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 O'Toole, G. A.
Right arrow Articles by Kolter, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by O'Toole, G. A.
Right arrow Articles by Kolter, R.

 Previous Article  |  Next Article 

Journal of Bacteriology, January 2000, p. 425-431, Vol. 182, No. 2
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

The Global Carbon Metabolism Regulator Crc Is a Component of a Signal Transduction Pathway Required for Biofilm Development by Pseudomonas aeruginosa

George A. O'Toole,1,2,* Karine A. Gibbs,2 Paul W. Hager,3 Paul V. Phibbs Jr.,3 and Roberto Kolter2

Department of Microbiology, Dartmouth Medical School, Hanover, New Hampshire 037551; Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 021152; and Department of Microbiology and Immunology, East Carolina University, Greenville, North Carolina 278583

Received 26 April 1999/Accepted 14 October 1999

The transition from a planktonic (free-swimming) existence to growth attached to a surface in a biofilm occurs in response to environmental factors, including the availability of nutrients. We show that the catabolite repression control (Crc) protein, which plays a role in the regulation of carbon metabolism, is necessary for biofilm formation in Pseudomonas aeruginosa. Using phase-contrast microscopy, we found that a crc mutant only makes a dispersed monolayer of cells on a plastic surface but does not develop the dense monolayer punctuated by microcolonies typical of the wild-type strain. This is a phenotype identical to that observed in mutants defective in type IV pilus biogenesis. Consistent with this observation, crc mutants are defective in type IV pilus-mediated twitching motility. We show that this defect in type IV pilus function is due (at least in part) to a decrease in pilA (pilin) transcription. We propose that nutritional cues are integrated by Crc as part of a signal transduction pathway that regulates biofilm development.

* Corresponding author. Mailing address: Department of Microbiology, Dartmouth Medical School, Rm. 202, Vail Bldg., Hanover, NH 03755. Phone: (603) 650-1248. Fax: (603) 650-1318. E-mail: George.O'Toole{at}Dartmouth.edu.

