Regulation of the Initiation of Endospore Formation in Bacillus subtilis

Under certain environmental conditions, cells of the bacterium Bacillus subtilis can initiate a developmental process leading to the formation of dormant endospores. Much of the work on sporulation in B. subtilis has focused on several key questions such as What are the environmental conditions that control sporulation? The authors describe some of the regulatory circuits that control the initiation of sporulation and the conditions that influence the activity of the regulatory factors. The responses of the gram-positive soil bacterium B. subtilis to changing nutrient conditions have been studied extensively. Regulatory mechanisms exist to help ensure that cells do not initiate sporulation unless it is likely that they will be able to complete the process successfully. spo0A and spo0H encode transcription factors that are required for the initiation of sporulation. Both spo0A and spo0H are required for asymmetric division and for transcription of the genes required for establishing cell-type-specific gene expression. The genes controlled by Spo0A that are involved in formation of the axial filament and the polar FtsZ rings are not known. Extracellular and intracellular signals are generated by nutrient deprivation, cell density, DNA replication, DNA damage, glucose metabolism, the tricarboxylic acid (TCA) cycle, and chromosome-partitioning proteins. Understanding both the signals that regulate these pathways and the organization of the pathways into networks regulating gene expression will contribute significantly to an integrated view of the interplay among cell physiology, gene expression, adaptation, and development.

[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]  J. Mandelstam,et al.  Sporulation of Bacillus subtilis in Continuous Culture , 1970, Journal of bacteriology.

[3]  J. Mandelstam,et al.  Induction of Sporulation During Synchronized Chromosome Replication in Bacillus subtilis , 1974, Journal of bacteriology.

[4]  P. Piggot,et al.  Genetic aspects of bacterial endospore formation. , 1976, Bacteriological reviews.

[5]  N. Vasantha,et al.  The role of manganese in growth and sporulation of Bacillus subtilis. , 1979, Journal of general microbiology.

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

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

[8]  K. Ochi,et al.  Evidence that Bacillus subtilis sporulation induced by the stringent response is caused by the decrease in GTP or GDP , 1982, Journal of bacteriology.

[9]  J. Hoch,et al.  Identification of the transcriptional suppressor sof-1 as an alteration in the spo0A protein , 1985, Journal of bacteriology.

[10]  F. Kawamura,et al.  Catabolite-resistant sporulation (crsA) mutations in the Bacillus subtilis RNA polymerase sigma 43 gene (rpoD) can suppress and be suppressed by mutations in spo0 genes. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[11]  D. Dubnau,et al.  Expression of competence genes in Bacillus subtilis , 1987, Journal of bacteriology.

[12]  A. Grossman,et al.  Extracellular control of spore formation in Bacillus subtilis. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[13]  J. Hoch,et al.  Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis , 1989, Journal of bacteriology.

[14]  K. Nordström,et al.  Mechanisms that contribute to the stable segregation of plasmids. , 1989, Annual review of genetics.

[15]  K. Nordström,et al.  Partition-mediated incompatibility of bacterial plasmids , 1990, Cell.

[16]  P. Youngman,et al.  Novel mutations that alter the regulation of sporulation in Bacillus subtilis. Evidence that phosphorylation of regulatory protein SpoOA controls the initiation of sporulation. , 1990, Journal of molecular biology.

[17]  P. Stragier,et al.  The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes , 1990, Journal of bacteriology.

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

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

[20]  D. Dubnau,et al.  Genetic competence in Bacillus subtilis. , 1991, Microbiological reviews.

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

[22]  Christopher M Thomas,et al.  Active partitioning of bacterial plasmids. , 1992, Journal of general microbiology.

[23]  A. Sonenshein,et al.  Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system , 1992, Journal of bacteriology.

[24]  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.

[25]  H. Yoshikawa,et al.  Genes and their organization in the replication origin region of the bacterial chromosome , 1992, Molecular microbiology.

[26]  A. Grossman,et al.  Coupling between gene expression and DNA synthesis early during development in Bacillus subtilis. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Hiraga Chromosome and plasmid partition in Escherichia coli. , 1992, Annual review of biochemistry.

[28]  L. Hederstedt Krebs´ citric acid cycle , 1993 .

