Bacillus subtilis sporulation and stationary phase gene expression

Abstract.Bacillus subtilis cells entering stationary phase due to nutrient deprivation have a number of options. Complex interconnected regulatory circuits govern differential gene expression patterns that channel the cell along the path it has sensed is most advantageous for survival in the environment. The actual choice depends upon the activity of an elaborate signal transduction network (the phosphorelay) that ultimately affects the activity of two key transcription factors, Spo0A and AbrB. Should the cell commit to sporulation, a temporally and spatially controlled cascade of RNA polymerase sigma factors leads to the development and release of an endospore from within the terminally differentiated, apoptotic mother cell.

[1]  J. Helmann,et al.  Mutations in Multidrug Efflux Homologs, Sugar Isomerases, and Antimicrobial Biosynthesis Genes Differentially Elevate Activity of the ςX and ςW Factors inBacillus subtilis , 2000, Journal of bacteriology.

[2]  J. Helmann,et al.  Promoter Recognition by Bacillus subtilisςW: Autoregulation and Partial Overlap with the ςX Regulon , 1998 .

[3]  D. Dubnau,et al.  The major role of Spo0A in genetic competence is to downregulate abrB, an essential competence gene , 1995, Journal of bacteriology.

[4]  R. Losick,et al.  Negative regulation of the proteolytic activation of a developmental transcription factor in Bacillus subtilis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. Hoch,et al.  Two-component and phosphorelay signal transduction. , 2000, Current opinion in microbiology.

[6]  R. Losick,et al.  The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. , 1990, Genes & development.

[7]  Victoria A. Feher,et al.  Two-Component Signal Transduction in Bacillus subtilis: How One Organism Sees Its World , 1999, Journal of bacteriology.

[8]  J. Hoch Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System , 1995 .

[9]  J. Errington,et al.  Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. , 1994, Science.

[10]  R. Losick,et al.  Sporulation operon spoIVF and the characterization of mutations that uncouple mother-cell from forespore gene expression in Bacillus subtilis. , 1991, Journal of molecular biology.

[11]  M. Strauch,et al.  AbrB modulates expression and catabolite repression of a Bacillus subtilis ribose transport operon , 1995, Journal of bacteriology.

[12]  R. Losick,et al.  Post‐transcriptional control of a sporulation regulatory gene encoding transcription factor σH in Bacillus subtilis , 1991, Molecular microbiology.

[13]  J. Wang,et al.  Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. , 2000, Science.

[14]  J. Hoch,et al.  A novel histidine kinase inhibitor regulating development in Bacillus subtilis. , 1997, Genes & development.

[15]  J. Hoch,et al.  Transition‐state regulators: sentinels of Bacillus subtilis post‐exponential gene expression , 1993, Molecular microbiology.

[16]  E. M. Kellner,et al.  Two‐stage regulation of an anti‐sigma factor determines developmental fate during bacterial endospore formation , 1996, Molecular microbiology.

[17]  J. Hoch,et al.  Spo0A activates and represses its own synthesis by binding at its dual promoters. , 1992, Biochimie.

[18]  M. Yudkin,et al.  Fate of the SpoIIAB*-ADP Liberated after SpoIIAB Phosphorylates SpoIIAA of Bacillus subtilis , 2000, Journal of bacteriology.

[19]  R. Losick,et al.  Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in B. subtilis , 1995, Cell.

[20]  Moir,et al.  The expression of the protective antigen of Bacillusanthracis in Bacillus subtilis , 1998, Journal of applied microbiology.

[21]  U. Bai,et al.  SinI modulates the activity of SinR, a developmental switch protein of Bacillus subtilis, by protein-protein interaction. , 1993, Genes & development.

[22]  P. Stragier,et al.  Transient gene asymmetry during sporulation and establishment of cell specificity in Bacillus subtilis. , 1999, Genes & development.

[23]  J. Hoch,et al.  The transition state transcription regulator AbrB of Bacillus subtilis is autoregulated during vegetative growth , 1989, Molecular microbiology.

[24]  J. Errington,et al.  Postseptational chromosome partitioning in bacteria. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Hoch,et al.  Sequence analysis and regulation of the hpr locus, a regulatory gene for protease production and sporulation in Bacillus subtilis , 1988, Journal of bacteriology.