Journal of Bacteriology, January 2000, p. 425-431, Vol. 182, No. 2
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • 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]  
  • Zimmermann, T., Sorg, T., Siehler, S. Y., Gerischer, U. (2009). Role of Acinetobacter baylyi Crc in Catabolite Repression of Enzymes for Aromatic Compound Catabolism. J. Bacteriol. 191: 2834-2842 [Abstract] [Full Text]  
  • Tomaras, A. P., Flagler, M. J., Dorsey, C. W., Gaddy, J. A., Actis, L. A. (2008). Characterization of a two-component regulatory system from Acinetobacter baumannii that controls biofilm formation and cellular morphology. Microbiology 154: 3398-3409 [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]  
  • Moreau-Marquis, S., Bomberger, J. M., Anderson, G. G., Swiatecka-Urban, A., Ye, S., O'Toole, G. A., Stanton, B. A. (2008). The {Delta}F508-CFTR mutation results in increased biofilm formation by Pseudomonas aeruginosa by increasing iron availability. Am. J. Physiol. Lung Cell. Mol. Physiol. 295: L25-L37 [Abstract] [Full Text]  
  • Kalivoda, E. J., Stella, N. A., O'Dee, D. M., Nau, G. J., Shanks, R. M. Q. (2008). The Cyclic AMP-Dependent Catabolite Repression System of Serratia marcescens Mediates Biofilm Formation through Regulation of Type 1 Fimbriae. Appl. Environ. Microbiol. 74: 3461-3470 [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]  
  • Kuchma, S. L., Brothers, K. M., Merritt, J. H., Liberati, N. T., Ausubel, F. M., O'Toole, G. A. (2007). BifA, a Cyclic-Di-GMP Phosphodiesterase, Inversely Regulates Biofilm Formation and Swarming Motility by Pseudomonas aeruginosa PA14. J. Bacteriol. 189: 8165-8178 [Abstract] [Full Text]  
  • Morici, L. A., Carterson, A. J., Wagner, V. E., Frisk, A., Schurr, J. R., zu Bentrup, K. H., Hassett, D. J., Iglewski, B. H., Sauer, K., Schurr, M. J. (2007). Pseudomonas aeruginosa AlgR Represses the Rhl Quorum-Sensing System in a Biofilm-Specific Manner. J. Bacteriol. 189: 7752-7764 [Abstract] [Full Text]  
  • Wu, H., Zeng, M., Fives-Taylor, P. (2007). The Glycan Moieties and the N-Terminal Polypeptide Backbone of a Fimbria-Associated Adhesin, Fap1, Play Distinct Roles in the Biofilm Development of Streptococcus parasanguinis. Infect. Immun. 75: 2181-2188 [Abstract] [Full Text]  
  • Reeser, R. J., Medler, R. T., Billington, S. J., Jost, B. H., Joens, L. A. (2007). Characterization of Campylobacter jejuni Biofilms under Defined Growth Conditions. Appl. Environ. Microbiol. 73: 1908-1913 [Abstract] [Full Text]  
  • Davey, M. E., Duncan, M. J. (2006). Enhanced Biofilm Formation and Loss of Capsule Synthesis: Deletion of a Putative Glycosyltransferase in Porphyromonas gingivalis.. J. Bacteriol. 188: 5510-5523 [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]  
  • Lembke, C., Podbielski, A., Hidalgo-Grass, C., Jonas, L., Hanski, E., Kreikemeyer, B. (2006). Characterization of Biofilm Formation by Clinically Relevant Serotypes of Group A Streptococci. Appl. Environ. Microbiol. 72: 2864-2875 [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]  
  • Wu, M., Guina, T., Brittnacher, M., Nguyen, H., Eng, J., Miller, S. I. (2005). The Pseudomonas aeruginosa Proteome during Anaerobic Growth. J. Bacteriol. 187: 8185-8190 [Abstract] [Full Text]  
  • Silo-Suh, L., Suh, S.-J., Phibbs, P. V., Ohman, D. E. (2005). Adaptations of Pseudomonas aeruginosa to the Cystic Fibrosis Lung Environment Can Include Deregulation of zwf, Encoding Glucose-6-Phosphate Dehydrogenase. J. Bacteriol. 187: 7561-7568 [Abstract] [Full Text]  
  • Caiazza, N. C., Shanks, R. M. Q., O'Toole, G. A. (2005). Rhamnolipids Modulate Swarming Motility Patterns of Pseudomonas aeruginosa. J. Bacteriol. 187: 7351-7361 [Abstract] [Full Text]  
  • Banin, E., Vasil, M. L., Greenberg, E. P. (2005). From The Cover: Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA 102: 11076-11081 [Abstract] [Full Text]  
  • Parvatiyar, K., Alsabbagh, E. M., Ochsner, U. A., Stegemeyer, M. A., Smulian, A. G., Hwang, S. H., Jackson, C. R., McDermott, T. R., Hassett, D. J. (2005). Global Analysis of Cellular Factors and Responses Involved in Pseudomonas aeruginosa Resistance to Arsenite. J. Bacteriol. 187: 4853-4864 [Abstract] [Full Text]  
  • Ruiz-Manzano, A., Yuste, L., Rojo, F. (2005). Levels and Activity of the Pseudomonas putida Global Regulatory Protein Crc Vary According to Growth Conditions. J. Bacteriol. 187: 3678-3686 [Abstract] [Full Text]  
  • Kuchma, S. L., Connolly, J. P., O'Toole, G. A. (2005). A Three-Component Regulatory System Regulates Biofilm Maturation and Type III Secretion in Pseudomonas aeruginosa. J. Bacteriol. 187: 1441-1454 [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]  
  • Silby, M. W., Levy, S. B. (2004). Use of In Vivo Expression Technology To Identify Genes Important in Growth and Survival of Pseudomonas fluorescens Pf0-1 in Soil: Discovery of Expressed Sequences with Novel Genetic Organization. J. Bacteriol. 186: 7411-7419 [Abstract] [Full Text]  