[29]  Characterization of a new sporulation factor in Bacillus subtilis , 1993, Journal of bacteriology.

[30]  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.

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

[32]  A. Grossman,et al.  Integration of multiple developmental signals in Bacillus subtilis through the Spo0A transcription factor. , 1993, Genes & development.

[33]  B. Bukau Regulation of the Escherichia coli heat‐shock response , 1993, Molecular microbiology.

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

[35]  I. Smith Regulatory Proteins That Control Late-Growth Development , 1993 .

[36]  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.

[37]  P. Zuber,et al.  Mutations in pts cause catabolite-resistant sporulation and altered regulation of spo0H in Bacillus subtilis , 1994, Journal of bacteriology.

[38]  A. Grossman,et al.  Gene expression in single cells of Bacillus subtilis: evidence that a threshold mechanism controls the initiation of sporulation , 1994, Journal of bacteriology.

[39]  A. Grossman,et al.  spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis , 1994, Journal of bacteriology.

[40]  A. Sonenshein,et al.  Transcriptional regulation of Bacillus subtilis citrate synthase genes , 1994, Journal of bacteriology.

[41]  A. Grossman,et al.  A developmental checkpoint couples the initiation of sporulation to DNA replication in Bacillus subtilis. , 1994, The EMBO journal.

[42]  Philippe Glaser,et al.  Multiple protein-aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in B. subtilis , 1994, Cell.

[43]  Analysis of a suppressor mutation ssb (kinC) of sur0B20 (spo0A) mutation in Bacillus subtilis reveals that kinC encodes a histidine protein kinase , 1995, Journal of bacteriology.

[44]  K. Asai,et al.  Expression of kinA and accumulation of sigma H at the onset of sporulation in Bacillus subtilis , 1995, Journal of bacteriology.

[45]  J. Errington,et al.  Characterization of cell cycle events during the onset of sporulation in Bacillus subtilis , 1995, Journal of bacteriology.

[46]  A. Grossman,et al.  Convergent sensing pathways mediate response to two extracellular competence factors in Bacillus subtilis. , 1995, Genes & development.

[47]  A. Grossman Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. , 1995, Annual review of genetics.

[48]  A. Grossman,et al.  Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis , 1995, Journal of bacteriology.

[49]  C. Moran,et al.  Evidence that the transcriptional activator Spo0A interacts with two sigma factors in Bacillus subtilis , 1995, Molecular microbiology.

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

[51]  A. Grossman,et al.  Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis , 1995, Journal of bacteriology.

[52]  I. Mandic-Mulec,et al.  Copyright � 1995, American Society for Microbiology The Bacillus subtilis SinR Protein Is a Repressor of , 1995 .

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

[54]  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.

[55]  P. Youngman,et al.  Identification of a Bacillus subtilis spo0H allele that is necessary for suppression of the sporulation-defective phenotype of a spo0A mutation , 1995, Journal of bacteriology.

[56]  Philippe Glaser,et al.  Aspartyl‐phosphate phosphatases deactivate the response regulator components of the sporulation signal transduction system in Bacillus subtilis , 1996, Molecular microbiology.

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

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

[59]  J. S. Parkinson,et al.  Signal Transduction via the Multi-Step Phosphorelay: Not Necessarily a Road Less Traveled , 1996, Cell.

[60]  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.

[61]  A. Grossman,et al.  Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. , 1996, Genes & development.

[62]  N. Xuong,et al.  Crystal structure of a phosphatase-resistant mutant of sporulation response regulator Spo0F from Bacillus subtilis. , 1996, Structure.

[63]  J. Errington,et al.  The Bacillus subtilis soj‐spo0J locus is required for a centromere‐like function involved in prespore chromosome partitioning , 1996, Molecular microbiology.

[64]  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.

[65]  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.

[66]  I. Zhulin,et al.  PAS domain S-boxes in Archaea, Bacteria and sensors for oxygen and redox. , 1997, Trends in biochemical sciences.

[67]  A. Grossman,et al.  An Exported Peptide Functions Intracellularly to Contribute to Cell Density Signaling in B. subtilis , 1997, Cell.

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

[69]  J M Whiteley,et al.  High-resolution NMR structure and backbone dynamics of the Bacillus subtilis response regulator, Spo0F: implications for phosphorylation and molecular recognition. , 1997, Biochemistry.

