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. 1986 Sep;167(3):1058–1065. doi: 10.1128/jb.167.3.1058-1065.1986

Growth phase and ompR regulation of transcription of microcin B17 genes.

C Hernández-Chico, J L San Millán, R Kolter, F Moreno
PMCID: PMC215981  PMID: 3017916

Abstract

The synthesis of the peptide antibiotic microcin B17 was shown to occur as the cells entered the stationary phase of growth. This type of growth phase regulation is commonly observed in the production of a number of different bacterial products such as toxins and antibiotics. Microcin B17 synthesis is also dependent on the product of the ompR gene. To determine the role of transcription in this double regulation of microcin B17 production, operon fusions with Mu d1 (Ap lac) were constructed. Insertions were obtained in all four plasmid genes involved in production of microcin B17 (mcbA-D) and in the immunity region. Three classes of fusions were obtained. Fusions into mcbA, mcbB, and mcbC (first class) exhibited an increase in their transcription as the cells approached the stationary phase. These increases as well as basal levels of transcription were dependent on OmpR. Expression of fusions in mcbD and in the immunity region (second class) was also dependent on OmpR, but their expression remained constant throughout growth. One fusion in mcbC (third class) was obtained which was transcribed in the opposite direction than the others. It showed no growth phase regulation and no OmpR dependence. The implications of these results in terms of the transcriptional organization of the mbc genes are discussed.

