This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Hilbert, D. W.
Right arrow Articles by Piggot, P. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Hilbert, D. W.
Right arrow Articles by Piggot, P. J.

 Previous Article  |  Next Article 

Microbiology and Molecular Biology Reviews, June 2004, p. 234-262, Vol. 68, No. 2
1092-2172/04/$08.00+0     DOI: 10.1128/MMBR.68.2.234-262.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation

David W. Hilbert{dagger} and Patrick J. Piggot*

Department of Microbiology and Immunology, Temple University School of Medicine, Philadelphia, Pennsylvania 19140

Gene expression in members of the family Bacillaceae becomes compartmentalized after the distinctive, asymmetrically located sporulation division. It involves complete compartmentalization of the activities of sporulation-specific sigma factors, {sigma}F in the prespore and then {sigma}E in the mother cell, and then later, following engulfment, {sigma}G in the prespore and then {sigma}K in the mother cell. The coupling of the activation of {sigma}F to septation and {sigma}G to engulfment is clear; the mechanisms are not. The {sigma} factors provide the bare framework of compartment-specific gene expression. Within each {sigma} regulon are several temporal classes of genes, and for key regulators, timing is critical. There are also complex intercompartmental regulatory signals. The determinants for {sigma}F regulation are assembled before septation, but activation follows septation. Reversal of the anti-{sigma}F activity of SpoIIAB is critical. Only the origin-proximal 30% of a chromosome is present in the prespore when first formed; it takes {approx}15 min for the rest to be transferred. This transient genetic asymmetry is important for prespore-specific {sigma}F activation. Activation of {sigma}E requires {sigma}F activity and occurs by cleavage of a prosequence. It must occur rapidly to prevent the formation of a second septum. {sigma}G is formed only in the prespore. SpoIIAB can block {sigma}G activity, but SpoIIAB control does not explain why {sigma}G is activated only after engulfment. There is mother cell-specific excision of an insertion element in sigK and {sigma}E-directed transcription of sigK, which encodes pro-{sigma}K. Activation requires removal of the prosequence following a {sigma}G-directed signal from the prespore.

* Corresponding author. Mailing address: Department of Microbiology and Immunology, Temple University School of Medicine, 3400 N. Broad St., Philadelphia, PA 19140. Phone: (215) 707-7927. Fax: (215) 707-7788. E-mail: piggotp{at}temple.edu.

{dagger} Present address: Department of Anatomy and Cell Biology, Columbia University, New York, NY 10032.

