Additional Targets of the Bacillus subtilis Global Regulator CodY Identified by Chromatin Immunoprecipitation and Genome-Wide Transcript Analysis

ABSTRACT Additional targets of CodY, a GTP-activated repressor of early stationary-phase genes in Bacillus subtilis, were identified by combining chromatin immunoprecipitation, DNA microarray hybridization, and gel mobility shift assays. The direct targets of CodY newly identified by this approach included regulatory genes for sporulation, genes that are likely to encode transporters for amino acids and sugars, and the genes for biosynthesis of branched-chain amino acids.

[1]  P. Schaeffer,et al.  Catabolic repression of bacterial sporulation. , 1965, Proceedings of the National Academy of Sciences of the United States of America.

[2]  E. Freese,et al.  Induction of sporulation in Bacillus subtilis by decoyinine or hadacidin. , 1977, Biochemical and biophysical research communications.

[3]  E. Freese,et al.  The decrease of guanine nucleotides initiates sporulation of Bacillus subtilis. , 1979, Biochimica et biophysica acta.

[4]  E. Freese,et al.  Partial purine deprivation causes sporulation of Bacillus subtilis in the presence of excess ammonia, glucose and phosphate. , 1979, Journal of general microbiology.

[5]  A. Dromerick,et al.  Response of Guanosine 5′-Triphosphate Concentration to Nutritional Changes and Its Significance for Bacillus subtilis Sporulation , 1981, Journal of bacteriology.

[6]  Alexander Varshavsky,et al.  Mapping proteinDNA interactions in vivo with formaldehyde: Evidence that histone H4 is retained on a highly transcribed gene , 1988, Cell.

[7]  I. Smith,et al.  Regulation of procaryotic development , 1989 .

[8]  A. Fouet,et al.  A target for carbon source-dependent negative regulation of the citB promoter of Bacillus subtilis , 1990, Journal of bacteriology.

[9]  L. Wray,et al.  Regulation of histidine and proline degradation enzymes by amino acid availability in Bacillus subtilis , 1990, Journal of bacteriology.

[10]  J. Hoch,et al.  The transition state regulator Hpr of Bacillus subtilis is a DNA-binding protein. , 1991, The Journal of biological chemistry.

[11]  A. Sonenshein,et al.  A Bacillus subtilis dipeptide transport system expressed early during sporulation , 1991, Molecular microbiology.

[12]  J. Hoch,et al.  Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay , 1991, Cell.

[13]  M. Nakano,et al.  Transcription initiation region of the srfA operon, which is controlled by the comP-comA signal transduction system in Bacillus subtilis , 1991, Journal of bacteriology.

[14]  F. Kawamura,et al.  Differential regulation of spo0A transcription in Bacillus subtilis: glucose represses promoter switching at the initiation of sporulation , 1991, Journal of bacteriology.

[15]  A. Sonenshein,et al.  Role of the Bacillus subtilis gsiA gene in regulation of early sporulation gene expression , 1992, Journal of bacteriology.

[16]  R. Losick,et al.  Bacillus Subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics , 1993 .

[17]  M. Strauch AbrB, a Transition State Regulator , 1993 .

[18]  J. Hoch,et al.  Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway , 1993, Molecular microbiology.

[19]  J. Hoch Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis. , 1993, Annual review of microbiology.

[20]  A. Grossman,et al.  Activation of spo0A transcription by sigma H is necessary for sporulation but not for competence in Bacillus subtilis , 1994, Journal of bacteriology.

[21]  D. Dubnau,et al.  The regulation of competence transcription factor synthesis constitutes a critical control point in the regulation of competence in Bacillus subtilis , 1994, Journal of bacteriology.

[22]  F. Slack,et al.  A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon , 1995, Molecular microbiology.

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

[24]  J. L. San Millán,et al.  Structure and organization of plasmid genes required to produce the translation inhibitor microcin C7 , 1995, Journal of bacteriology.

[25]  E. Newman,et al.  The Leucine\Lrp Regulon , 1996 .

[26]  S. Fisher,et al.  Role of CodY in regulation of the Bacillus subtilis hut operon , 1996, Journal of bacteriology.

[27]  P. Serror,et al.  CodY is required for nutritional repression of Bacillus subtilis genetic competence , 1996, Journal of bacteriology.

[28]  S. Fisher,et al.  Expression of the Bacillus subtilis gabP gene is regulated independently in response to nitrogen and amino acid availability , 1996, Molecular microbiology.

[29]  J. Hoch,et al.  Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  A. Sonenshein,et al.  Interaction of Cody, a novel Bacillus subtillis DNA‐binding protein, with the dpp promoter region , 1996, Molecular microbiology.

[31]  J. Hoch,et al.  Alterations in the flow of one‐carbon units affect KinB‐dependent sporulation in Bacillus subtilis , 1997, Molecular microbiology.

[32]  A. Sonenshein,et al.  An lrp-like gene of Bacillus subtilis involved in branched-chain amino acid transport , 1997, Journal of bacteriology.

[33]  L. Wray,et al.  Expression of the Bacillus subtilis ureABC operon is controlled by multiple regulatory factors including CodY, GlnR, TnrA, and Spo0H , 1997, Journal of bacteriology.

[34]  A. Grossman,et al.  Identification and Characterization of a Bacterial Chromosome Partitioning Site , 1998, Cell.

[35]  S. Ehrlich,et al.  A vector for systematic gene inactivation in Bacillus subtilis. , 1998, Microbiology.

