Regulation of sigL Expression by the Catabolite Control Protein CcpA Involves a Roadblock Mechanism in Bacillus subtilis: Potential Connection between Carbon and Nitrogen Metabolism

ABSTRACT A catabolite-responsive element (CRE), a binding site for the CcpA transcription factor, was identified within the sigL structural gene encoding σL in Bacillus subtilis. We show that CcpA binds to this CRE to regulate sigL expression by a “roadblock” mechanism and that this mechanism in part accounts for catabolite repression of σL-directed levD operon expression.

[1]  M. Hecker,et al.  The catabolite control protein CcpA controls ammonium assimilation in Bacillus subtilis. , 1999, Journal of molecular microbiology and biotechnology.

[2]  M. Buck,et al.  The biology of enhancer-dependent transcriptional regulation in bacteria: insights from genome sequences. , 2000, FEMS microbiology letters.

[3]  C. Harwood,et al.  Molecular biological methods for Bacillus , 1990 .

[4]  M. Saier Regulatory interactions involving the proteins of the phosphotransferase system in enteric bacteria , 1993, Journal of cellular biochemistry.

[5]  M. Saier,et al.  Multiple mechanisms controlling carbon metabolism in bacteria. , 1998, Biotechnology and bioengineering.

[6]  David J. Studholme,et al.  The Bacterial Enhancer-Dependent ς54(ςN) Transcription Factor , 2000, Journal of bacteriology.

[7]  A. Sonenshein,et al.  Role and Regulation of Bacillus subtilisGlutamate Dehydrogenase Genes , 1998, Journal of bacteriology.

[8]  M. Débarbouillé,et al.  Expression of the rocDEF operon involved in arginine catabolism in Bacillus subtilis. , 1995, Journal of molecular biology.

[9]  A. Steinbüchel,et al.  Biochemical and Molecular Characterization of theBacillus subtilis Acetoin Catabolic Pathway , 1999, Journal of bacteriology.

[10]  G. Rapoport,et al.  Two different mechanisms mediate catabolite repression of the Bacillus subtilis levanase operon , 1995, Journal of bacteriology.

[11]  B. Magasanik,et al.  The regulation of nitrogen utilization in enteric bacteria , 1993, Journal of cellular biochemistry.

[12]  M. Arnaud,et al.  Role of BkdR, a Transcriptional Activator of the SigL-Dependent Isoleucine and Valine Degradation Pathway inBacillus subtilis , 1999, Journal of bacteriology.

[13]  M H Saier,et al.  Cyclic AMP-independent catabolite repression in bacteria. , 1996, FEMS microbiology letters.

[14]  L. Wray,et al.  Expression of the Bacillus subtilis acsAGene: Position and Sequence Context Affect cre-Mediated Carbon Catabolite Repression , 1998, Journal of bacteriology.

[15]  D. Court,et al.  Novel Proteins of the Phosphotransferase System Encoded within the rpoN Operon of Escherichia coli , 1995, The Journal of Biological Chemistry.

[16]  W. Haldenwang The sigma factors of Bacillus subtilis , 1995, Microbiological reviews.

[17]  M. Saier,et al.  Protein phosphorylation and regulation of carbon metabolism in gram-negative versus gram-positive bacteria. , 1995, Trends in biochemical sciences.

[18]  I. Paulsen,et al.  Regulation of carbon utilization by sulfur availability in Escherichia coli and Salmonella typhimurium. , 2002, Microbiology.

[19]  Vitaly Epshtein,et al.  Transcription through the roadblocks: the role of RNA polymerase cooperation , 2003, The EMBO journal.

[20]  M H Saier,et al.  GRASP-DNA: a web application to screen prokaryotic genomes for specific DNA-binding sites and repeat motifs. , 2000, Journal of molecular microbiology and biotechnology.

[21]  I. Tikhonovich,et al.  Nitrogen Fixation: Fundamentals and Applications , 1995, Current Plant Science and Biotechnology in Agriculture.

[22]  P Glaser,et al.  RocR, a novel regulatory protein controlling arginine utilization in Bacillus subtilis, belongs to the NtrC/NifA family of transcriptional activators , 1994, Journal of bacteriology.

