Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1989 Dec 1;8(12):3923–3931. doi: 10.1002/j.1460-2075.1989.tb08573.x

Induction of a growth-phase-dependent promoter triggers transcription of bolA, an Escherichia coli morphogene.

M Aldea 1, T Garrido 1, C Hernández-Chico 1, M Vicente 1, S R Kushner 1
PMCID: PMC402084  PMID: 2684651

Abstract

The bolA gene, which is involved in the morphogenetic pathways of Escherichia coli, was sequenced and two potential promoters were identified. Expression from promoter P1, proximal to the bolA structural gene is specifically induced during the transition to the stationary phase of growth. This promoter contains an unusual--10 region (CGGCTAGTA), which defines a new class of E. coli promoters necessary for the dramatic increase in the rate of synthesis of a large set of proteins during the cessation of logarithmic growth. This conclusion was confirmed by identifying two additional E. coli promoters and one plasmid promoter, which also were induced during the transition to the stationary phase of growth. Analysis of proteins produced during the exponential and stationary phases of growth in a bolA null mutant suggest a possible role for the BolA protein in the induction of the expression of penicillin-binding protein 6 (PBP6) in the transition to the stationary phase. Supporting this hypothesis is the presence of a putative DNA-binding domain within the bolA coding sequence.

Full text

PDF
3923

Images in this article

3925Image
on p.3925
3927Image
on p.3927
3928Image
on p.3928
3928Image
on p.3928

Selected References

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

  1. Aldea M., Claverie-Martín F., Díaz-Torres M. R., Kushner S. R. Transcript mapping using [35S]DNA probes, trichloroacetate solvent and dideoxy sequencing ladders: a rapid method for identification of transcriptional start points. Gene. 1988 May 15;65(1):101–110. doi: 10.1016/0378-1119(88)90421-0. [DOI] [PubMed] [Google Scholar]
  2. Aldea M., Hernández-Chico C., de la Campa A. G., Kushner S. R., Vicente M. Identification, cloning, and expression of bolA, an ftsZ-dependent morphogene of Escherichia coli. J Bacteriol. 1988 Nov;170(11):5169–5176. doi: 10.1128/jb.170.11.5169-5176.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alton T. H., Koch A. L. Unused protein synthetic capacity of Escherichia coli grown in phosphate-limited chemostats. J Mol Biol. 1974 Jun 15;86(1):1–9. doi: 10.1016/s0022-2836(74)80002-1. [DOI] [PubMed] [Google Scholar]
  4. Arnold J., Eckenrode V. K., Lemke K., Phillips G. J., Schaeffer S. W. A comprehensive package for DNA sequence analysis in FORTRAN IV for the PDP-11. Nucleic Acids Res. 1986 Jan 10;14(1):239–254. doi: 10.1093/nar/14.1.239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Broome-Smith J. K., Spratt B. G. Deletion of the penicillin-binding protein 6 gene of Escherichia coli. J Bacteriol. 1982 Nov;152(2):904–906. doi: 10.1128/jb.152.2.904-906.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Castilho B. A., Olfson P., Casadaban M. J. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. doi: 10.1128/jb.158.2.488-495.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chou P. Y., Fasman G. D. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. doi: 10.1021/bi00699a002. [DOI] [PubMed] [Google Scholar]
  10. Connell N., Han Z., Moreno F., Kolter R. An E. coli promoter induced by the cessation of growth. Mol Microbiol. 1987 Sep;1(2):195–201. doi: 10.1111/j.1365-2958.1987.tb00512.x. [DOI] [PubMed] [Google Scholar]
  11. Groat R. G., Schultz J. E., Zychlinsky E., Bockman A., Matin A. Starvation proteins in Escherichia coli: kinetics of synthesis and role in starvation survival. J Bacteriol. 1986 Nov;168(2):486–493. doi: 10.1128/jb.168.2.486-493.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harley C. B., Reynolds R. P. Analysis of E. coli promoter sequences. Nucleic Acids Res. 1987 Mar 11;15(5):2343–2361. doi: 10.1093/nar/15.5.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Helmann J. D., Chamberlin M. J. Structure and function of bacterial sigma factors. Annu Rev Biochem. 1988;57:839–872. doi: 10.1146/annurev.bi.57.070188.004203. [DOI] [PubMed] [Google Scholar]