[70]  A. Grossman,et al.  Deletion of the Bacillus subtilis isocitrate dehydrogenase gene causes a block at stage I of sporulation , 1997, Journal of bacteriology.

[71]  M. Perego,et al.  A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[72]  P. Zuber,et al.  Regulation of Bacillus subtilis sigmaH (spo0H) and AbrB in response to changes in external pH , 1997, Journal of bacteriology.

[73]  A. Grossman,et al.  Bipolar localization of a chromosome partition protein in Bacillus subtilis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[74]  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.

[75]  J. Errington,et al.  Direct evidence for active segregation of oriC regions of the Bacillus subtilis chromosome and co‐localization with the Spo0J partitioning protein , 1997, Molecular microbiology.

[76]  C. Moran,et al.  Activation of the Bacillus subtilis spoIIG promoter requires interaction of Spo0A and the sigma subunit of RNA polymerase , 1997, Journal of bacteriology.

[77]  A. Sonenshein,et al.  A null mutation in the Bacillus subtilis aconitase gene causes a block in Spo0A-phosphate-dependent gene expression , 1997, Journal of bacteriology.

[78]  C. Ponting,et al.  PAS: a multifunctional domain family comes to light , 1997, Current Biology.

[79]  J. Errington,et al.  Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. , 1997, Genes & development.

[80]  J. Hoch,et al.  Molecular recognition in signal transduction: the interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. , 1997, Journal of molecular biology.

[81]  A. Goffeau,et al.  The complete genome sequence of the Gram-positive bacterium Bacillus subtilis , 1997, Nature.

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

[83]  N. Xuong,et al.  A response regulatory protein with the site of phosphorylation blocked by an arginine interaction: crystal structure of Spo0F from Bacillus subtilis. , 1997, Biochemistry.

[84]  J. Gober,et al.  Cell Cycle–Dependent Polar Localization of Chromosome Partitioning Proteins in Caulobacter crescentus , 1997, Cell.

[85]  J. Hoch,et al.  Formation of a novel four-helix bundle and molecular recognition sites by dimerization of a response regulator phosphotransferase. , 1998, Molecular cell.

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

[87]  Correlation of PAS domains with electron transport-associated proteins in completely sequenced microbial genomes. , 1998, Molecular microbiology.

[88]  C. Moran,et al.  A Region in the Bacillus subtilisTranscription Factor Spo0A That Is Important for spoIIGPromoter Activation , 1998, Journal of bacteriology.

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

[90]  J. Hoch,et al.  Characterization of interactions between a two-component response regulator, Spo0F, and its phosphatase, RapB. , 1998, Biochemistry.

[91]  Contributions of the Domains of the Bacillus subtilis Response Regulator Spo0A to Transcription Stimulation of the spoIIG Operon* , 1998, The Journal of Biological Chemistry.

[92]  I. Smith,et al.  An evolutionary link between sporulation and prophage induction in the structure of a repressor:anti-repressor complex. , 1998, Journal of molecular biology.

[93]  J. Hoch,et al.  Phosphorylation of the Spo0B Response Regulator Phosphotransferase of the Phosphorelay Initiating Development inBacillus subtilis * , 1998, The Journal of Biological Chemistry.

[94]  Y. Sadaie,et al.  Feedback loops involving Spo0A and AbrB in in vitro transcription of the genes involved in the initiation of sporulation in Bacillus subtilis. , 1998, Journal of biochemistry.

[95]  Richard Sparling,et al.  Regulation in the rpoS regulon of Escherichia coli , 1998 .

[96]  P. Youngman,et al.  Spo0A Mutants of Bacillus subtilis with Sigma Factor-Specific Defects in Transcription Activation , 1998, Journal of bacteriology.

[97]  J M Whiteley,et al.  Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis. , 1998, Biochemistry.

[98]  J. Hoch,et al.  Identification of communication networks in Spo0F: a model for phosphorylation‐induced conformational change and implications for activation of multiple domain bacterial response regulators , 1998, FEBS letters.

[99]  A Region in Bacillus subtilisςH Required for Spo0A-Dependent Promoter Activity , 1998 .