Escherichia coli K-12. Evidence that structural genes for the two proteins are different. J Biochem. 1978 Apr;83(4):1095–1100. doi: 10.1093/oxfordjournals.jbchem.a131998. [DOI] [PubMed] [Google Scholar]
  18. Ichihara S., Mizushima S. Strain specificity of outer membrane proteins in Escherichia coli. J Biochem. 1977 May;81(5):1525–1530. [PubMed] [Google Scholar]
  19. Ikeda H., Tomizawa J. I. Transducing fragments in generalized transduction by phage P1. I. Molecular origin of the fragments. J Mol Biol. 1965 Nov;14(1):85–109. doi: 10.1016/s0022-2836(65)80232-7. [DOI] [PubMed] [Google Scholar]
  20. Ito K. Effects of a protease inhibitor on biosynthesis of Escherichia coli proteins. J Bacteriol. 1977 Dec;132(3):1021–1023. doi: 10.1128/jb.132.3.1021-1023.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ito K. Protease inhibitors inhibit production of protein I of the outer membrane in Escherichia coli. Biochem Biophys Res Commun. 1978 May 15;82(1):99–107. doi: 10.1016/0006-291x(78)90582-x. [DOI] [PubMed] [Google Scholar]
  22. Ito K., Sato T., Yura T. Synthesis and assembly of the membrane proteins in E. coli. Cell. 1977 Jul;11(3):551–559. doi: 10.1016/0092-8674(77)90073-3. [DOI] [PubMed] [Google Scholar]
  23. Kamio Y., Nikaido H. Outer membrane of Salmonella typhimurium. Identification of proteins exposed on cell surface. Biochim Biophys Acta. 1977 Feb 4;464(3):589–601. doi: 10.1016/0005-2736(77)90033-5. [DOI] [PubMed] [Google Scholar]
  24. LENNOX E. S. Transduction of linked genetic characters of the host by bacteriophage P1. Virology. 1955 Jul;1(2):190–206. doi: 10.1016/0042-6822(55)90016-7. [DOI] [PubMed] [Google Scholar]
  25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  26. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  27. Low B. Formation of merodiploids in matings with a class of Rec- recipient strains of Escherichia coli K12. Proc Natl Acad Sci U S A. 1968 May;60(1):160–167. doi: 10.1073/pnas.60.1.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lugtenberg B., Meijers J., Peters R., van der Hoek P., van Alphen L. Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett. 1975 Oct 15;58(1):254–258. doi: 10.1016/0014-5793(75)80272-9. [DOI] [PubMed] [Google Scholar]
  29. Lutkenhaus J. F. Role of a major outer membrane protein in Escherichia coli. J Bacteriol. 1977 Aug;131(2):631–637. doi: 10.1128/jb.131.2.631-637.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nagata T., Horiuchi T. Isolation and characterization of a temperature-sensitive amber suppressor mutant of Escherichia coli K12. Mol Gen Genet. 1973;123(1):77–88. doi: 10.1007/BF00282991. [DOI] [PubMed] [Google Scholar]
  31. Nakae T. Identification of the outer membrane protein of E. coli that produces transmembrane channels in reconstituted vesicle membranes. Biochem Biophys Res Commun. 1976 Aug 9;71(3):877–884. doi: 10.1016/0006-291x(76)90913-x. [DOI] [PubMed] [Google Scholar]
  32. Nakae T. Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J Biol Chem. 1976 Apr 10;251(7):2176–2178. [PubMed] [Google Scholar]
  33. Nakamura K., Mizushima S. Effects of heating in dodecyl sulfate solution on the conformation and electrophoretic mobility of isolated major outer membrane proteins from Escherichia coli K-12. J Biochem. 1976 Dec;80(6):1411–1422. doi: 10.1093/oxfordjournals.jbchem.a131414. [DOI] [PubMed] [Google Scholar]
  34. Nurminen M., Lounatmaa K., Sarvas M., Mäkelä P. H., Nakae T. Bacteriophage-resistant mutants of Salmonella typhimurium deficient in two major outer membrane proteins. J Bacteriol. 1976 Aug;127(2):941–955. doi: 10.1128/jb.127.2.941-955.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
  36. Palva E. T., Randall L. L. Arrangement of protein I in Escherichia coli outer membrane: cross-linking study. J Bacteriol. 1978 Jan;133(1):279–286. doi: 10.1128/jb.133.1.279-286.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Palva E. T., Randall L. L. Nearest-neighbor analysis of Escherichia coli outer membrane proteins using cleavable cross-links. J Bacteriol. 1976 Sep;127(3):1558–1560. doi: 10.1128/jb.127.3.1558-1560.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Rosenbusch J. P. Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulfate binding. J Biol Chem. 1974 Dec 25;249(24):8019–8029. [PubMed] [Google Scholar]
  40. Sanderson K. E., Hartman P. E. Linkage map of Salmonella typhimurium, edition V. Microbiol Rev. 1978 Jun;42(2):471–519. doi: 10.1128/mr.42.2.471-519.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sarma V., Reeves P. Genetic locus (ompB) affecting a major outer-membrane protein in Escherichia coli K-12. J Bacteriol. 1977 Oct;132(1):23–27. doi: 10.1128/jb.132.1.23-27.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sato T., Horiuchi T., Nagata T. Genetic analyses of an amber mutation in Escherichia coli K-12, affecting deoxyribonucleic acid ligase and viability. J Bacteriol. 1975 Dec;124(3):1089–1096. doi: 10.1128/jb.124.3.1089-1096.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sato T., Ito K., Yura T. Membrane proteins of Escherichia coli K-12: two-dimensional polyacrylamide gel electrophoresis of inner and outer membranes. Eur J Biochem. 1977 Sep;78(2):557–567. doi: 10.1111/j.1432-1033.1977.tb11769.x. [DOI] [PubMed] [Google Scholar]
  44. Sato T., Ohki M., Yura T., Ito K. Genetic studies of an Escherichia coli K-12 temperature-sensitive mutant defective in membrane protein synthesis. J Bacteriol. 1979 May;138(2):305–313. doi: 10.1128/jb.138.2.305-313.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Schmitges C. J., Henning U. The major proteins of the Escherichia coli outer cell-envelope membrane. Heterogeneity of protein I. Eur J Biochem. 1976 Mar 16;63(1):47–52. doi: 10.1111/j.1432-1033.1976.tb10205.x. [DOI] [PubMed] [Google Scholar]
  46. Schnaitman C. A. Outer membrane proteins of Escherichia coli. IV. Differences in outer membrane proteins due to strain and cultural differences. J Bacteriol. 1974 May;118(2):454–464. doi: 10.1128/jb.118.2.454-464.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sekizawa J., Inouye S., Halegoua S., Inouye M. Precursors of major outer membrane proteins of Escherichia coli. Biochem Biophys Res Commun. 1977 Aug 8;77(3):1126–1133. doi: 10.1016/s0006-291x(77)80095-8. [DOI] [PubMed] [Google Scholar]
  48. Smit J., Nikaido H. Outer membrane of gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. J Bacteriol. 1978 Aug;135(2):687–702. doi: 10.1128/jb.135.2.687-702.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yamamoto M., Nomura M., Ohsawa H., Maruo B. Identification of a temperature-sensitive asparaginyl-transfer ribonucleic acid synthetase mutant of Escherichia coli. J Bacteriol. 1977 Oct;132(1):127–131. doi: 10.1128/jb.132.1.127-131.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

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