A Dispensable Role for Forespore-Specific Gene Expression in Engulfment of the Forespore during Sporulation ofBacillus subtilis

ABSTRACT During the stage of engulfment in the Bacillus subtilisspore formation pathway, the larger mother cell engulfs the smaller forespore. We have tested the role of forespore-specific gene expression in engulfment using two separate approaches. First, using an assay that unambiguously detects sporangia that have completed engulfment, we found that a mutant lacking the only forespore-expressed engulfment protein identified thus far, SpoIIQ, is able to efficiently complete engulfment under certain sporulation conditions. However, we have found that the mutant is defective, under all conditions, in the expression of the late-forespore-specific transcription factor ςG; thus, SpoIIQ is essential for spore production. Second, to determine if engulfment could proceed in the absence of forespore-specific gene expression, we made use of a strain in which activation of the mother cell-specific sigma factor ςE was uncoupled from forespore-specific gene expression. Remarkably, engulfment occurred in the complete absence of ςF-directed gene expression under the same conditions permissive for engulfment in the absence of SpoIIQ. Our results demonstrate that forespore-specific gene expression is not essential for engulfment, suggesting that the machinery used to move the membranes around the forespore is within the mother cell.

[1]  K. Pogliano,et al.  SpoIIB Localizes to Active Sites of Septal Biogenesis and Spatially Regulates Septal Thinning during Engulfment in Bacillus subtilis , 2000, Journal of bacteriology.

[2]  K. Pogliano,et al.  An in vivo membrane fusion assay implicates SpoIIIE in the final stages of engulfment during Bacillus subtilis sporulation. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[3]  J. Errington,et al.  Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. , 1999, Molecular cell.

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

[5]  P. D. de Boer,et al.  MinDE-Dependent Pole-to-Pole Oscillation of Division Inhibitor MinC in Escherichia coli , 1999, Journal of bacteriology.

[6]  S. Foster,et al.  Analysis of Peptidoglycan Structure from Vegetative Cells of Bacillus subtilis 168 and Role of PBP 5 in Peptidoglycan Maturation , 1999, Journal of bacteriology.

[7]  P A de Boer,et al.  Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[8]  K. Pogliano,et al.  A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation , 1999, Molecular microbiology.

[9]  A. Wright,et al.  DNA segregation: Putting chromosomes in their place , 1998, Current Biology.

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

[11]  P. Silver,et al.  Use of time‐lapse microscopy to visualize rapid movement of the replication origin region of the chromosome during the cell cycle in Bacillus subtilis , 1998, Molecular microbiology.

[12]  H. Erickson,et al.  Atomic structures of tubulin and FtsZ. , 1998, Trends in cell biology.

[13]  A. Murray,et al.  Chromosome and Low Copy Plasmid Segregation in E. coli: Visual Evidence for Distinct Mechanisms , 1997, Cell.

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

[15]  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.

[16]  P. Stragier,et al.  spoIIQ, a forespore‐expressed gene required for engulfment in Bacillus subtilis , 1997, Molecular microbiology.

[17]  L. Shapiro,et al.  Bacterial Chromosome Segregation: Is There a Mitotic Apparatus? , 1997, Cell.

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

[19]  A. Grossman,et al.  Bipolar Localization of the Replication Origin Regions of Chromosomes in Vegetative and Sporulating Cells of B. subtilis , 1997, Cell.

[20]  R. Losick,et al.  Disappearance of the s 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 .

[21]  R. Losick,et al.  Identification of additional genes under the control of the transcription factor sigma F of Bacillus subtilis , 1996, Journal of bacteriology.

[22]  M. Karow,et al.  Analysis of the role of prespore gene expression in the compartmentalization of mother cell-specific gene expression during sporulation of Bacillus subtilis , 1996, Journal of bacteriology.

[23]  J. Errington,et al.  Structure, function and controls in microbial division , 1996, Molecular microbiology.

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

[25]  R. Losick,et al.  Activation of Cell-Specific Transcription by a Serine Phosphatase at the Site of Asymmetric Division , 1995, Science.

