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J Bacteriol. Oct 1995; 177(19): 5590–5597.
PMCID: PMC177369

Regulation of the putative bglPH operon for aryl-beta-glucoside utilization in Bacillus subtilis.

Abstract

The expression of the putative operon bglPH of Bacillus subtilis was studied by using bglP'-lacZ transcriptional fusions. The bglP gene encodes an aryl-beta-glucoside-specific enzyme II of the phosphoenolpyruvate sugar:phosphotransferase system, whereas the bglH gene product functions as a phospho-beta-glucosidase. Expression of bglPH is regulated by at least two different mechanisms: (i) carbon catabolite repression and (ii) induction via an antitermination mechanism. Distinct deletions of the promoter region were created to determine cis-acting sites for regulation. An operatorlike structure partially overlapping the -35 box of the promoter of bglP appears to be the catabolite-responsive element of this operon. The motif is similar to that of amyO and shows no mismatches with respect to the consensus sequence established as the target of carbon catabolite repression in B. subtilis. Catabolite repression is abolished in both ccpA and ptsH1 mutants. The target of the induction by the substrate, salicin or arbutin, is a transcriptional terminator located downstream from the promoter of bglP. This structure is very similar to that of transcriptional terminators which regulate the induction of the B. subtilis sacB gene, the sacPA operon, and the Escherichia coli bgl operon. The licT gene product, a member of the BglG-SacY family of antitermination proteins, is essential for the induction process. Expression of bglP is under the negative control of its own gene product. The general proteins of the phosphoenolpyruvate-dependent phosphotransferase system are required for bglP expression. Furthermore, the region upstream from bglP, which reveals a high AT content, exerts a negative regulatory effect on bglP expression.