Microbiology and Molecular Biology Reviews, June 2004, p. 234-262, Vol. 68, No. 2
1092-2172/04/$08.00+0     DOI: 10.1128/MMBR.68.2.234-262.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Cheng, G., Zhao, P., Tang, X.-F., Tang, B. (2009). Identification and characterization of a novel spore-associated subtilase from Thermoactinomyces sp. CDF. Microbiology 155: 3661-3672 [Abstract] [Full Text]  
  • Veening, J.-W., Murray, H., Errington, J. (2009). A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev. 23: 1959-1970 [Abstract] [Full Text]  
  • Harry, K. H., Zhou, R., Kroos, L., Melville, S. B. (2009). Sporulation and Enterotoxin (CPE) Synthesis Are Controlled by the Sporulation-Specific Sigma Factors SigE and SigK in Clostridium perfringens. J. Bacteriol. 191: 2728-2742 [Abstract] [Full Text]  
  • Camp, A. H., Losick, R. (2009). A feeding tube model for activation of a cell-specific transcription factor during sporulation in Bacillus subtilis. Genes Dev. 23: 1014-1024 [Abstract] [Full Text]  
  • Chesnokova, O. N., McPherson, S. A., Steichen, C. T., Turnbough, C. L. Jr. (2009). The Spore-Specific Alanine Racemase of Bacillus anthracis and Its Role in Suppressing Germination during Spore Development. J. Bacteriol. 191: 1303-1310 [Abstract] [Full Text]  
  • Maughan, H., Birky, C. W. Jr., Nicholson, W. L. (2009). Transcriptome Divergence and the Loss of Plasticity in Bacillus subtilis after 6,000 Generations of Evolution under Relaxed Selection for Sporulation. J. Bacteriol. 191: 428-433 [Abstract] [Full Text]  
  • Serrano, M., Vieira, F., Moran, C. P. Jr., Henriques, A. O. (2008). Processing of a Membrane Protein Required for Cell-to-Cell Signaling during Endospore Formation in Bacillus subtilis. J. Bacteriol. 190: 7786-7796 [Abstract] [Full Text]  
  • Meisner, J., Wang, X., Serrano, M., Henriques, A. O., Moran, C. P. Jr (2008). A channel connecting the mother cell and forespore during bacterial endospore formation. Proc. Natl. Acad. Sci. USA 105: 15100-15105 [Abstract] [Full Text]  
  • Marquis, K. A., Burton, B. M., Nollmann, M., Ptacin, J. L., Bustamante, C., Ben-Yehuda, S., Rudner, D. Z. (2008). SpoIIIE strips proteins off the DNA during chromosome translocation. Genes Dev. 22: 1786-1795 [Abstract] [Full Text]  
  • Dong, S., McPherson, S. A., Tan, L., Chesnokova, O. N., Turnbough, C. L. Jr., Pritchard, D. G. (2008). Anthrose Biosynthetic Operon of Bacillus anthracis. J. Bacteriol. 190: 2350-2359 [Abstract] [Full Text]  
  • Sorg, J. A., Sonenshein, A. L. (2008). Bile Salts and Glycine as Cogerminants for Clostridium difficile Spores. J. Bacteriol. 190: 2505-2512 [Abstract] [Full Text]  
  • Rice, K. C., Bayles, K. W. (2008). Molecular Control of Bacterial Death and Lysis. Microbiol. Mol. Biol. Rev. 72: 85-109 [Abstract] [Full Text]  
  • Chary, V. K., Xenopoulos, P., Piggot, P. J. (2007). Expression of the {sigma}F-Directed csfB Locus Prevents Premature Appearance of {sigma}G Activity during Sporulation of Bacillus subtilis. J. Bacteriol. 189: 8754-8757 [Abstract] [Full Text]  
  • Guillot, C., Moran, C. P. Jr. (2007). Essential Internal Promoter in the spoIIIA Locus of Bacillus subtilis. J. Bacteriol. 189: 7181-7189 [Abstract] [Full Text]  
  • Campo, N., Rudner, D. Z. (2007). SpoIVB and CtpB Are Both Forespore Signals in the Activation of the Sporulation Transcription Factor {sigma}K in Bacillus subtilis. J. Bacteriol. 189: 6021-6027 [Abstract] [Full Text]  
  • Lu, Z., Takeuchi, M., Sato, T. (2007). The LysR-Type Transcriptional Regulator YofA Controls Cell Division through the Regulation of Expression of ftsW in Bacillus subtilis. J. Bacteriol. 189: 5642-5651 [Abstract] [Full Text]  
  • Bogush, M., Xenopoulos, P., Piggot, P. J. (2007). Separation of Chromosome Termini during Sporulation of Bacillus subtilis Depends on SpoIIIE. J. Bacteriol. 189: 3564-3572 [Abstract] [Full Text]  
  • Keijser, B. J. F., Ter Beek, A., Rauwerda, H., Schuren, F., Montijn, R., van der Spek, H., Brul, S. (2007). Analysis of Temporal Gene Expression during Bacillus subtilis Spore Germination and Outgrowth. J. Bacteriol. 189: 3624-3634 [Abstract] [Full Text]  