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

[27]  M. Karow,et al.  Construction of gusA transcriptional fusion vectors for Bacillus subtilis and their utilization for studies of spore formation. , 1995, Gene.

[28]  P. Glaser,et al.  Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  P. Stragier,et al.  Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis. , 1995, Genes & development.

[30]  P. Stragier,et al.  Identification and characterization of the Bacillus subtilis spoIIP locus , 1995, Journal of bacteriology.

[31]  J. Errington,et al.  Role of interactions between SpoIIAA and SpoIIAB in regulating cell-specific transcription factor sigma F of Bacillus subtilis. , 1994, Genes & development.

[32]  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.

[33]  J. Errington,et al.  σ F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-σ factor that is also a protein kinase , 1993, Cell.

[34]  P. Youngman,et al.  Physical and functional characterization of the Bacillus subtilis spoIIM gene , 1993, Journal of bacteriology.

[35]  J. Errington,et al.  The importance of morphological events and intercellular interactions in the regulation of prespore‐specific gene expression during sporulation in Bacillus subtilis , 1993, Molecular microbiology.

[36]  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.

[37]  R. Losick,et al.  Sporulation gene spoIIB from Bacillus subtilis , 1993, Journal of bacteriology.

[38]  J. Errington,et al.  Sigma F, the first compartment-specific transcription factor of B. subtilis, is regulated by an anti-sigma factor that is also a protein kinase. , 1993, Cell.

[39]  D. Sun,et al.  Effect of chromosome location of Bacillus subtilis forespore genes on their spo gene dependence and transcription by E sigma F: identification of features of good E sigma F-dependent promoters , 1991, Journal of bacteriology.

[40]  R. Losick,et al.  Establishment of cell type by compartmentalized activation of a transcription factor. , 1991, Science.

[41]  N. Illing,et al.  Genetic regulation of morphogenesis in Bacillus subtilis: roles of sigma E and sigma F in prespore engulfment , 1991, Journal of bacteriology.

[42]  D. Sun,et al.  Control of transcription of the Bacillus subtilis spoIIIG gene, which codes for the forespore-specific transcription factor sigma G , 1991, Journal of bacteriology.

[43]  R. Losick,et al.  Control of developmental transcription factor sigma F by sporulation regulatory proteins SpoIIAA and SpoIIAB in Bacillus subtilis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[44]  P. Stragier,et al.  Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis. , 1989, Genes & development.

[45]  P. Stragier,et al.  Processing of a sporulation sigma factor in Bacillus subtilis: How morphological structure could control gene expression , 1988, Cell.

[46]  J. M. Mason,et al.  Regulation of expression of genes coding for small, acid-soluble proteins of Bacillus subtilis spores: studies using lacZ gene fusions , 1988, Journal of bacteriology.

[47]  J. Mandelstam,et al.  spoIID operon of Bacillus subtilis: cloning and sequence. , 1986, Journal of general microbiology.

[48]  H. Cheung,et al.  Rates of peptidoglycan turnover and cell growth of Bacillus subtilis are correlated , 1983, Journal of bacteriology.

[49]  J. Mandelstam,et al.  Variety of sporulation phenotypes resulting from mutations in a single regulatory locus, spoIIA, in Bacillus subtilis. , 1983, Journal of general microbiology.

[50]  W. de Boer,et al.  Cell wall turnover in growing and nongrowing cultures of Bacillus subtilis , 1982, Journal of bacteriology.

[51]  W. de Boer,et al.  Cell wall metabolism in Bacillus subtilis subsp. niger: effects of changes in phosphate supply to the culture , 1981, Journal of bacteriology.

[52]  W. de Boer,et al.  Effects of carbon source and growth rate on cell wall composition of Bacillus subtilis subsp. niger , 1980, Journal of bacteriology.

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

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

[55]  D. Dubnau,et al.  Fate of transforming DNA following uptake by competent Bacillus subtilis. I. Formation and properties of the donor-recipient complex. , 1971 .

[56]  J. Mandelstam,et al.  Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance. , 1969, The Biochemical journal.

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