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2 - Quorum Sensing and Microbial Biofilms

Published online by Cambridge University Press:  23 November 2009

Teresa R. de Kievit
Affiliation:
Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada
Barbara H. Iglewski
Affiliation:
Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York, USA
Michael Wilson
Affiliation:
University College London
Deirdre Devine
Affiliation:
Leeds Dental Institute, University of Leeds
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Summary

INTRODUCTION

For a long time bacteria were believed to exist as unicellular organisms; however, it is now realized that in nature bacteria are more often found clustered in communities. Within these communities, bacteria are capable of coordinated activity through the use of a sophisticated intercellular communication mechanism called quorum sensing (QS). The capacity to behave collectively as a group has obvious advantages, for example, migration to a more suitable environment/better nutrient supply or adopting a more favourable mode of growth such as sporulation. Recently, QS was discovered to play a role in the formation of biofilms. This latter phenomenon will be the focus of this chapter as we review our current understanding of how QS affects the complex processes of biofilm development. With respect to intercellular communication and biofilms, Pseudomonas aeruginosa is one of the most intensely studied organisms, and therefore, much of this chapter will concentrate on this bacterium.

QUORUM SENSING

QS exists in both Gram-positive and Gram-negative bacteria with obvious differences between the two systems (for reviews, see Dunny and Leonard, 1997; Fuqua, Winans, and Greenberg, 1996). Here, we will focus on Gram-negative bacteria, where the two primary components of QS systems are the autoinducer (AI) signal molecule and the transcriptional activator, or R-protein. In general, the ‘language’ used for intercellular communication is based on small, diffusible, self-generated signal molecules called AIs.

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Publisher: Cambridge University Press
Print publication year: 2003