  14. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  15. Holland S. K., Cutting S., Mandelstam J. The possible DNA-binding nature of the regulatory proteins, encoded by spoIID and gerE, involved in the sporulation of Bacillus subtilis. J Gen Microbiol. 1987 Sep;133(9):2381–2391. doi: 10.1099/00221287-133-9-2381. [DOI] [PubMed] [Google Scholar]
  16. Ish-Horowicz D., Burke J. F. Rapid and efficient cosmid cloning. Nucleic Acids Res. 1981 Jul 10;9(13):2989–2998. doi: 10.1093/nar/9.13.2989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ishino F., Matsuhashi M. Peptidoglycan synthetic enzyme activities of highly purified penicillin-binding protein 3 in Escherichia coli: a septum-forming reaction sequence. Biochem Biophys Res Commun. 1981 Aug 14;101(3):905–911. doi: 10.1016/0006-291x(81)91835-0. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lin-Chao S., Bremer H. Effect of the bacterial growth rate on replication control of plasmid pBR322 in Escherichia coli. Mol Gen Genet. 1986 Apr;203(1):143–149. doi: 10.1007/BF00330395. [DOI] [PubMed] [Google Scholar]
  20. Lopilato J., Bortner S., Beckwith J. Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives. Mol Gen Genet. 1986 Nov;205(2):285–290. doi: 10.1007/BF00430440. [DOI] [PubMed] [Google Scholar]
  21. Markiewicz Z., Broome-Smith J. K., Schwarz U., Spratt B. G. Spherical E. coli due to elevated levels of D-alanine carboxypeptidase. Nature. 1982 Jun 24;297(5868):702–704. doi: 10.1038/297702a0. [DOI] [PubMed] [Google Scholar]
  22. Messing J., Gronenborn B., Müller-Hill B., Hans Hopschneider P. Filamentous coliphage M13 as a cloning vehicle: insertion of a HindII fragment of the lac regulatory region in M13 replicative form in vitro. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3642–3646. doi: 10.1073/pnas.74.9.3642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mirelman D., Yashouv-Gan Y., Nuchamovitz Y., Rozenhak S., Ron E. Z. Murein biosynthesis during a synchromous cell cycle of Escherichia coli B. J Bacteriol. 1978 May;134(2):458–461. doi: 10.1128/jb.134.2.458-461.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Pabo C. O., Sauer R. T. Protein-DNA recognition. Annu Rev Biochem. 1984;53:293–321. doi: 10.1146/annurev.bi.53.070184.001453. [DOI] [PubMed] [Google Scholar]
  26. Pisabarro A. G., Prats R., Váquez D., Rodríguez-Tébar A. Activity of penicillin-binding protein 3 from Escherichia coli. J Bacteriol. 1986 Oct;168(1):199–206. doi: 10.1128/jb.168.1.199-206.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Robinson A. C., Kenan D. J., Hatfull G. F., Sullivan N. F., Spiegelberg R., Donachie W. D. DNA sequence and transcriptional organization of essential cell division genes ftsQ and ftsA of Escherichia coli: evidence for overlapping transcriptional units. J Bacteriol. 1984 Nov;160(2):546–555. doi: 10.1128/jb.160.2.546-555.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  30. Smith D. R., Calvo J. M. Nucleotide sequence of the E coli gene coding for dihydrofolate reductase. Nucleic Acids Res. 1980 May 24;8(10):2255–2274. doi: 10.1093/nar/8.10.2255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Spratt B. G. Deletion of the penicillin-binding protein 5 gene of Escherichia coli. J Bacteriol. 1980 Dec;144(3):1190–1192. doi: 10.1128/jb.144.3.1190-1192.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Spratt B. G. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2999–3003. doi: 10.1073/pnas.72.8.2999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ward J. E., Jr, Lutkenhaus J. Overproduction of FtsZ induces minicell formation in E. coli. Cell. 1985 Oct;42(3):941–949. doi: 10.1016/0092-8674(85)90290-9. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES