Processing of a sporulation sigma factor in Bacillus subtilis: How morphological structure could control gene expression

Sporulation of Bacillus subtilis is a primitive example of coupling between morphological changes and timing of gene expression during development. A major early control of transcriptional activity is dependent on a new sigma factor, sigma E, which is encoded by the sigE gene and synthesized as an inactive precursor, pro-sigma E. We show that mutations in the spoIIGA gene block the processing of pro-sigma E. Moreover, synthesis of both spoIIGA and sigE products in vegetative cells leads to expression of a sigma E-controlled promoter during growth, suggesting that SpoIIGA has pro-sigma E processing activity. The SpoIIGA polypeptide, which contains five potential transmembrane domains, is synthesized during sporulation 1 hr before processing activity can be detected. We propose that SpoIIGA processing activity is triggered by the presence of the sporulation septum, which is itself dependent on the spoIIAA and spoIIE products. These proteins are normally needed for pro-sigma E processing during sporulation but can be bypassed in vegetative cells. According to this model, a morphological structure would directly control the synthesis of a developmental sigma factor and would modify gene expression.

[1]  W. Haldenwang,et al.  Sporulation-specific sigma factor sigma 29 of Bacillus subtilis is synthesized from a precursor protein, P31. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[2]  K. Chak,et al.  Facile in vivo transfer of mutations between the Bacillus subtilis chromosome and a plasmid harbouring homologous DNA. , 1982, Journal of general microbiology.

[3]  Frederick M. Ausubel,et al.  Conserved domains in bacterial regulatory proteins that respond to environmental stimuli , 1987, Cell.

[4]  J. Mandelstam,et al.  Duplicated sporulation genes in bacteria , 1985 .

[5]  D. Henner,et al.  Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis. , 1986, Gene.

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

[7]  J. Hoch,et al.  Construction and properties of an integrable plasmid for Bacillus subtilis , 1983, Journal of bacteriology.

[8]  P. Piggot,et al.  Use of integrational plasmid vectors to demonstrate the polycistronic nature of a transcriptional unit (spoIIA) required for sporulation of Bacillus subtilis. , 1984, Journal of general microbiology.

[9]  R. Losick,et al.  A sporulation-induced sigma-like regulatory protein from b. subtilis , 1981, Cell.

[10]  D. Eisenberg Three-dimensional structure of membrane and surface proteins. , 1984, Annual review of biochemistry.

[11]  G. Heijne The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans‐membrane topology , 1986, The EMBO journal.

[12]  R. Losick,et al.  Cascades of sigma factors , 1981, Cell.

[13]  A. Sonenshein,et al.  Promoter-probe plasmid for Bacillus subtilis , 1984, Journal of bacteriology.

[14]  D. Henner,et al.  Use of the Escherichia coli lac repressor and operator to control gene expression in Bacillus subtilis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[15]  William R. Taylor,et al.  A structural model for the retroviral proteases , 1987, Nature.

[16]  C. Moran,et al.  The Bacillus subtilis spoIIG operon encodes both sigma E and a gene necessary for sigma E activation , 1988, Journal of bacteriology.

[17]  P. Stragier Comment on ‘Duplicated sporulation genes in bacteria’ by J. Errington, P. Fort and J. Mandelstam (FEBS Letters 188 (1985) 184‐188) , 1986, FEBS letters.

[18]  J. Mandelstam,et al.  Use of lacZ gene fusions to determine the dependence pattern of the sporulation gene spoIID in spo mutants of Bacillus subtilis. , 1986, Journal of general microbiology.

[19]  A. Sonenshein,et al.  Transcriptional control of the Bacillus subtilis spoIID gene , 1986, Journal of bacteriology.

[20]  N. Sueoka,et al.  Correction. A revision of the nucleotide sequence and functional map of pUB110. , 1987, Plasmid.

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

[22]  W. Haldenwang,et al.  Synthesis of sigma 29, an RNA polymerase specificity determinant, is a developmentally regulated event in Bacillus subtilis , 1985, Journal of bacteriology.

[23]  J. Hoch,et al.  Isolation and sequence of the spoOE gene: its role in initiation of sporulation in Bacillus subtills , 1987 .

[24]  S. Horinouchi,et al.  Nucleotide sequence and functional map of pE194, a plasmid that specifies inducible resistance to macrolide, lincosamide, and streptogramin type B antibodies , 1982, Journal of bacteriology.

[25]  J. Mandelstam,et al.  Use of a lacZ gene fusion to determine the dependence pattern of sporulation operon spoIIA in spo mutants of Bacillus subtilis. , 1986, Journal of general microbiology.

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

[27]  P. Stragier,et al.  A developmental gene product of Bacillus subtilis homologous to the sigma factor of Escherichia coli , 1984, Nature.

[28]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[29]  R. Losick,et al.  Genetics of endospore formation in Bacillus subtilis. , 1986, Annual review of genetics.

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

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

[32]  A. Sonenshein,et al.  Altered regulation of the glnA gene in glutamine synthetase mutants of Bacillus subtilis , 1986, Journal of bacteriology.

[33]  J. Mandelstam,et al.  Dependent sequences of gene expression controlling spore formation in Bacillus subtilis. , 1987, Microbiological sciences.