[23]  W. Hillen,et al.  Catabolite repression in Bacillus subtilis: a global regulatory mechanism for the Gram‐positive bacteria? , 1995, Molecular microbiology.

[24]  A. Matin,et al.  Insufficient Expression of the ilv-leu Operon Encoding Enzymes of Branched-Chain Amino Acid Biosynthesis Limits Growth of a Bacillus subtilis ccpA Mutant , 2002, Journal of bacteriology.

[25]  I. Paulsen,et al.  CcpB, a Novel Transcription Factor Implicated in Catabolite Repression in Bacillus subtilis , 1998, Journal of bacteriology.

[26]  L. Reitzer,et al.  Nitrogen assimilation and global regulation in Escherichia coli. , 2003, Annual review of microbiology.

[27]  J. Gralla,et al.  Multiple In Vivo Roles for the −12-Region Elements of Sigma 54 Promoters , 1998, Journal of bacteriology.

[28]  L. Reitzer,et al.  Metabolic Context and Possible Physiological Themes of ς54-Dependent Genes in Escherichia coli , 2001, Microbiology and Molecular Biology Reviews.

[29]  M. Débarbouillé,et al.  The Bacillus subtilis sigL gene encodes an equivalent of sigma 54 from gram-negative bacteria. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[30]  L. Reitzer,et al.  Metabolic context and possible physiological themes of sigma(54)-dependent genes in Escherichia coli. , 2001, Microbiology and molecular biology reviews : MMBR.

[31]  M. Débarbouillé,et al.  Mutagenesis of the Bacillus subtilis "-12, -24" promoter of the levanase operon and evidence for the existence of an upstream activating sequence. , 1992, Journal of molecular biology.

[32]  W. Hillen,et al.  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 , 1991, Molecular and General Genetics MGG.

[33]  M. Saier,et al.  The Role of Genes Downstream of The σN Structural Gene rpoN in Klebsiella Pneumoniae , 1995 .

[34]  B. Wanner Gene regulation by phosphate in enteric bacteria , 1993, Journal of cellular biochemistry.

[35]  Uwe Sauer,et al.  Bacillus subtilis Metabolism and Energetics in Carbon-Limited and Excess-Carbon Chemostat Culture , 2001, Journal of bacteriology.

[36]  A. Ogiwara,et al.  Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. , 2000, Nucleic acids research.

[37]  H. Zalkin,et al.  Repression of Escherichia coli purB is by a transcriptional roadblock mechanism , 1992, Journal of bacteriology.

[38]  C. Turnbough,et al.  Translocation of Escherichia coli RNA polymerase against a protein roadblock in vivo highlights a passive sliding mechanism for transcript elongation , 2004, Molecular microbiology.

[39]  I. Paulsen,et al.  Catabolite repression and inducer control in Gram-positive bacteria. , 1996, Microbiology.

[40]  Jörg Stülke,et al.  The regulatory link between carbon and nitrogen metabolism in Bacillus subtilis: regulation of the gltAB operon by the catabolite control protein CcpA. , 2003, Microbiology.

[41]  Howard C. Berg,et al.  Genetic analysis , 1957, Nature Biotechnology.

[42]  Jeffrey H. Miller Experiments in molecular genetics , 1972 .

[43]  Promoters and transcripts associated with the aroP gene of Escherichia coli , 1997, Journal of bacteriology.

[44]  J. Deutscher,et al.  Phosphorylation of HPr and Crh by HprK, Early Steps in the Catabolite Repression Signalling Pathway for the Bacillus subtilis Levanase Operon , 1999, Journal of bacteriology.

[45]  A. Sonenshein,et al.  An enhancer element located downstream of the major glutamate dehydrogenase gene of Bacillus subtilis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. Débarbouillé,et al.  Role of the transcriptional activator RocR in the arginine‐degradation pathway of Bacillus subtilis , 1997, Molecular microbiology.

[47]  M. Merrick In a class of its own--the RNA polymerase sigma factor sigma 54 (sigma N). , 1993, Molecular microbiology.

[48]  W. Hillen,et al.  Regulation of carbon catabolism in Bacillus species. , 2000, Annual review of microbiology.

[49]  M. Débarbouillé,et al.  Regulation of the Acetoin Catabolic Pathway Is Controlled by Sigma L in Bacillus subtilis , 2001, Journal of bacteriology.