[36]  A. Grossman,et al.  Control of development by altered localization of a transcription factor in B. subtilis. , 1999, Molecular cell.

[37]  I. Kurtser,et al.  An Autoregulatory Circuit Affecting Peptide Signaling in Bacillus subtilis , 1999, Journal of bacteriology.

[38]  S. Fisher,et al.  Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence! , 1999, Molecular microbiology.

[39]  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.

[40]  Y. Fujita,et al.  Systematic study of gene expression and transcription organization in the gntZ-ywaA region of the Bacillus subtilis genome. , 2000, Microbiology.

[41]  Min Jiang,et al.  Differential Processing of Propeptide Inhibitors of Rap Phosphatases in Bacillus subtilis , 2000, Journal of bacteriology.

[42]  J. Frère,et al.  The dppA gene of Bacillus subtilis encodes a new d‐aminopeptidase , 2000, Molecular microbiology.

[43]  John J. Wyrick,et al.  Genome-wide location and function of DNA binding proteins. , 2000, Science.

[44]  M. Zouine,et al.  Characterization of LrpC DNA-Binding Properties and Regulation of Bacillus subtilis lrpC Gene Expression , 2000, Journal of bacteriology.

[45]  R. Losick,et al.  The transcriptional profile of early to middle sporulation in Bacillus subtilis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  A. Grossman,et al.  Regulation of the Initiation of Endospore Formation in Bacillus subtilis , 2000 .

[47]  D. Mirel,et al.  Environmental Regulation of Bacillus subtilis ςD-Dependent Gene Expression , 2000, Journal of bacteriology.

[48]  A. Sonenshein,et al.  CcpC, a novel regulator of the LysR family required for glucose repression of the citB gene in Bacillus subtilis. , 2000, Journal of molecular biology.

[49]  K. Taira,et al.  cis‐Acting regulatory sequences for antitermination in the transcript of the Bacillus subtilis hut operon and histidine‐dependent binding of HutP to the transcript containing the regulatory sequences , 2000, Molecular microbiology.

[50]  E. Ferrari,et al.  Correlation between Bacillus subtilis scoC Phenotype and Gene Expression Determined Using Microarrays for Transcriptome Analysis , 2001, Journal of Bacteriology.

[51]  P. Renault,et al.  Transcriptional Pattern of Genes Coding for the Proteolytic System of Lactococcus lactis and Evidence for Coordinated Regulation of Key Enzymes by Peptide Supply , 2001, Journal of bacteriology.

[52]  A. Sonenshein,et al.  Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. , 2001, Genes & development.

[53]  D. Botstein,et al.  Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF , 2001, Nature.

[54]  R. Losick,et al.  Bacillus Subtilis and Its Closest Relatives: From Genes to Cells , 2001 .

[55]  Yasutaro Fujita,et al.  Involvement of Two Distinct Catabolite-Responsive Elements in Catabolite Repression of the Bacillus subtilis myo-Inositol (iol) Operon , 2001, Journal of bacteriology.

[56]  T. Tanaka,et al.  DNA microarray analysis of Bacillus subtilis DegU, ComA and PhoP regulons: an approach to comprehensive analysis of B.subtilis two-component regulatory systems. , 2001, Nucleic acids research.

[57]  Naotake Ogasawara,et al.  Comprehensive DNA Microarray Analysis ofBacillus subtilis Two-Component Regulatory Systems , 2001, Journal of bacteriology.

[58]  P. Renault,et al.  Pleiotropic transcriptional repressor CodY senses the intracellular pool of branched‐chain amino acids in Lactococcus lactis , 2001, Molecular microbiology.

[59]  K. Kobayashi,et al.  Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. , 2001, Nucleic acids research.

[60]  J. Gerlt,et al.  Evolution of enzymatic activities in the enolase superfamily: functional assignment of unknown proteins in Bacillus subtilis and Escherichia coli as L-Ala-D/L-Glu epimerases. , 2001, Biochemistry.

[61]  C. Price,et al.  General Stress Response , 2002 .

[62]  Patrick Eichenberger,et al.  Genome-Wide Analysis of the Stationary-Phase Sigma Factor (Sigma-H) Regulon of Bacillus subtilis , 2002, Journal of bacteriology.

[63]  Michael Hecker,et al.  Transcriptome and Proteome Analysis of Bacillus subtilis Gene Expression Modulated by Amino Acid Availability , 2002, Journal of bacteriology.

[64]  M. Hecker,et al.  Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis , 2002, Journal of bacteriology.

[65]  Leighton J. Core,et al.  Biochemical Characterization of Aspartyl Phosphate Phosphatase Interaction with a Phosphorylated Response Regulator and Its Inhibition by a Pentapeptide* , 2002, The Journal of Biological Chemistry.

[66]  K. Ochi,et al.  RelA Protein Is Involved in Induction of Genetic Competence in Certain Bacillus subtilis Strains by Moderating the Level of Intracellular GTP , 2002, Journal of bacteriology.

[67]  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.

[68]  Lucy Shapiro,et al.  Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[69]  A. Sonenshein,et al.  Direct and indirect roles of CcpA in regulation of Bacillus subtilis Krebs cycle genes , 2002, Molecular microbiology.

[70]  Isabelle Martin-Verstraete,et al.  Carbohydrate Uptake and Metabolism , 2002 .

[71]  Hyun-Jin Kim,et al.  Complex Regulation of the Bacillus subtilis Aconitase Gene , 2003, Journal of bacteriology.