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References

Albus, A. M., Pesci, E. C., Runyen-Janecky, L. J., West, S. E. and Iglewski, B. H. (1997). Vfr controls quorum sensing in Pseudomonas aeruginosa. Journal of Bacteriology, 179, 3928–3935CrossRefGoogle ScholarPubMed
Anderson, J. B., Heydorn, A., Hentzer, M., Eberl, L., Geisenberger, O., Christensen, B. B., Molin, S. and Givskov, M. (2001). gfp-Based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Applied and Environmental Microbiology, 67, 575–585CrossRefGoogle Scholar
Andersen, J. B., Sternberg, C., Poulsen, L. K., Bjorn, S. P., Givskov, M. and Molin, S. (1998). New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Applied and Environmental Microbiology, 64, 2240–2246Google ScholarPubMed
Brint, J. M. and Ohman, D. E. (1995). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. Journal of Bacteriology, 177, 7155–7163CrossRefGoogle ScholarPubMed
Chapon-Herve, V., Akrim, M., Latifi, A., Williams, P., Lazdunski, A. and Bally, M. (1997). Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Molecular Microbiology, 24, 1169–1178CrossRefGoogle ScholarPubMed
Charlton, T. S., Nys, R., Netting, A., Kumar, N., Hentzer, M., Givskov, M. and Kjelleberg, S. (2000). A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatograph-mass spectrometry: application to a model bacterial biofilm. Environmental Microbiology, 2, 530–541CrossRefGoogle Scholar
Costerton, J. W., Stewart, P. S. and Greenberg, E. P. (1999). Bacterial biofilms: a common cause of persistant infections. Science, 284, 1318–1322CrossRefGoogle Scholar
Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W. and Greenberg, E. P. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 280, 295–298CrossRefGoogle ScholarPubMed
Kievit, T. R., Gillis, R., Marx, S., Brown, C. and Iglewski, B. H. (2001). Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Applied and Environmental Microbiology, 67, 1865–1873CrossRefGoogle ScholarPubMed
Kievit, T. R. and Iglewski, B. H. (2000). Bacterial quorum sensing in pathogenic relationships. Infection and Immunity, 68, 4839–4849CrossRefGoogle ScholarPubMed
Kievit, T., Seed, P. C., Nezezon, J., Passador, L. and Iglewski, B. H. (1999). RsaL, a novel repressor of virulence gene expression in Pseudomonas aeruginosa. Journal of Bacteriology, 181, 2175–84Google ScholarPubMed
Nys, R., Steinberg, P. D., Willemsen, P., Dworjanyn, S. A., Gabelish, C. L. and King, R. J. (1995). Broad spectrum effects of secondary metabolites from the red alga Delisea pulchra in antifouling assays. Biofouling, 8, 259–271CrossRefGoogle Scholar
DiMango, E., Zar, H. J., Bryan, R. and Prince, A. (1995). Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. Journal of Clinical Investigation, 96, 2204–2210CrossRefGoogle ScholarPubMed
Dunny, G. M. and Leonard, B. A. B. (1997). Cell–cell communication in Gram-positive bacteria. Annual Review of Microbiology, 51, 527–564CrossRefGoogle ScholarPubMed
Flemming, C. A., Palmer, R. J. Jr., Arrage, A. A., Mei, H. C. and White, D. C. (1998). Cell surface physiochemistry alters biofilm development of Pseudomonas aeruginosa lipopolysaccharide mutants. Biofouling, 13, 213–231CrossRefGoogle Scholar
Fuqua, W. C., Winans, S. C. and Greenberg, E. P. (1996). Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annual Review of Microbiology, 50, 727–751CrossRefGoogle ScholarPubMed
Gambello, M. J., Kaye, S. and Iglewski, B. H. (1993). LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infection and Immunity, 61, 1180–1184Google ScholarPubMed
Geisenberger, O., Givskov, M., Riedel, K., H⊘iby, N., Tümmler, B. and Eberl, L. (2000). Production of N-acyl-L-homoserine lactones by P. aeruginosa isolates from chronic lung infections associated with cystic fibrosis. FEMS Microbiology Letters, 184, 273–278Google ScholarPubMed
Givskov, M., Nys, R., Manefield, M., Gram, L., Maximilien, R., Eberl, L., Molin, S., Steinberg, P. D. and Kjelleberg, S. (1996). Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. Journal of Bacteriology, 178, 6618–6622CrossRefGoogle ScholarPubMed
Hancock, R. W., Mutharia, L. M., Chan, M., Darveau, R. P., Speert, D. P. and Pier, G. B. (1983). Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains. Infection and Immunity, 42, 170–177Google ScholarPubMed
Huber, B., Riedel, K., Hentzer, M., Heydorn, A., Gotschlich, A., Givskov, M., Molin, S. and Eberl, L. (2001). The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology, 147, 2517–2528CrossRefGoogle ScholarPubMed
Kolter, R. and Losick, R. (1998). One for all and all for one. Science, 280, 226–227CrossRefGoogle ScholarPubMed
