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. 1988 Oct;7(10):3271–3277. doi: 10.1002/j.1460-2075.1988.tb03194.x

Regulation of the bgl operon of Escherichia coli by transcriptional antitermination.

K Schnetz 1, B Rak 1
PMCID: PMC454751  PMID: 2846278

Abstract

The bgl operon of Escherichia coli encodes all functions necessary for the regulated uptake and utilization of aryl beta-glucosides. The operon is unusual, however, in that it is cryptic in wild-type strains, requiring activation by mutational events. The vast majority of these mutations are due to transposition of insertion elements into the promoter region of the operon. In this report we show that integration of IS5 into the vicinity of the bgl promoter (P0) enhances its activity by greater than 60-fold thereby activating the operon. In the activated state the operon is subject to induction by substrate. Recent studies have shown that induction of the bgl operon by substrate involves antitermination within the leader of the operon. We now show that substrate-dependent regulation involves specific termination/antitermination of transcription at two signal structures flanking the first gene of the operon, bglG. Antitermination is mediated by the product of gene bglG. In the absence of substrate this antitermination is prevented by the action of the product of gene bglF (the second gene of the operon), which encodes the beta-glucoside-specific transport protein (enzymeIIBgl of the phosphoenolpyruvate-dependent phosphotransferase system, PTS) resulting in repression of the operon. The bgl promoter (P0) is not subject to substrate-dependent regulation. The bgl operon has two additional promoters (P1 and P2) located within the terminators, which could also participate in regulation.

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Selected References

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  1. Alt-Moerbe J., Rak B., Schröder J. A 3.6-kbp segment from the vir region of Ti plasmids contains genes responsible for border-sequence-directed production of T region circles in E. coli. EMBO J. 1986 Jun;5(6):1129–1135. doi: 10.1002/j.1460-2075.1986.tb04337.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Amann E., Brosius J., Ptashne M. Vectors bearing a hybrid trp-lac promoter useful for regulated expression of cloned genes in Escherichia coli. Gene. 1983 Nov;25(2-3):167–178. doi: 10.1016/0378-1119(83)90222-6. [DOI] [PubMed] [Google Scholar]
  3. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Deng G., Wu R. Terminal transferase: use of the tailing of DNA and for in vitro mutagenesis. Methods Enzymol. 1983;100:96–116. doi: 10.1016/0076-6879(83)00047-6. [DOI] [PubMed] [Google Scholar]
  8. Fox C. F., Wilson G. The role of a phosphoenolpyruvate-dependent kinase system in beta-glucoside catabolism in Escherichia coli. Proc Natl Acad Sci U S A. 1968 Mar;59(3):988–995. doi: 10.1073/pnas.59.3.988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Mahadevan S., Reynolds A. E., Wright A. Positive and negative regulation of the bgl operon in Escherichia coli. J Bacteriol. 1987 Jun;169(6):2570–2578. doi: 10.1128/jb.169.6.2570-2578.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mahadevan S., Wright A. A bacterial gene involved in transcription antitermination: regulation at a rho-independent terminator in the bgl operon of E. coli. Cell. 1987 Jul 31;50(3):485–494. doi: 10.1016/0092-8674(87)90502-2. [DOI] [PubMed] [Google Scholar]
  11. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  12. Postma P. W., Lengeler J. W. Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol Rev. 1985 Sep;49(3):232–269. doi: 10.1128/mr.49.3.232-269.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Prasad I., Schaefler S. Regulation of the beta-glucoside system in Escherchia coli K-12. J Bacteriol. 1974 Nov;120(2):638–650. doi: 10.1128/jb.120.2.638-650.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Rak B., Lusky M., Hable M. Expression of two proteins from overlapping and oppositely oriented genes on transposable DNA insertion element IS5. Nature. 1982 May 13;297(5862):124–128. doi: 10.1038/297124a0. [DOI] [PubMed] [Google Scholar]
  15. Rak B., von Reutern M. Insertion element IS5 contains a third gene. EMBO J. 1984 Apr;3(4):807–811. doi: 10.1002/j.1460-2075.1984.tb01889.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Reynolds A. E., Felton J., Wright A. Insertion of DNA activates the cryptic bgl operon in E. coli K12. Nature. 1981 Oct 22;293(5834):625–629. doi: 10.1038/293625a0. [DOI] [PubMed] [Google Scholar]
  17. Reynolds A. E., Mahadevan S., LeGrice S. F., Wright A. Enhancement of bacterial gene expression by insertion elements or by mutation in a CAP-cAMP binding site. J Mol Biol. 1986 Sep 5;191(1):85–95. doi: 10.1016/0022-2836(86)90424-9. [DOI] [PubMed] [Google Scholar]
  18. Ronecker H. J., Rak B. Genetic organization of insertion element IS2 based on a revised nucleotide sequence. Gene. 1987;59(2-3):291–296. doi: 10.1016/0378-1119(87)90337-4. [DOI] [PubMed] [Google Scholar]
  19. Saedler H., Besemer J., Kemper B., Rosenwirth B., Starlinger P. Insertion mutations in the control region of the Gal operon of E. coli. I. Biological characterization of the mutations. Mol Gen Genet. 1972;115(3):258–265. doi: 10.1007/BF00268889. [DOI] [PubMed] [Google Scholar]
  20. Saier M. H., Jr, Yamada M., Erni B., Suda K., Lengeler J., Ebner R., Argos P., Rak B., Schnetz K., Lee C. A. Sugar permeases of the bacterial phosphoenolpyruvate-dependent phosphotransferase system: sequence comparisons. FASEB J. 1988 Mar 1;2(3):199–208. doi: 10.1096/fasebj.2.3.2832233. [DOI] [PubMed] [Google Scholar]
  21. Schaefler S. Inducible system for the utilization of beta-glucosides in Escherichia coli. I. Active transport and utilization of beta-glucosides. J Bacteriol. 1967 Jan;93(1):254–263. doi: 10.1128/jb.93.1.254-263.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schnetz K., Toloczyki C., Rak B. Beta-glucoside (bgl) operon of Escherichia coli K-12: nucleotide sequence, genetic organization, and possible evolutionary relationship to regulatory components of two Bacillus subtilis genes. J Bacteriol. 1987 Jun;169(6):2579–2590. doi: 10.1128/jb.169.6.2579-2590.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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