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 Lazazzera, B. A.
Right arrow Articles by Grossman, A. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lazazzera, B. A.
Right arrow Articles by Grossman, A. D.

 Previous Article  |  Next Article 

Journal of Bacteriology, September 1999, p. 5193-5200, Vol. 181, No. 17
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

An Autoregulatory Circuit Affecting Peptide Signaling in Bacillus subtilis

Beth A. Lazazzera, Iren G. Kurtser, Ryan S. McQuade, and Alan D. Grossman*

Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139

Received 30 September 1998/Accepted 16 June 1999

The competence and sporulation factor (CSF) of Bacillus subtilis is an extracellular pentapeptide produced from the product of phrC. CSF has at least three activities: (i) at low concentrations, it stimulates expression of genes activated by the transcription factor ComA; at higher concentrations, it (ii) inhibits expression of those same genes and (iii) stimulates sporulation. Because the activities of CSF are concentration dependent, we measured the amount of extracellular CSF produced by cells. We found that by mid-exponential phase, CSF accumulated to concentrations (1 to 5 nM) that stimulate ComA-dependent gene expression. Upon entry into stationary phase, CSF reached 50 to 100 nM, concentrations that stimulate sporulation and inhibit ComA-dependent gene expression. Transcription of phrC was found to be controlled by two promoters: P1, which precedes rapC, the gene upstream of phrC; and P2, which directs transcription of phrC only. Both RapC and CSF were found to be part of autoregulatory loops that affect transcription from P1, which we show is activated by ComA~P. RapC negatively regulates its own expression, presumably due to its ability to inhibit accumulation of ComA~P. CSF positively regulates its own expression, presumably due to its ability to inhibit RapC activity. Transcription from P2, which is controlled by the alternate sigma factor sigma H, increased as cells entered stationary phase, contributing to the increase in extracellular CSF at this time. In addition to controlling transcription of phrC, sigma H appears to control expression of at least one other gene required for production of CSF.

* Corresponding author. Mailing address: Department of Biology, Building 68-530, Massachusetts Institute of Technology, Cambridge, MA 02139. Phone: (617) 253-1515. Fax: (617) 253-2643. E-mail: adg{at}mit.edu.