[26]  R. Losick,et al.  SpoIIAB is an anti-sigma factor that binds to and inhibits transcription by regulatory protein sigma F from Bacillus subtilis. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Hoch,et al.  Genetic analysis of a class of polymyxin resistant partial revertants of stage O sporulation mutants of Bacillus subtilis: Map of the chromosome region near the origin of replication , 1979, Molecular and General Genetics MGG.

[28]  J. Hoch,et al.  The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

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

[30]  J. Hoch,et al.  The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein. , 1989, The EMBO journal.

[31]  P. Youngman,et al.  Phosphorylation of Bacillus subtilis transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes , 1994, Journal of bacteriology.

[32]  A. Sonenshein Endospore-Forming Bacteria: an Overview , 2000 .

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

[34]  R. Losick,et al.  The kinase activity of the antisigma factor SpoIIAB is required for activation as well as inhibition of transcription factor sigmaF during sporulation in Bacillus subtilis. , 1998, Journal of molecular biology.

[35]  P. Wakeley,et al.  Proteolysis of SpoIVB is a critical determinant in signalling of Pro‐σK processing in Bacillus subtilis , 2000, Molecular microbiology.

[36]  J. Hoch,et al.  cis‐Unsaturated fatty acids specifically inhibit a signal‐transducing protein kinase required for initiation of sporulation in Bacillus subtilis , 1992, Molecular microbiology.

[37]  G. Rapoport,et al.  A Signal Transduction Network in Bacillus subtilis Includes the DegS/DegU and ComP/ComA Two-Component Systems , 1995 .

[38]  J. Hoch,et al.  Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis , 2000, Molecular microbiology.

[39]  R. Losick,et al.  Molecular genetics of sporulation in Bacillus subtilis. , 1996, Annual review of genetics.

[40]  J. Hoch,et al.  Identification of a membrane protein involved in activation of the KinB pathway to sporulation in Bacillus subtilis , 1996, Journal of bacteriology.

[41]  I. Smith,et al.  Structure and expression of the Bacillus subtilis sin operon , 1988, Journal of bacteriology.

[42]  A. Driks,et al.  Regulation of Synthesis of the Bacillus subtilis Transition-Phase, Spore-Associated Antibacterial Protein TasA , 1999, Journal of bacteriology.

[43]  I. Smith,et al.  Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor , 1991, Journal of bacteriology.

[44]  R. Losick,et al.  Disappearance of the sigma E transcription factor from the forespore and the SpoIIE phosphatase from the mother cell contributes to establishment of cell-specific gene expression during sporulation in Bacillus subtilis , 1997, Journal of bacteriology.

[45]  R. Losick,et al.  Localization of the sporulation protein SpoIIE in Bacillus subtilis is dependent upon the cell division protein FtsZ , 1997, Molecular microbiology.

[46]  J. Hoch,et al.  Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[47]  P. Stragier,et al.  The SpoIIE phosphatase, the sporulation septum and the establishment of forespore‐specific transcription in Bacillus subtilis: a reassessment , 1999, Molecular microbiology.

[48]  J. Hoch,et al.  A negative regulator linking chromosome segregation to developmental transcription in Bacillus subtilis , 1998, Molecular microbiology.

[49]  R. Losick,et al.  Localization of Protein Implicated in Establishment of Cell Type to Sites of Asymmetric Division , 1995, Science.

[50]  A. Grossman,et al.  Krebs cycle function is required for activation of the Spo0A transcription factor in Bacillus subtilis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[51]  B. Lazazzera,et al.  Quorum sensing and starvation: signals for entry into stationary phase. , 2000, Current opinion in microbiology.

[52]  R. Losick,et al.  Characterization of bofA, a gene involved in intercompartmental regulation of pro-sigma K processing during sporulation in Bacillus subtilis , 1992, Journal of bacteriology.

[53]  J. Vederas,et al.  Genes of the sbo-alb Locus ofBacillus subtilis Are Required for Production of the Antilisterial Bacteriocin Subtilosin , 1999, Journal of bacteriology.

[54]  L. Ornella,et al.  De novo fatty acid synthesis is required for establishment of cell type‐specific gene transcription during sporulation in Bacillus subtilis , 1998, Molecular microbiology.

