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 Stanley, N. R.
Right arrow Articles by Lazazzera, B. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Stanley, N. R.
Right arrow Articles by Lazazzera, B. A.

 Previous Article  |  Next Article 

Journal of Bacteriology, March 2003, p. 1951-1957, Vol. 185, No. 6
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.6.1951-1957.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Identification of Catabolite Repression as a Physiological Regulator of Biofilm Formation by Bacillus subtilis by Use of DNA Microarrays

Nicola R. Stanley,1 Robert A. Britton,2,{dagger} Alan D. Grossman,2 and Beth A. Lazazzera1*

Department of Microbiology, Immunology and Molecular Genetics, University of California—Los Angeles, Los Angeles, California 90095,1 Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts 021392

Received 17 October 2002/ Accepted 20 December 2002

Biofilms are structured communities of cells that are encased in a self-produced polymeric matrix and are adherent to a surface. Many biofilms have a significant impact in medical and industrial settings. The model gram-positive bacterium Bacillus subtilis has recently been shown to form biofilms. To gain insight into the genes involved in biofilm formation by this bacterium, we used DNA microarrays representing >99% of the annotated B. subtilis open reading frames to follow the temporal changes in gene expression that occurred as cells transitioned from a planktonic to a biofilm state. We identified 519 genes that were differentially expressed at one or more time points as cells transitioned to a biofilm. Approximately 6% of the genes of B. subtilis were differentially expressed at a time when 98% of the cells in the population were in a biofilm. These genes were involved in motility, phage-related functions, and metabolism. By comparing the genes differentially expressed during biofilm formation with those identified in other genomewide transcriptional-profiling studies, we were able to identify several transcription factors whose activities appeared to be altered during the transition from a planktonic state to a biofilm. Two of these transcription factors were Spo0A and sigma-H, which had previously been shown to affect biofilm formation by B. subtilis. A third signal that appeared to be affecting gene expression during biofilm formation was glucose depletion. Through quantitative biofilm assays and confocal scanning laser microscopy, we observed that glucose inhibited biofilm formation through the catabolite control protein CcpA.

* Corresponding author. Mailing address: Department of Microbiology, Immunology and Molecular Genetics, University of California—Los Angeles, 1602 Molecular Sciences Building, 405 Hilgard Ave., Los Angeles, CA 90095. Phone: (310) 794-4804. Fax: (310) 206-5231. E-mail: bethl{at}microbio.ucla.edu.

{dagger} Present address: Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48823.