Lam, M. Y. C., McGroarty, E. J., Kropinski, A. M., MacDonald, L. A., Peterson, S. S., H⊘iby, N. and Lam, J. S. (1989). Occurrence of a common lipopolysaccharide antigen in standard and clinical strains of Pseudomonas aeruginosa. Journal of Clinical Microbiology, 27, 962–967Google ScholarPubMed
Latifi, A., Foglino, M., Tanaka, K., Williams, P. and Lazdunski, A. (1996). A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR to expression of the stationary-phase sigma factor RpoS. Molecular Microbiology, 21, 1137–1146CrossRefGoogle ScholarPubMed
Latifi, A., Winson, M. K., Foglino, M., Bycroft, B. W., Stewart, G. S. A. B., Lazdunski, L. and Williams, P. (1995). Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Molecular Microbiology, 17, 333–343CrossRefGoogle ScholarPubMed
Lewenza, S., Conway, B., Greenberg, E. P. and Sokol, P. A. (1999). Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepRI. Journal of Bacteriology, 181, 748–756Google ScholarPubMed
McLean, R. J., Whiteley, M., Stickler, D. J. and Fuqua, W. C. (1997). Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiology Letters, 154, 259–263CrossRefGoogle ScholarPubMed
Ochsner, U. A., Koch, A. K., Fiechter, A. and Reiser, J. (1994). Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Journal of Bacteriology, 176, 2044–2054CrossRefGoogle ScholarPubMed
Ochsner, U. A. and Reiser, J. (1995). Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the USA, 92, 6424–6428CrossRefGoogle ScholarPubMed
O'Toole, G. A. and Kolter, R. (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbiology, 30, 295–304CrossRefGoogle ScholarPubMed
Passador, L., Cook, J. M., Gambello, M. J., Rust, L. and Iglewski, B. H. (1993). Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science, 260, 1127–1130CrossRefGoogle ScholarPubMed
Pearson, J. P., Feldman, M., Iglewski, B. H. and Prince, A. (2000). Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infection and Immunity, 68, 4331–4334CrossRefGoogle Scholar
Pearson, J. P., Gray, K. M., Passador, L., Tucker, K. D., Eberhard, A., Iglewski, B. H. and Greenberg, E. P. (1994). Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proceedings of the National Academy of Sciences of the USA, 91, 197–201CrossRefGoogle ScholarPubMed
Pearson, J. P., Passador, L., Iglewski, B. H. and Greenberg, E. P. (1995). A second N-acyl homoserine lactone signal produced by Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the USA, 92, 1490–1494CrossRefGoogle Scholar
Pearson, J. P., Pesci, E. C. and Iglewski, B. H. (1997). Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. Journal of Bacteriology, 179, 5756–5767CrossRefGoogle ScholarPubMed
Pesci, E. C., Milbank, J. B., Pearson, J. P., McKnight, S., Kende, A. S., Greenberg, E. P., and Iglewski, B. H. (1999). Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of the USA, 96, 11229–11234CrossRefGoogle ScholarPubMed
Pesci, E. C., Pearson, J. P., Seed, P. C. and Iglewski, B. H. (1997). Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. Journal of Bacteriology, 179, 3127–3132CrossRefGoogle ScholarPubMed
Rahme, L. G., Stevens, E. J., Wolfort, S. F., Shao, J., Tompkins, R. G. and Ausubel, F. M. (1995). Common virulence factors for bacterial pathogenicity in plants and animals. Science, 268, 1899–1902CrossRefGoogle ScholarPubMed
Rahme, L. G., Tan, M.-W., Le, L., Wong, S. M., Tompkins, R. G., Calderwood, S. B. and Ausubel, F. M. (1997). Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proceedings of the National Academy of Sciences of the USA, 94, 13245–13250CrossRefGoogle ScholarPubMed
Reichelt, J. L. and Borowitzka, M. A. (1984). Antimicrobial activity from marine algae: results of a large-scale screening programme. Hydrobiologia, 116/117, 158–168CrossRefGoogle Scholar
Reimmann, C., Beyeler, M., Latifi, A., Winteler, H., Foglino, M., Lazdunski, A. and Haas, D. (1997). The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Molecular Microbiology, 24, 309–319CrossRefGoogle Scholar
Rocchetta, H. L., Burrows, L. L. and Lam, J. S. (1999). Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiology and Molecular Biology Reviews, 63, 523–553Google ScholarPubMed
Rumbaugh, K. P., Griswold, J. A. and Hamood, A. N., (1999a). Contribution of the regulatory gene lasR to the pathogenesis of Pseudomonas aeruginosa infection of burned mice. Journal of Burn Care and Rehabilitation, 20, 42–49CrossRefGoogle Scholar
Rumbaugh, K. P.Griswold, J. A., Iglewski, B. H. and Hamood, A. N. (1999b). Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infection and Immunity, 67, 5854–5862Google Scholar