[55]  M. Strauch In vitro binding affinity of the Bacillus subtilis AbrB protein to six different DNA target regions , 1995, Journal of bacteriology.

[56]  W. Haldenwang,et al.  The Bacillus subtilis GTP Binding Protein Obg and Regulators of the ςB Stress Response Transcription Factor Cofractionate with Ribosomes , 2000, Journal of bacteriology.

[57]  Wei Liu,et al.  Pho signal transduction network reveals direct transcriptional regulation of one two‐component system by another two‐component regulator: Bacillus subtilis PhoP directly regulates production of ResD , 1998, Molecular microbiology.

[58]  R. Losick,et al.  Asymmetric Division and Cell Fate during Sporulation in Bacillus subtilis , 2000 .

[59]  M. Marahiel,et al.  AbrB, a regulator of gene expression in Bacillus, interacts with the transcription initiation regions of a sporulation gene and an antibiotic biosynthesis gene. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Losick,et al.  Crisscross regulation of cell-type-specific gene expression during development in B. subtilis , 1992, Nature.

[61]  M. Strauch Regulation of Bacillus subtilis gene expression during the transition from exponential growth to stationary phase. , 1993, Progress in nucleic acid research and molecular biology.

[62]  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.

[63]  J. Hoch,et al.  Negative regulation of Bacillus subtilis sporulation by the spo0E gene product , 1991, Journal of bacteriology.

[64]  A. Hofmeister Activation of the Proprotein Transcription Factor Pro-ςE Is Associated with Its Progression through Three Patterns of Subcellular Localization during Sporulation in Bacillus subtilis , 1998, Journal of bacteriology.

[65]  J. Hoch,et al.  A positive feedback loop controls transcription of the spo0F gene, a component of the sporulation phosphorelay In Bacillus subtilis , 1993, Molecular microbiology.

[66]  J. Hoch,et al.  The Bacillus subtilis spo0B stage 0 sporulation operon encodes an essential GTP-binding protein , 1989, Journal of bacteriology.

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

[68]  I. Smith,et al.  Characterization of a cloned Bacillus subtilis gene that inhibits sporulation in multiple copies , 1986, Journal of bacteriology.

[69]  M. Strauch,et al.  In vitro selection of optimal AbrB‐binding sites: comparison to known in vivo sites indicates flexibility in AbrB binding and recognition of three‐dimensional DNA structures , 1996, Molecular microbiology.

[70]  G. Spiegelman,et al.  DNA strand separation during activation of a developmental promoter by the Bacillus subtilis response regulator Spo0A. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[72]  I. Smith,et al.  The Bacillus subtilis sin gene, a regulator of alternate developmental processes, codes for a DNA-binding protein , 1991, Journal of bacteriology.

[73]  J. Hoch,et al.  KapB is a lipoprotein required for KinB signal transduction and activation of the phosphorelay to sporulation in Bacillus subtilis , 1997, Molecular microbiology.

[74]  J. Hoch,et al.  ScoC Regulates Peptide Transport and Sporulation Initiation in Bacillus subtilis , 1999, Journal of bacteriology.

[75]  The Bacillus subtilis response regulator Spo0A stimulates transcription of the spoIIG operon through modification of RNA polymerase promoter complexes. , 1996, Journal of molecular biology.

[76]  S. Cutting,et al.  A compartmentalized regulator of developmental gene expression in Bacillus subtilis , 1996, Journal of bacteriology.

[77]  M. Strauch,et al.  Delineation of AbrB-binding sites on the Bacillus subtilis spo0H, kinB, ftsAZ, and pbpE promoters and use of a derived homology to identify a previously unsuspected binding site in the bsuB1 methylase promote , 1995, Journal of bacteriology.

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

[79]  M. Strauch,et al.  Novel DNA binding domain and genetic regulation model of Bacillus subtilis transition state regulator AbrB , 2000, Nature Structural Biology.

[80]  R. Losick,et al.  Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. , 1996, Genes & development.

[81]  P. Miller,et al.  Overlaps and parallels in the regulation of intrinsic multiple‐antibiotic resistance in Escherichia coli , 1996, Molecular microbiology.