Journal of Bacteriology, March 2003, p. 1951-1957, Vol. 185, No. 6
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.6.1951-1957.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Murray, E. J., Strauch, M. A., Stanley-Wall, N. R. (2009). {sigma}X Is Involved in Controlling Bacillus subtilis Biofilm Architecture through the AbrB Homologue Abh. J. Bacteriol. 191: 6822-6832 [Abstract] [Full Text]  
  • Karatan, E., Watnick, P. (2009). Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms. Microbiol. Mol. Biol. Rev. 73: 310-347 [Abstract] [Full Text]  
  • Varga, J. J., Therit, B., Melville, S. B. (2008). Type IV Pili and the CcpA Protein Are Needed for Maximal Biofilm Formation by the Gram-Positive Anaerobic Pathogen Clostridium perfringens. Infect. Immun. 76: 4944-4951 [Abstract] [Full Text]  
  • Fong, J. C. N., Yildiz, F. H. (2008). Interplay between Cyclic AMP-Cyclic AMP Receptor Protein and Cyclic di-GMP Signaling in Vibrio cholerae Biofilm Formation. J. Bacteriol. 190: 6646-6659 [Abstract] [Full Text]  
  • Nagorska, K., Hinc, K., Strauch, M. A., Obuchowski, M. (2008). Influence of the {sigma}B Stress Factor and yxaB, the Gene for a Putative Exopolysaccharide Synthase under {sigma}B Control, on Biofilm Formation. J. Bacteriol. 190: 3546-3556 [Abstract] [Full Text]  
  • Seidl, K., Goerke, C., Wolz, C., Mack, D., Berger-Bachi, B., Bischoff, M. (2008). Staphylococcus aureus CcpA Affects Biofilm Formation. Infect. Immun. 76: 2044-2050 [Abstract] [Full Text]  
  • Mendez, M., Huang, I-H., Ohtani, K., Grau, R., Shimizu, T., Sarker, M. R. (2008). Carbon Catabolite Repression of Type IV Pilus-Dependent Gliding Motility in the Anaerobic Pathogen Clostridium perfringens. J. Bacteriol. 190: 48-60 [Abstract] [Full Text]  
  • Houot, L., Watnick, P. I. (2008). A Novel Role for Enzyme I of the Vibrio cholerae Phosphoenolpyruvate Phosphotransferase System in Regulation of Growth in a Biofilm. J. Bacteriol. 190: 311-320 [Abstract] [Full Text]  
  • Auvray, F., Chassaing, D., Duprat, C., Carpentier, B. (2007). The Listeria monocytogenes Homolog of the Escherichia coli era Gene Is Involved in Adhesion to Inert Surfaces. Appl. Environ. Microbiol. 73: 7789-7792 [Abstract] [Full Text]  
  • Curtis, P. D., Atwood, J. III, Orlando, R., Shimkets, L. J. (2007). Proteins Associated with the Myxococcus xanthus Extracellular Matrix. J. Bacteriol. 189: 7634-7642 [Abstract] [Full Text]  
  • Jordan, S., Rietkotter, E., Strauch, M. A., Kalamorz, F., Butcher, B. G., Helmann, J. D., Mascher, T. (2007). LiaRS-dependent gene expression is embedded in transition state regulation in Bacillus subtilis. Microbiology 153: 2530-2540 [Abstract] [Full Text]  
  • Kobayashi, K. (2007). Bacillus subtilis Pellicle Formation Proceeds through Genetically Defined Morphological Changes. J. Bacteriol. 189: 4920-4931 [Abstract] [Full Text]  
  • Lee, K., Costerton, J. W., Ravel, J., Auerbach, R. K., Wagner, D. M., Keim, P., Leid, J. G. (2007). Phenotypic and functional characterization of Bacillus anthracis biofilms. Microbiology 153: 1693-1701 [Abstract] [Full Text]  
  • Rice, K. C., Mann, E. E., Endres, J. L., Weiss, E. C., Cassat, J. E., Smeltzer, M. S., Bayles, K. W. (2007). The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104: 8113-8118 [Abstract] [Full Text]  
  • Motegi, M., Takagi, Y., Yonezawa, H., Hanada, N., Terajima, J., Watanabe, H., Senpuku, H. (2006). Assessment of Genes Associated with Streptococcus mutans Biofilm Morphology. Appl. Environ. Microbiol. 72: 6277-6287 [Abstract] [Full Text]  
  • Morikawa, M., Kagihiro, S., Haruki, M., Takano, K., Branda, S., Kolter, R., Kanaya, S. (2006). Biofilm formation by a Bacillus subtilis strain that produces {gamma}-polyglutamate.. Microbiology 152: 2801-2807 [Abstract] [Full Text]  
  • Viswanathan, P., Singer, M., Kroos, L. (2006). Role of {sigma}D in Regulating Genes and Signals during Myxococcus xanthus Development. J. Bacteriol. 188: 3246-3256 [Abstract] [Full Text]  
  • Domka, J., Lee, J., Wood, T. K. (2006). YliH (BssR) and YceP (BssS) Regulate Escherichia coli K-12 Biofilm Formation by Influencing Cell Signaling. Appl. Environ. Microbiol. 72: 2449-2459 [Abstract] [Full Text]  
  • Veening, J.-W., Kuipers, O. P., Brul, S., Hellingwerf, K. J., Kort, R. (2006). Effects of Phosphorelay Perturbations on Architecture, Sporulation, and Spore Resistance in Biofilms of Bacillus subtilis.. J. Bacteriol. 188: 3099-3109 [Abstract] [Full Text]  