Seed, P. C., Passador, L. and Iglewski, B. H. (1995). Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. Journal of Bacteriology, 177, 654–659CrossRefGoogle Scholar
Shaw, P. D., Ping, G., Daly, S. L., Cha, C., Cronan, J. E. Jr., Renehart, K. L.., (1997). Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proceedings of the National Academy of Sciences of the USA, 94, 6036–6041CrossRefGoogle ScholarPubMed
Singh, P. K., Schaefer, A. L., Parsek, M. R., Moninger, T. O., Welsh, M. J. and Greenberg, E. P. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature, 407, 762–764CrossRefGoogle ScholarPubMed
Spoering, A. L. and Lewis, K. (2001). Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. Journal of Bacteriology, 183, 6746–6751CrossRefGoogle ScholarPubMed
Stickler, D. J., Morris, N. S., McLean, R. J. and Fuqua, C. (1998). Biofilms on indwelling urethral catheters produce quorum-sensing signal molecules in situ and in vitro. Applied and Environmental Microbiology, 64, 3486–3490Google ScholarPubMed
Storey, D. G., Ujack, E. E., Rabin, H. R. and Mitchell, I. (1998). Pseudomonas aeruginosa lasR transcription correlates with the transcription of lasA, lasB, and toxA in chronic lung infections associated with cystic fibrosis. Infection and Immunity, 66, 2521–2528Google ScholarPubMed
Tan, M.-W., Rahme, L. G., Sternberg, J. A., Tompkins, R. G. and Ausubel, F. M. (1999). Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proceedings of the National Academy of Sciences of the USA, 96, 2408–2413CrossRefGoogle ScholarPubMed
Tang, H. B., DiMango, E., Bryan, R., Gambello, M., Iglewski, B. H., Goldberg, J. B. and Prince, A. (1996). Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infection and Immunity, 64, 37–43Google Scholar
Telford, G., Wheeler, D., Williams, P., Tomkins, P. T., Appleby, P., Sewell, H., Stewart, G. S. A. B., Bycroft, B. W. and Pritchard, D. I. (1998). The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3–oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infection and Immunity, 66, 36–42Google ScholarPubMed
Tombolini, R., Unge, A., Davey, M. E., Bruijn, F. J. and Jansson, J. K. (1997). Flow cytometric and microscopic analysis of GFP-tagged Pseudomonas fluorescens bacteria. FEMS Microbiology Ecology, 22, 17–28CrossRefGoogle Scholar
Woods, D. E., Sokol, P. A., Bryan, L. E., Storey, D. G., Mattingly, S. J., Vogel, H. J. and Ceri, H. (1991). In vivo regulation of virulence in Pseudomonas aeruginosa associated with genetic rearrangement. Journal of Infectious Diseases, 163, 143–149CrossRefGoogle ScholarPubMed
Wu, H., Song, Z., Hentzer, M.Andersen, J. B., Heydorn, A., Mathee, K., Moser, C., Eberl, L., Molin, S., H⊘iby, N., and Givskov, M. (2000). Detection of N-acyl-homoserine lactones in lung tissue of mice infected with Pseudomonas aeruginosa. Microbiology, 146, 2481–2493CrossRefGoogle Scholar

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  • Quorum Sensing and Microbial Biofilms
    • By Teresa R. de Kievit, Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada, Barbara H. Iglewski, Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York, USA
  • Edited by Michael Wilson, University College London, Deirdre Devine, Leeds Dental Institute, University of Leeds
  • Book: Medical Implications of Biofilms
  • Online publication: 23 November 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546297.003
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  • Quorum Sensing and Microbial Biofilms
    • By Teresa R. de Kievit, Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada, Barbara H. Iglewski, Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York, USA
  • Edited by Michael Wilson, University College London, Deirdre Devine, Leeds Dental Institute, University of Leeds
  • Book: Medical Implications of Biofilms
  • Online publication: 23 November 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546297.003
Available formats
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To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

  • Quorum Sensing and Microbial Biofilms
    • By Teresa R. de Kievit, Department of Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada, Barbara H. Iglewski, Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York, USA
  • Edited by Michael Wilson, University College London, Deirdre Devine, Leeds Dental Institute, University of Leeds
  • Book: Medical Implications of Biofilms
  • Online publication: 23 November 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511546297.003
Available formats
×