A positive feedback loop controls transcription of the spo0F gene, a component of the sporulation phosphorelay In Bacillus subtilis

The spo0Fgene of Bacillus subtilisencodes a protein that functions as a secondary messenger in a phosphorelay system controlling the initiation of sporulation. Transcription of the spo0F gene was known to be dependent on an intact gene for the transcription regulator Spo0A. In vitro footprint analysis revealed that Spo0A protein bound to two locations in the spo0F promoter region. Deletion of a 40 bp region upstream of one of the promoters (P2) abolished the activation of spo0Fexpression that occurs at the onset of stationary phase and sporulation. This 40 bp region contains a Spo0A‐binding site. These observations are consistent with a hypothesis that Spo0A binding to this region is responsible for activating spo0F transcription. Additionally, Spo0A binding at a downstream site could modulate the level of this activation. Since Spo0F protein is required for the formation of Spo0A∼P (the form needed for transcriptional activation) a positive feedback loop controls transcription of spo0F.

[1]  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.

[2]  P Youngman,et al.  Spo0A controls the sigma A-dependent activation of Bacillus subtilis sporulation-specific transcription unit spoIIE , 1992, Journal of bacteriology.

[3]  J. Hoch,et al.  Sequence analysis of the spo0B locus reveals a polycistronic transcription unit , 1985, Journal of bacteriology.

[4]  J. Hoch,et al.  Structural alterations in the Bacillus subtilis Spo0A regulatory protein which suppress mutations at several spo0 loci , 1990, Journal of bacteriology.

[5]  J. Stock,et al.  Signal transduction in bacteria , 1990, Nature.

[6]  P. Fort,et al.  Nucleotide sequence of sporulation locus spoIIA in Bacillus subtilis. , 1984, Journal of general microbiology.

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

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

[9]  C. Moran,et al.  Organization and regulation of an operon that encodes a sporulation-essential sigma factor in Bacillus subtilis , 1987, Journal of bacteriology.

[10]  M. Simon,et al.  Signal transduction pathways involving protein phosphorylation in prokaryotes. , 1991, Annual review of biochemistry.

[11]  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.

[12]  C. Anagnostopoulos,et al.  REQUIREMENTS FOR TRANSFORMATION IN BACILLUS SUBTILIS , 1961, Journal of bacteriology.

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

[14]  T. Kunkel.  Rapid and efficient site-specific mutagenesis without phenotypic selection. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[15]  I. Smith,et al.  Use of a versatile lacZ vector to analyze the upstream region of the Bacillus subtilis spoOF gene. , 1988, Plasmid.

[16]  I. Smith,et al.  Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by the RNA polymerase containing sigma H , 1992, Journal of bacteriology.

[17]  A. Ninfa,et al.  Protein phosphorylation and regulation of adaptive responses in bacteria. , 1989, Microbiological reviews.

[18]  C P Moran,et al.  Spo0A binds to a promoter used by sigma A RNA polymerase during sporulation in Bacillus subtilis. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. P. Gallagher,et al.  The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation , 1991, Molecular microbiology.

[20]  I. Smith,et al.  Bacillus sporulation gene spo0H codes for sigma 30 (sigma H) , 1988, Journal of bacteriology.

[21]  J. Hoch,et al.  Control of the initiation of sporulation in Bacillus subtilis by a phosphorelay. , 1991, Research in microbiology.

[22]  J. Hoch,et al.  Transcription of Bacillus subtilis subtilisin and expression of subtilisin in sporulation mutants , 1988, Journal of bacteriology.

[23]  J. Hoch,et al.  Complete sequence and transcriptional analysis of the spo0F region of the Bacillus subtilis chromosome , 1988, Journal of bacteriology.

[24]  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.

[25]  P. Stragier,et al.  Identification of a new sigma-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. , 1989, Genes & development.

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

[27]  J. Hoch,et al.  Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis , 1988, Molecular microbiology.

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

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

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

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

[32]  I. Smith,et al.  Regulation of spo0H, an early sporulation gene in bacilli , 1987, Journal of bacteriology.

[33]  J. Hoch,et al.  PHOSPHORYLATION OF THE Spo0A PROTEIN: A CUMULATIVE ENVIRONSENSORY ACTIVATION MECHANISM , 1990 .

[34]  U. Bai,et al.  Temporal regulation of the Bacillus subtilis early sporulation gene spo0F , 1990, Journal of bacteriology.

[35]  J. Hoch,et al.  Mutational dissociation of the positive and negative regulatory properties of the Spo0A sporulation transcription factor of Bacillus subtilis. , 1991, Gene.

[36]  I. Smith,et al.  Transcriptional regulation of the spo0F gene of Bacillus subtilis , 1986, Journal of bacteriology.