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Selected References

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  • Amster-Choder O, Houman F, Wright A. Protein phosphorylation regulates transcription of the beta-glucoside utilization operon in E. coli. Cell. 1989 Sep 8;58(5):847–855. [PubMed]
  • Amster-Choder O, Wright A. Modulation of the dimerization of a transcriptional antiterminator protein by phosphorylation. Science. 1992 Sep 4;257(5075):1395–1398. [PubMed]
  • Arnaud M, Vary P, Zagorec M, Klier A, Debarbouille M, Postma P, Rapoport G. Regulation of the sacPA operon of Bacillus subtilis: identification of phosphotransferase system components involved in SacT activity. J Bacteriol. 1992 May;174(10):3161–3170. [PMC free article] [PubMed]
  • Aymerich S, Gonzy-Tréboul G, Steinmetz M. 5'-noncoding region sacR is the target of all identified regulation affecting the levansucrase gene in Bacillus subtilis. J Bacteriol. 1986 Jun;166(3):993–998. [PMC free article] [PubMed]
  • Aymerich S, Steinmetz M. Cloning and preliminary characterization of the sacS locus from Bacillus subtilis which controls the regulation of the exoenzyme levansucrase. Mol Gen Genet. 1987 Jun;208(1-2):114–120. [PubMed]
  • Aymerich S, Steinmetz M. Specificity determinants and structural features in the RNA target of the bacterial antiterminator proteins of the BglG/SacY family. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10410–10414. [PMC free article] [PubMed]
  • Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW, Crosa JH, Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed]
  • Crutz AM, Steinmetz M, Aymerich S, Richter R, Le Coq D. Induction of levansucrase in Bacillus subtilis: an antitermination mechanism negatively controlled by the phosphotransferase system. J Bacteriol. 1990 Feb;172(2):1043–1050. [PMC free article] [PubMed]
  • Debarbouille M, Arnaud M, Fouet A, Klier A, Rapoport G. The sacT gene regulating the sacPA operon in Bacillus subtilis shares strong homology with transcriptional antiterminators. J Bacteriol. 1990 Jul;172(7):3966–3973. [PMC free article] [PubMed]
  • Débarbouillé M, Martin-Verstraete I, Arnaud M, Klier A, Rapoport G. Positive and negative regulation controlling expression of the sac genes in Bacillus subtilis. Res Microbiol. 1991 Sep-Oct;142(7-8):757–764. [PubMed]
  • Deutscher J, Küster E, Bergstedt U, Charrier V, Hillen W. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol Microbiol. 1995 Mar;15(6):1049–1053. [PubMed]
  • Deutscher J, Reizer J, Fischer C, Galinier A, Saier MH, Jr, Steinmetz M. Loss of protein kinase-catalyzed phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, by mutation of the ptsH gene confers catabolite repression resistance to several catabolic genes of Bacillus subtilis. J Bacteriol. 1994 Jun;176(11):3336–3344. [PMC free article] [PubMed]
  • Deutscher J, Saier MH., Jr ATP-dependent protein kinase-catalyzed phosphorylation of a seryl residue in HPr, a phosphate carrier protein of the phosphotransferase system in Streptococcus pyogenes. Proc Natl Acad Sci U S A. 1983 Nov;80(22):6790–6794. [PMC free article] [PubMed]
  • Fisher SH, Sonenshein AL. Control of carbon and nitrogen metabolism in Bacillus subtilis. Annu Rev Microbiol. 1991;45:107–135. [PubMed]
  • Glaser P, Kunst F, Arnaud M, Coudart MP, Gonzales W, Hullo MF, Ionescu M, Lubochinsky B, Marcelino L, Moszer I, et al. Bacillus subtilis genome project: cloning and sequencing of the 97 kb region from 325 degrees to 333 degrees. Mol Microbiol. 1993 Oct;10(2):371–384. [PubMed]
  • Haima P, Bron S, Venema G. The effect of restriction on shotgun cloning and plasmid stability in Bacillus subtilis Marburg. Mol Gen Genet. 1987 Sep;209(2):335–342. [PubMed]
  • Hall BG, Xu L. Nucleotide sequence, function, activation, and evolution of the cryptic asc operon of Escherichia coli K12. Mol Biol Evol. 1992 Jul;9(4):688–706. [PubMed]
  • Henkin TM, Grundy FJ, Nicholson WL, Chambliss GH. Catabolite repression of alpha-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacl and galR repressors. Mol Microbiol. 1991 Mar;5(3):575–584. [PubMed]
  • Hoch JA. Genetic analysis in Bacillus subtilis. Methods Enzymol. 1991;204:305–320. [PubMed]
  • Holmes DS, Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. [PubMed]
  • Houman F, Diaz-Torres MR, Wright A. Transcriptional antitermination in the bgl operon of E. coli is modulated by a specific RNA binding protein. Cell. 1990 Sep 21;62(6):1153–1163. [PubMed]
  • Hueck CJ, Hillen W. Catabolite repression in Bacillus subtilis: a global regulatory mechanism for the gram-positive bacteria? Mol Microbiol. 1995 Feb;15(3):395–401. [PubMed]