  • Hosoya, S., Lu, Z., Ozaki, Y., Takeuchi, M., Sato, T. (2007). Cytological Analysis of the Mother Cell Death Process during Sporulation in Bacillus subtilis. J. Bacteriol. 189: 2561-2565 [Abstract] [Full Text]  
  • Thompson, L. S., Beech, P. L., Real, G., Henriques, A. O., Harry, E. J. (2006). Requirement for the Cell Division Protein DivIB in Polar Cell Division and Engulfment during Sporulation in Bacillus subtilis. J. Bacteriol. 188: 7677-7685 [Abstract] [Full Text]  
  • Chary, V. K., Xenopoulos, P., Piggot, P. J. (2006). Blocking Chromosome Translocation during Sporulation of Bacillus subtilis Can Result in Prespore-Specific Activation of {sigma}G That Is Independent of {sigma}E and of Engulfment.. J. Bacteriol. 188: 7267-7273 [Abstract] [Full Text]  
  • Perry, S. E., Edwards, D. H. (2006). The Bacillus subtilis DivIVA Protein Has a Sporulation-Specific Proximity to Spo0J.. J. Bacteriol. 188: 6039-6043 [Abstract] [Full Text]  
  • Philippe, V. A., Mendez, M. B., Huang, I-H., Orsaria, L. M., Sarker, M. R., Grau, R. R. (2006). Inorganic Phosphate Induces Spore Morphogenesis and Enterotoxin Production in the Intestinal Pathogen Clostridium perfringens.. Infect. Immun. 74: 3651-3656 [Abstract] [Full Text]  
  • Hinc, K., Nagorska, K., Iwanicki, A., Wegrzyn, G., Seror, S. J., Obuchowski, M. (2006). Expression of Genes Coding for GerA and GerK Spore Germination Receptors Is Dependent on the Protein Phosphatase PrpE.. J. Bacteriol. 188: 4373-4383 [Abstract] [Full Text]  
  • McPherson, D. C., Kim, H., Hahn, M., Wang, R., Grabowski, P., Eichenberger, P., Driks, A. (2005). Characterization of the Bacillus subtilis Spore Morphogenetic Coat Protein CotO. J. Bacteriol. 187: 8278-8290 [Abstract] [Full Text]  
  • Salas-Pacheco, J. M., Setlow, B., Setlow, P., Pedraza-Reyes, M. (2005). Role of the Nfo (YqfS) and ExoA Apurinic/Apyrimidinic Endonucleases in Protecting Bacillus subtilis Spores from DNA Damage. J. Bacteriol. 187: 7374-7381 [Abstract] [Full Text]  
  • Flint, J. F., Drzymalski, D., Montgomery, W. L., Southam, G., Angert, E. R. (2005). Nocturnal Production of Endospores in Natural Populations of Epulopiscium-Like Surgeonfish Symbionts. J. Bacteriol. 187: 7460-7470 [Abstract] [Full Text]  
  • Patterson, H. M., Brannigan, J. A., Cutting, S. M., Wilson, K. S., Wilkinson, A. J., AB, E., Diercks, T., de Jong, R. N., Truffault, V., Folkers, G. E., Kaptein, R. (2005). The Structure of Bypass of Forespore C, an Intercompartmental Signaling Factor during Sporulation in Bacillus. J. Biol. Chem. 280: 36214-36220 [Abstract] [Full Text]  
  • Chary, V. K., Meloni, M., Hilbert, D. W., Piggot, P. J. (2005). Control of the Expression and Compartmentalization of {sigma}G Activity during Sporulation of Bacillus subtilis by Regulators of {sigma}F and {sigma}E. J. Bacteriol. 187: 6832-6840 [Abstract] [Full Text]  
  • Kort, R., O'Brien, A. C., van Stokkum, I. H. M., Oomes, S. J. C. M., Crielaard, W., Hellingwerf, K. J., Brul, S. (2005). Assessment of Heat Resistance of Bacterial Spores from Food Product Isolates by Fluorescence Monitoring of Dipicolinic Acid Release. Appl. Environ. Microbiol. 71: 3556-3564 [Abstract] [Full Text]  
  • Carniol, K., Ben-Yehuda, S., King, N., Losick, R. (2005). Genetic Dissection of the Sporulation Protein SpoIIE and Its Role in Asymmetric Division in Bacillus subtilis. J. Bacteriol. 187: 3511-3520 [Abstract] [Full Text]  
  • McLeod, B. N., Spiegelman, G. B. (2005). Soj Antagonizes Spo0A Activation of Transcription in Bacillus subtilis. J. Bacteriol. 187: 2532-2536 [Abstract] [Full Text]  
  • Errington, J., Murray, H., Wu, L. J. (2005). Diversity and redundancy in bacterial chromosome segregation mechanisms. Phil Trans R Soc B 360: 497-505 [Abstract] [Full Text]  
  • Scheffers, D.-J. (2005). Dynamic localization of penicillin-binding proteins during spore development in Bacillus subtilis. Microbiology 151: 999-1012 [Abstract] [Full Text]  
  • Steil, L., Serrano, M., Henriques, A. O., Volker, U. (2005). Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis. Microbiology 151: 399-420 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»