Journal of Bacteriology, September 1999, p. 5193-5200, Vol. 181, No. 17
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Lopez, D., Vlamakis, H., Losick, R., Kolter, R. (2009). Paracrine signaling in a bacterium. Genes Dev. 23: 1631-1638 [Abstract] [Full Text]  
  • Bischofs, I. B., Hug, J. A., Liu, A. W., Wolf, D. M., Arkin, A. P. (2009). Complex Systems: From Chemistry to Systems Biology Special Feature: Complexity in bacterial cell-cell communication: Quorum signal integration and subpopulation signaling in the Bacillus subtilis phosphorelay. Proc. Natl. Acad. Sci. USA 106: 6459-6464 [Abstract] [Full Text]  
  • Hamze, K., Julkowska, D., Autret, S., Hinc, K., Nagorska, K., Sekowska, A., Holland, I. B., Seror, S. J. (2009). Identification of genes required for different stages of dendritic swarming in Bacillus subtilis, with a novel role for phrC. Microbiology 155: 398-412 [Abstract] [Full Text]  
  • Nandy, S. K., Prasad, V., Venkatesh, K. V. (2008). Effect of Temperature on the Cannibalistic Behavior of Bacillus subtilis. Appl. Environ. Microbiol. 74: 7427-7430 [Abstract] [Full Text]  
  • Lanigan-Gerdes, S., Briceno, G., Dooley, A. N., Faull, K. F., Lazazzera, B. A. (2008). Identification of Residues Important for Cleavage of the Extracellular Signaling Peptide CSF of Bacillus subtilis from Its Precursor Protein. J. Bacteriol. 190: 6668-6675 [Abstract] [Full Text]  
  • Mitrophanov, A. Y., Groisman, E. A. (2008). Signal integration in bacterial two-component regulatory systems. Genes Dev. 22: 2601-2611 [Abstract] [Full Text]  
  • Pottathil, M., Jung, A., Lazazzera, B. A. (2008). CSF, a Species-Specific Extracellular Signaling Peptide for Communication among Strains of Bacillus subtilis and Bacillus mojavensis. J. Bacteriol. 190: 4095-4099 [Abstract] [Full Text]  
  • Belitsky, B. R., Sonenshein, A. L. (2008). Genetic and Biochemical Analysis of CodY-Binding Sites in Bacillus subtilis. J. Bacteriol. 190: 1224-1236 [Abstract] [Full Text]  
  • Duitman, E. H., Wyczawski, D., Boven, L. G., Venema, G., Kuipers, O. P., Hamoen, L. W. (2007). Novel Methods for Genetic Transformation of Natural Bacillus subtilis Isolates Used To Study the Regulation of the Mycosubtilin and Surfactin Synthetases. Appl. Environ. Microbiol. 73: 3490-3496 [Abstract] [Full Text]  
  • Tanous, C., Chambellon, E., Yvon, M. (2007). Sequence analysis of the mobilizable lactococcal plasmid pGdh442 encoding glutamate dehydrogenase activity. Microbiology 153: 1664-1675 [Abstract] [Full Text]  
  • Auchtung, J. M., Lee, C. A., Grossman, A. D. (2006). Modulation of the ComA-Dependent Quorum Response in Bacillus subtilis by Multiple Rap Proteins and Phr Peptides.. J. Bacteriol. 188: 5273-5285 [Abstract] [Full Text]  
  • Ohsawa, T., Tsukahara, K., Sato, T., Ogura, M. (2006). Superoxide Stress Decreases Expression of srfA through Inhibition of Transcription of the comQXP Quorum-Sensing Locus in Bacillus subtilis. J Biochem 139: 203-211 [Abstract] [Full Text]  
  • Guedon, E., Sperandio, B., Pons, N., Ehrlich, S. D., Renault, P. (2005). Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology 151: 3895-3909 [Abstract] [Full Text]  
  • Bongiorni, C., Ishikawa, S., Stephenson, S., Ogasawara, N., Perego, M. (2005). Synergistic Regulation of Competence Development in Bacillus subtilis by Two Rap-Phr Systems. J. Bacteriol. 187: 4353-4361 [Abstract] [Full Text]  
  • Wu, X., Liu, D., Lee, M. H., Golden, J. W. (2004). patS Minigenes Inhibit Heterocyst Development of Anabaena sp. Strain PCC 7120. J. Bacteriol. 186: 6422-6429 [Abstract] [Full Text]  
  • Charbonnel, P., Lamarque, M., Piard, J.-C., Gilbert, C., Juillard, V., Atlan, D. (2003). Diversity of Oligopeptide Transport Specificity in Lactococcus lactis Species. A TOOL TO UNRAVEL THE ROLE OF OppA IN UPTAKE SPECIFICITY. J. Biol. Chem. 278: 14832-14840 [Abstract] [Full Text]  
  • Molle, V., Nakaura, Y., Shivers, R. P., Yamaguchi, H., Losick, R., Fujita, Y., Sonenshein, A. L. (2003). Additional Targets of the Bacillus subtilis Global Regulator CodY Identified by Chromatin Immunoprecipitation and Genome-Wide Transcript Analysis. J. Bacteriol. 185: 1911-1922 [Abstract] [Full Text]  
  • Hamoen, L. W., Venema, G., Kuipers, O. P. (2003). Controlling competence in Bacillus subtilis: shared use of regulators. Microbiology 149: 9-17 [Abstract] [Full Text]  
  • Koetje, E. J., Hajdo-Milasinovic, A., Kiewiet, R., Bron, S., Tjalsma, H. (2003). A plasmid-borne Rap-Phr system of Bacillus subtilis can mediate cell-density controlled production of extracellular proteases. Microbiology 149: 19-28 [Abstract] [Full Text]  
  • Britton, R. A., Eichenberger, P., Gonzalez-Pastor, J. E., Fawcett, P., Monson, R., Losick, R., Grossman, A. D. (2002). Genome-Wide Analysis of the Stationary-Phase Sigma Factor (Sigma-H) Regulon of Bacillus subtilis. J. Bacteriol. 184: 4881-4890 [Abstract] [Full Text]  
  • Schneider, K. B., Palmer, T. M., Grossman, A. D. (2002). Characterization of comQ and comX, Two Genes Required for Production of ComX Pheromone in Bacillus subtilis. J. Bacteriol. 184: 410-419 [Abstract] [Full Text]  
  • Jarmer, H., Larsen, T. S., Krogh, A., Saxild, H. H., Brunak, S., Knudsen, S. (2001). Sigma A recognition sites in the Bacillus subtilis genome. Microbiology 147: 2417-2424 [Abstract] [Full Text]  
  • McQuade, R. S., Comella, N., Grossman, A. D. (2001). Control of a Family of Phosphatase Regulatory Genes (phr) by the Alternate Sigma Factor Sigma-H of Bacillus subtilis. J. Bacteriol. 183: 4905-4909 [Abstract] [Full Text]  
  • Ratnayake-Lecamwasam, M., Serror, P., Wong, K.-W., Sonenshein, A. L. (2001). Bacillus subtilis CodY represses early-stationary-phase genes by sensing GTP levels. Genes Dev. 15: 1093-1103 [Abstract] [Full Text]  
  • Cvitkovitch, D.G. (2001). Genetic Competence and Transformation in Oral Streptococci. CROBM 12: 217-243 [Abstract] [Full Text]  
  • Mirel, D. B., Estacio, W. F., Mathieu, M., Olmsted, E., Ramirez, J., Márquez-Magaña, L. M. (2000). Environmental Regulation of Bacillus subtilis sigma D-Dependent Gene Expression. J. Bacteriol. 182: 3055-3062 [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»