  • Hueck CJ, Hillen W, Saier MH., Jr Analysis of a cis-active sequence mediating catabolite repression in gram-positive bacteria. Res Microbiol. 1994 Sep;145(7):503–518. [PubMed]
  • Jacob S, Allmansberger R, Gärtner D, Hillen W. Catabolite repression of the operon for xylose utilization from Bacillus subtilis W23 is mediated at the level of transcription and depends on a cis site in the xylA reading frame. Mol Gen Genet. 1991 Oct;229(2):189–196. [PubMed]
  • Kraus A, Hueck C, Gärtner D, Hillen W. Catabolite repression of the Bacillus subtilis xyl operon involves a cis element functional in the context of an unrelated sequence, and glucose exerts additional xylR-dependent repression. J Bacteriol. 1994 Mar;176(6):1738–1745. [PMC free article] [PubMed]
  • Krüger S, Stülke J, Hecker M. Catabolite repression of beta-glucanase synthesis in Bacillus subtilis. J Gen Microbiol. 1993 Sep;139(9):2047–2054. [PubMed]
  • Le Coq D, Lindner C, Krüger S, Steinmetz M, Stülke J. New beta-glucoside (bgl) genes in Bacillus subtilis: the bglP gene product has both transport and regulatory functions similar to those of BglF, its Escherichia coli homolog. J Bacteriol. 1995 Mar;177(6):1527–1535. [PMC free article] [PubMed]
  • Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol. 1982 Jan;149(1):114–122. [PMC free article] [PubMed]
  • Miwa Y, Fujita Y. Determination of the cis sequence involved in catabolite repression of the Bacillus subtilis gnt operon; implication of a consensus sequence in catabolite repression in the genus Bacillus. Nucleic Acids Res. 1990 Dec 11;18(23):7049–7053. [PMC free article] [PubMed]
  • Nicholson WL, Chambliss GH. Isolation and characterization of a cis-acting mutation conferring catabolite repression resistance to alpha-amylase synthesis in Bacillus subtilis. J Bacteriol. 1985 Mar;161(3):875–881. [PMC free article] [PubMed]
  • Parker LL, Hall BG. Characterization and nucleotide sequence of the cryptic cel operon of Escherichia coli K12. Genetics. 1990 Mar;124(3):455–471. [PMC free article] [PubMed]
  • Postma PW, Lengeler JW, Jacobson GR. Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev. 1993 Sep;57(3):543–594. [PMC free article] [PubMed]
  • Prasad I, Young B, Schaefler S. Genetic determination of the constitutive biosynthesis of phospho- -glucosidase A in Escherichia coli K-12. J Bacteriol. 1973 Jun;114(3):909–915. [PMC free article] [PubMed]
  • Reizer J, Novotny MJ, Hengstenberg W, Saier MH., Jr Properties of ATP-dependent protein kinase from Streptococcus pyogenes that phosphorylates a seryl residue in HPr, a phosphocarrier protein of the phosphotransferase system. J Bacteriol. 1984 Oct;160(1):333–340. [PMC free article] [PubMed]
  • Reynolds AE, Mahadevan S, LeGrice SF, 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. [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schnetz K, Rak B. Beta-glucoside permease represses the bgl operon of Escherichia coli by phosphorylation of the antiterminator protein and also interacts with glucose-specific enzyme III, the key element in catabolite control. Proc Natl Acad Sci U S A. 1990 Jul;87(13):5074–5078. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Steinmetz M, Le Coq D, Aymerich S. Induction of saccharolytic enzymes by sucrose in Bacillus subtilis: evidence for two partially interchangeable regulatory pathways. J Bacteriol. 1989 Mar;171(3):1519–1523. [PMC free article] [PubMed]
  • Steinmetz M, Richter R. Plasmids designed to alter the antibiotic resistance expressed by insertion mutations in Bacillus subtilis, through in vivo recombination. Gene. 1994 May 3;142(1):79–83. [PubMed]
  • Stragier P, Bonamy C, Karmazyn-Campelli C. Processing of a sporulation sigma factor in Bacillus subtilis: how morphological structure could control gene expression. Cell. 1988 Mar 11;52(5):697–704. [PubMed]
  • Stülke J, Hanschke R, Hecker M. Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J Gen Microbiol. 1993 Sep;139(9):2041–2045. [PubMed]
  • Weickert MJ, Chambliss GH. Site-directed mutagenesis of a catabolite repression operator sequence in Bacillus subtilis. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6238–6242. [PMC free article] [PubMed]
  • Wray LV, Jr, Pettengill FK, Fisher SH. Catabolite repression of the Bacillus subtilis hut operon requires a cis-acting site located downstream of the transcription initiation site. J Bacteriol. 1994 Apr;176(7):1894–1902. [PMC free article] [PubMed]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [PubMed]
  • Zhang J, Aronson A. A Bacillus subtilis bglA gene encoding phospho-beta-glucosidase is inducible and closely linked to a NADH dehydrogenase-encoding gene. Gene. 1994 Mar 11;140(1):85–90. [PubMed]

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