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Selected References

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

  1. Aharonowitz Y. Nitrogen metabolite regulation of antibiotic biosynthesis. Annu Rev Microbiol. 1980;34:209–233. doi: 10.1146/annurev.mi.34.100180.001233. [DOI] [PubMed] [Google Scholar]
  2. Asensio C., Pérez-Díaz J. C. A new family of low molecular weight antibiotics from enterobacteria. Biochem Biophys Res Commun. 1976 Mar 8;69(1):7–14. doi: 10.1016/s0006-291x(76)80264-1. [DOI] [PubMed] [Google Scholar]
  3. Baquero F., Bouanchaud D., Martinez-Perez M. C., Fernandez C. Microcin plasmids: a group of extrachromosomal elements coding for low-molecular-weight antibiotics in Escherichia coli. J Bacteriol. 1978 Aug;135(2):342–347. doi: 10.1128/jb.135.2.342-347.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beutin L., Manning P. A., Achtman M., Willetts N. sfrA and sfrB products of Escherichia coli K-12 are transcriptional control factors. J Bacteriol. 1981 Feb;145(2):840–844. doi: 10.1128/jb.145.2.840-844.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buchanan C. E., Sowell M. O. Synthesis of penicillin-binding protein 6 by stationary-phase Escherichia coli. J Bacteriol. 1982 Jul;151(1):491–494. doi: 10.1128/jb.151.1.491-494.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casadaban M. J., Cohen S. N. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J Mol Biol. 1980 Apr;138(2):179–207. doi: 10.1016/0022-2836(80)90283-1. [DOI] [PubMed] [Google Scholar]
  7. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Comeau D. E., Ikenaka K., Tsung K. L., Inouye M. Primary characterization of the protein products of the Escherichia coli ompB locus: structure and regulation of synthesis of the OmpR and EnvZ proteins. J Bacteriol. 1985 Nov;164(2):578–584. doi: 10.1128/jb.164.2.578-584.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Drury L. S., Buxton R. S. DNA sequence analysis of the dye gene of Escherichia coli reveals amino acid homology between the dye and OmpR proteins. J Biol Chem. 1985 Apr 10;260(7):4236–4242. [PubMed] [Google Scholar]
  12. Ferrari F. A., Trach K., LeCoq D., Spence J., Ferrari E., Hoch J. A. Characterization of the spo0A locus and its deduced product. Proc Natl Acad Sci U S A. 1985 May;82(9):2647–2651. doi: 10.1073/pnas.82.9.2647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Genilloud O., Garrido M. C., Moreno F. The transposon Tn5 carries a bleomycin-resistance determinant. Gene. 1984 Dec;32(1-2):225–233. doi: 10.1016/0378-1119(84)90050-7. [DOI] [PubMed] [Google Scholar]
  14. Gilman M. Z., Chamberlin M. J. Developmental and genetic regulation of Bacillus subtilis genes transcribed by sigma 28-RNA polymerase. Cell. 1983 Nov;35(1):285–293. doi: 10.1016/0092-8674(83)90231-3. [DOI] [PubMed] [Google Scholar]
  15. Glenn A. R. Production of extracellular proteins by bacteria. Annu Rev Microbiol. 1976;30:41–62. doi: 10.1146/annurev.mi.30.100176.000353. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Hantke K. Major outer membrane proteins of E. coli K12 serve as receptors for the phages T2 (protein Ia) and 434 (protein Ib). Mol Gen Genet. 1978 Aug 17;164(2):131–135. doi: 10.1007/BF00267377. [DOI] [PubMed] [Google Scholar]
  20. Hernández-Chico C., Herrero M., Rejas M., San Millán J. L., Moreno F. Gene ompR and regulation of microcin 17 and colicin e2 syntheses. J Bacteriol. 1982 Nov;152(2):897–900. doi: 10.1128/jb.152.2.897-900.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Herrero M., Moreno F. Microcin B17 blocks DNA replication and induces the SOS system in Escherichia coli. J Gen Microbiol. 1986 Feb;132(2):393–402. doi: 10.1099/00221287-132-2-393. [DOI] [PubMed] [Google Scholar]
  22. Jorgensen R. A., Reznikoff W. S. Organization of structural and regulatory genes that mediate tetracycline resistance in transposon Tn10. J Bacteriol. 1979 Jun;138(3):705–714. doi: 10.1128/jb.138.3.705-714.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Little J. W., Mount D. W. The SOS regulatory system of Escherichia coli. Cell. 1982 May;29(1):11–22. doi: 10.1016/0092-8674(82)90085-x. [DOI] [PubMed] [Google Scholar]
  24. Miller J. H., Ganem D., Lu P., Schmitz A. Genetic studies of the lac repressor. I. Correlation of mutational sites with specific amino acid residues: construction of a colinear gene-protein map. J Mol Biol. 1977 Jan 15;109(2):275–298. doi: 10.1016/s0022-2836(77)80034-x. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. O'Connor M. B., Malamy M. H. A new insertion sequence, IS121, is found on the Mu dI1 (Ap lac) bacteriophage and the Escherichia coli K-12 chromosome. J Bacteriol. 1983 Nov;156(2):669–679. doi: 10.1128/jb.156.2.669-679.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Okita T. W., Rodriguez R. L., Preiss J. Biosynthesis of bacterial glycogen. Cloning of the glycogen biosynthetic enzyme structural genes of Escherichia coli. J Biol Chem. 1981 Jul 10;256(13):6944–6952. [PubMed] [Google Scholar]
  28. Ollington J. F., Haldenwang W. G., Huynh T. V., Losick R. Developmentally regulated transcription in a cloned segment of the Bacillus subtilis chromosome. J Bacteriol. 1981 Aug;147(2):432–442. doi: 10.1128/jb.147.2.432-442.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Priest F. G. Extracellular enzyme synthesis in the genus Bacillus. Bacteriol Rev. 1977 Sep;41(3):711–753. doi: 10.1128/br.41.3.711-753.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rao N. N., Roberts M. F., Torriani A. Amount and chain length of polyphosphates in Escherichia coli depend on cell growth conditions. J Bacteriol. 1985 Apr;162(1):242–247. doi: 10.1128/jb.162.1.242-247.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. San Millan J. L., Hernandez-Chico C., Pereda P., Moreno F. Cloning and mapping of the genetic determinants for microcin B17 production and immunity. J Bacteriol. 1985 Jul;163(1):275–281. doi: 10.1128/jb.163.1.275-281.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. San Millán J. L., Kolter R., Moreno F. Plasmid genes required for microcin B17 production. J Bacteriol. 1985 Sep;163(3):1016–1020. doi: 10.1128/jb.163.3.1016-1020.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Trach K. A., Chapman J. W., Piggot P. J., Hoch J. A. Deduced product of the stage 0 sporulation gene spo0F shares homology with the Spo0A, OmpR, and SfrA proteins. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7260–7264. doi: 10.1073/pnas.82.21.7260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Villarejo M., Davis J. L., Granett S. Osmoregulation of alkaline phosphatase synthesis in Escherichia coli K-12. J Bacteriol. 1983 Nov;156(2):975–978. doi: 10.1128/jb.156.2.975-978.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wandersman C., Moreno F., Schwartz M. Pleiotropic mutations rendering Escherichia coli K-12 resistant to bacteriophage TP1. J Bacteriol. 1980 Sep;143(3):1374–1383. doi: 10.1128/jb.143.3.1374-1383.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. de Lorenzo V., Martínez J. L., Asensio C. Microcin-mediated interactions between Klebsiella pneumoniae and Escherichia coli strains. J Gen Microbiol. 1984 Feb;130(2):391–400. doi: 10.1099/00221287-130-2-391. [DOI] [PubMed] [Google Scholar]

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