  • Caiazza, N. C., O'Toole, G. A. (2004). SadB Is Required for the Transition from Reversible to Irreversible Attachment during Biofilm Formation by Pseudomonas aeruginosa PA14. J. Bacteriol. 186: 4476-4485 [Abstract] [Full Text]  
  • Morales, G., Linares, J. F., Beloso, A., Albar, J. P., Martinez, J. L., Rojo, F. (2004). The Pseudomonas putida Crc Global Regulator Controls the Expression of Genes from Several Chromosomal Catabolic Pathways for Aromatic Compounds. J. Bacteriol. 186: 1337-1344 [Abstract] [Full Text]  
  • Huang, B., Whitchurch, C. B., Mattick, J. S. (2003). FimX, a Multidomain Protein Connecting Environmental Signals to Twitching Motility in Pseudomonas aeruginosa. J. Bacteriol. 185: 7068-7076 [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]  
  • Carter, G., Wu, M., Drummond, D. C., Bermudez, L. E. (2003). Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol 52: 747-752 [Abstract] [Full Text]  
  • Beenken, K. E., Blevins, J. S., Smeltzer, M. S. (2003). Mutation of sarA in Staphylococcus aureus Limits Biofilm Formation. Infect. Immun. 71: 4206-4211 [Abstract] [Full Text]  
  • Finelli, A., Gallant, C. V., Jarvi, K., Burrows, L. L. (2003). Use of In-Biofilm Expression Technology To Identify Genes Involved in Pseudomonas aeruginosa Biofilm Development. J. Bacteriol. 185: 2700-2710 [Abstract] [Full Text]  
  • Loo, C. Y., Mitrakul, K., Voss, I. B., Hughes, C. V., Ganeshkumar, N. (2003). Involvement of the adc Operon and Manganese Homeostasis in Streptococcus gordonii Biofilm Formation. J. Bacteriol. 185: 2887-2900 [Abstract] [Full Text]  
  • Stewart, P. S. (2003). Diffusion in Biofilms. J. Bacteriol. 185: 1485-1491 [Full Text]  
  • Davey, M. E., Caiazza, N. C., O'Toole, G. A. (2003). Rhamnolipid Surfactant Production Affects Biofilm Architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185: 1027-1036 [Abstract] [Full Text]  
  • Yoshida, A., Kuramitsu, H. K. (2002). Multiple Streptococcus mutans Genes Are Involved in Biofilm Formation. Appl. Environ. Microbiol. 68: 6283-6291 [Abstract] [Full Text]  
  • Dinamarca, M. A., Ruiz-Manzano, A., Rojo, F. (2002). Inactivation of Cytochrome o Ubiquinol Oxidase Relieves Catabolic Repression of the Pseudomonas putida GPo1 Alkane Degradation Pathway. J. Bacteriol. 184: 3785-3793 [Abstract] [Full Text]  
  • Jackson, D. W., Simecka, J. W., Romeo, T. (2002). Catabolite Repression of Escherichia coli Biofilm Formation. J. Bacteriol. 184: 3406-3410 [Abstract] [Full Text]  
  • Wen, Z. T., Burne, R. A. (2002). Functional Genomics Approach to Identifying Genes Required for Biofilm Development by Streptococcus mutans. Appl. Environ. Microbiol. 68: 1196-1203 [Abstract] [Full Text]  
  • Sauer, K., Camper, A. K., Ehrlich, G. D., Costerton, J. W., Davies, D. G. (2002). Pseudomonas aeruginosa Displays Multiple Phenotypes during Development as a Biofilm. J. Bacteriol. 184: 1140-1154 [Abstract] [Full Text]  
  • Jackson, D. W., Suzuki, K., Oakford, L., Simecka, J. W., Hart, M. E., Romeo, T. (2002). Biofilm Formation and Dispersal under the Influence of the Global Regulator CsrA of Escherichia coli. J. Bacteriol. 184: 290-301 [Abstract] [Full Text]  
  • Sauer, K., Camper, A. K. (2001). Characterization of Phenotypic Changes in Pseudomonas putida in Response to Surface-Associated Growth. J. Bacteriol. 183: 6579-6589 [Abstract] [Full Text]  
  • Yuste, L., Rojo, F. (2001). Role of the crc Gene in Catabolic Repression of the Pseudomonas putida GPo1 Alkane Degradation Pathway. J. Bacteriol. 183: 6197-6206 [Abstract] [Full Text]  
  • Vallet, I., Olson, J. W., Lory, S., Lazdunski, A., Filloux, A. (2001). The chaperone/usher pathways of Pseudomonas aeruginosa: Identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 10.1073/pnas.111551898v1 [Abstract] [Full Text]  
  • De Kievit, T. R., Gillis, R., Marx, S., Brown, C., Iglewski, B. H. (2001). Quorum-Sensing Genes in Pseudomonas aeruginosa Biofilms: Their Role and Expression Patterns. Appl. Environ. Microbiol. 67: 1865-1873 [Abstract] [Full Text]  
  • Froeliger, E. H., Fives-Taylor, P. (2001). Streptococcus parasanguis Fimbria-Associated Adhesin Fap1 Is Required for Biofilm Formation. Infect. Immun. 69: 2512-2519 [Abstract] [Full Text]  
  • Davey, M. E., O'toole, G. A. (2000). Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol. Mol. Biol. Rev. 64: 847-867 [Abstract] [Full Text]  
  • Köhler, T., Curty, L. K., Barja, F., van Delden, C., Pechère, J.-C. (2000). Swarming of Pseudomonas aeruginosa Is Dependent on Cell-to-Cell Signaling and Requires Flagella and Pili. J. Bacteriol. 182: 5990-5996 [Abstract] [Full Text]  
  • Heydorn, A., Nielsen, A. T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B. K., Molin, S. (2000). Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407 [Abstract] [Full Text]  
  • Otto, K., Silhavy, T. J. (2002). Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99: 2287-2292 [Abstract] [Full Text]  
  • Vallet, I., Olson, J. W., Lory, S., Lazdunski, A., Filloux, A. (2001). The chaperone/usher pathways of Pseudomonas aeruginosa: Identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. USA 98: 6911-6916 [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»