  • Sampathkumar, B., Napper, S., Carrillo, C. D., Willson, P., Taboada, E., Nash, J. H. E., Potter, A. A., Babiuk, L. A., Allan, B. J. (2006). Transcriptional and translational expression patterns associated with immobilized growth of Campylobacter jejuni. Microbiology 152: 567-577 [Abstract] [Full Text]  
  • Southey-Pillig, C. J., Davies, D. G., Sauer, K. (2005). Characterization of Temporal Protein Production in Pseudomonas aeruginosa Biofilms. J. Bacteriol. 187: 8114-8126 [Abstract] [Full Text]  
  • Hunter, R. C., Beveridge, T. J. (2005). High-Resolution Visualization of Pseudomonas aeruginosa PAO1 Biofilms by Freeze-Substitution Transmission Electron Microscopy. J. Bacteriol. 187: 7619-7630 [Abstract] [Full Text]  
  • Ren, D., Zuo, R., Gonzalez Barrios, A. F., Bedzyk, L. A., Eldridge, G. R., Pasmore, M. E., Wood, T. K. (2005). Differential Gene Expression for Investigation of Escherichia coli Biofilm Inhibition by Plant Extract Ursolic Acid. Appl. Environ. Microbiol. 71: 4022-4034 [Abstract] [Full Text]  
  • Rathsam, C., Eaton, R. E., Simpson, C. L., Browne, G. V., Berg, T., Harty, D. W. S., Jacques, N. A. (2005). Up-regulation of competence- but not stress-responsive proteins accompanies an altered metabolic phenotype in Streptococcus mutans biofilms. Microbiology 151: 1823-1837 [Abstract] [Full Text]  
  • Lazarevic, V., Soldo, B., Medico, N., Pooley, H., Bron, S., Karamata, D. (2005). Bacillus subtilis {alpha}-Phosphoglucomutase Is Required for Normal Cell Morphology and Biofilm Formation. Appl. Environ. Microbiol. 71: 39-45 [Abstract] [Full Text]  
  • Webb, J. S., Lau, M., Kjelleberg, S. (2004). Bacteriophage and Phenotypic Variation in Pseudomonas aeruginosa Biofilm Development. J. Bacteriol. 186: 8066-8073 [Abstract] [Full Text]  
  • Sauer, K., Cullen, M. C., Rickard, A. H., Zeef, L. A. H., Davies, D. G., Gilbert, P. (2004). Characterization of Nutrient-Induced Dispersion in Pseudomonas aeruginosa PAO1 Biofilm. J. Bacteriol. 186: 7312-7326 [Abstract] [Full Text]  
  • Ren, D., Bedzyk, L. A., Setlow, P., England, D. F., Kjelleberg, S., Thomas, S. M., Ye, R. W., Wood, T. K. (2004). Differential Gene Expression To Investigate the Effect of (5Z)-4-Bromo- 5-(Bromomethylene)-3-Butyl-2(5H)-Furanone on Bacillus subtilis. Appl. Environ. Microbiol. 70: 4941-4949 [Abstract] [Full Text]  
  • Parsek, M. R., Fuqua, C. (2004). Biofilms 2003: Emerging Themes and Challenges in Studies of Surface-Associated Microbial Life. J. Bacteriol. 186: 4427-4440 [Full Text]  
  • Beenken, K. E., Dunman, P. M., McAleese, F., Macapagal, D., Murphy, E., Projan, S. J., Blevins, J. S., Smeltzer, M. S. (2004). Global Gene Expression in Staphylococcus aureus Biofilms. J. Bacteriol. 186: 4665-4684 [Abstract] [Full Text]  
  • Nicholson, T. L., Chiu, K., Stephens, R. S. (2004). Chlamydia trachomatis Lacks an Adaptive Response to Changes in Carbon Source Availability. Infect. Immun. 72: 4286-4289 [Abstract] [Full Text]  
  • Branda, S. S., Gonzalez-Pastor, J. E., Dervyn, E., Ehrlich, S. D., Losick, R., Kolter, R. (2004). Genes Involved in Formation of Structured Multicellular Communities by Bacillus subtilis. J. Bacteriol. 186: 3970-3979 [Abstract] [Full Text]  
  • Zhang, Y., Lei, Y., Khammanivong, A., Herzberg, M. C. (2004). Identification of a Novel Two-Component System in Streptococcus gordonii V288 Involved in Biofilm Formation. Infect. Immun. 72: 3489-3494 [Abstract] [Full Text]  
  • Ren, D., Bedzyk, L. A., Ye, R. W., Thomas, S. M., Wood, T. K. (2004). Stationary-Phase Quorum-Sensing Signals Affect Autoinducer-2 and Gene Expression in Escherichia coli. Appl. Environ. Microbiol. 70: 2038-2043 [Abstract] [Full Text]  
  • Lemos, J. A. C., Brown, T. A. Jr., Burne, R. A. (2004). Effects of RelA on Key Virulence Properties of Planktonic and Biofilm Populations of Streptococcus mutans. Infect. Immun. 72: 1431-1440 [Abstract] [Full Text]  
  • Esteban, C. D., Mahr, K., Monedero, V., Hillen, W., Perez-Martinez, G., Titgemeyer, F. (2004). Complementation of a {Delta}ccpA mutant of Lactobacillus casei with CcpA mutants affected in the DNA- and cofactor-binding domains. Microbiology 150: 613-620 [Abstract] [Full Text]  
  • Bais, H. P., Fall, R., Vivanco, J. M. (2004). Biocontrol of Bacillus subtilis against Infection of Arabidopsis Roots by Pseudomonas syringae Is Facilitated by Biofilm Formation and Surfactin Production. Plant Physiol. 134: 307-319 [Abstract] [Full Text]  
  • Loo, C. Y., Mitrakul, K., Voss, I. B., Hughes, C. V., Ganeshkumar, N. (2003). Involvement of an Inducible Fructose Phosphotransferase Operon in Streptococcus gordonii Biofilm Formation. J. Bacteriol. 185: 6241-6254 [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»