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5 - Quorum-sensing-mediated regulation of biofilm growth and virulence of Vibrio cholerae

Published online by Cambridge University Press:  08 August 2009

By
Jun Zhu  and
John J. Mekalanos
Edited by
Donald R. Demuth  and
Richard Lamont
Jun Zhu
Affiliation:
University of Pennsylvania School of Medicine
John J. Mekalanos
Affiliation:
Harvard Medical School Boston, MA USA
Donald R. Demuth
Affiliation:
University of Louisville, Kentucky
Richard Lamont
Affiliation:
University of Florida
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Summary

INTRODUCTION

Many species of bacterium exchange chemical signals to help them monitor their population densities, a phenomenon referred to as quorum sensing. Quorum sensing was first described over two decades ago in two luminescent marine bacterial species, Vibrio fischeri and V. harveyi (40), which have served as model species for studies of cell-density-dependent gene expression. In both species, the enzymes responsible for light production are encoded by the luciferase structural operon luxCDABE (13, 39) and light emission occurs only at high cell density in response to the accumulation of secreted autoinducer signaling molecules (40). In the 1980s, Eberhard et al. (11) purified the first homoserine lactone autoinducer from V. fischeri and showed that it was indeed a specific inducer of luminescence. In 1983, the basic features of the autoinduction system were revealed at the molecular level when the lux genes of V. fischeri were successfully cloned and expressed in Escherichia coli (12).

Although quorum sensing regulation has been analyzed in great detail in V. harveyi and V. fischeri, the study of quorum sensing phenotypes in the clinically important Vibrio species V. cholerae was virtually non-existent until quite recently. This was partly because, unlike V. fischeri and V. harveyi, V. cholerae does not possess luciferase genes and it was therefore unclear whether it possessed any genes that were regulated by quorum sensing. However, when the V. cholerae genome sequence was completed (22) it was revealed that V. cholerae contains several quorum-sensing genes similar to those of V. harveyi.

Type
Chapter
Information
Bacterial Cell-to-Cell Communication
Role in Virulence and Pathogenesis
 , pp. 101 - 116
Publisher: Cambridge University Press
Print publication year: 2006

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References

Bassler, B. L. 1999. How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr. Opin. Microbiol. 2: 582–7.CrossRefGoogle ScholarPubMed
Bassler, B. L., Wright, M. and Silverman, M. R. 1994. Multiple signaling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Molec. Microbiol. 13: 273–86.CrossRefGoogle ScholarPubMed
Bina, J., Zhu, J., Dziejman, M.et al. 2003. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natn. Acad. Sci. USA 100: 2801–6.CrossRefGoogle ScholarPubMed
Broza, M. and Halpern, M. 2001. Pathogen reservoirs. Chironomid egg masses and Vibrio cholerae. Nature 412: 40.CrossRefGoogle ScholarPubMed
Casper-Lindley, C. and Yildiz, F. H. 2004. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J. Bacteriol. 186: 1574–8.CrossRefGoogle ScholarPubMed
Chen, X., Schauder, S., Potier, N. 2002. Structural identification of a bacterial quorum sensing signal containing boron. Nature 415: 545–9.CrossRefGoogle ScholarPubMed
Colwell, R. R. 1996. Global climate and infectious disease: the cholera paradigm. Science 274: 2025–31.CrossRefGoogle ScholarPubMed
Colwell, R. R., Huq, A., Islam, M. S.et al. 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natn. Acad. Sci. USA 100: 1051–5.CrossRefGoogle ScholarPubMed
Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. and Lappin-Scott, H. M. 1995. Microbial biofilms. A. Rev. Microbiol. 49: 711–45.CrossRefGoogle ScholarPubMed
Costerton, J. W., Stewart, P. S. and Greenberg, E. P. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318–22.CrossRefGoogle ScholarPubMed
Eberhard, A., Burlingame, A. L., Eberhard, C.et al. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444–9.CrossRefGoogle ScholarPubMed
Engebrecht, J., Nealson, K. and Silverman, M. 1983. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32: 773–81.CrossRefGoogle ScholarPubMed
Engebrecht, J. and Silverman, M. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natn. Acad. Sci. USA 81: 4154–8.CrossRefGoogle ScholarPubMed
Faruque, S., Nasser, I. B., Islam, M. J.et al. 2005. Seasonal epidemics of cholera are inversely correlated with the prevalence of environmental cholera phages. Proc. Natn. Acad. Sci. USA 102: 1702–7.CrossRefGoogle Scholar
Faruque, S. M., Albert, M. J. and Mekalanos, J. J. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Molec. Biol. Rev. 62: 1301–14.Google ScholarPubMed
Finkelstein, R. A., Boesman-Finkelstein, M., Chang, Y. and Hase, C. C. 1992. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect. Immun. 60: 472–8.Google ScholarPubMed
Fuqua, C. and Greenberg, E. P. 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat. Rev. Molec. Cell Biol. 3: 685–95.CrossRefGoogle Scholar
Hall-Stoodley, L., Costerton, J. W. and Stoodley, P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95–108.CrossRefGoogle ScholarPubMed
Halpern, M., Broza, Y. B., Mittler, S., Arakawa, E., and Broza, M. 2004. Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 47: 341–9.CrossRefGoogle ScholarPubMed
Hammer, B. K. and Bassler, B. L. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Molec. Microbiol. 50: 101–4.CrossRefGoogle ScholarPubMed
Haugo, A. J. and Watnick, P. I. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Molec. Microbiol. 45: 471–83.CrossRefGoogle ScholarPubMed
Heidelberg, J. F., Eisen, J. A., Nelson, W. C.et al. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406: 477–83.Google ScholarPubMed
Huq, A., Huq, S. A., Grimes, D. J.et al. 1986. Colonization of the gut of the blue crab (Callinectes sapidus) by Vibrio cholerae. Appl. Environ. Microbiol. 52: 586–8.Google ScholarPubMed
Huq, A., Small, E. B., West, P. A.et al. 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45: 275–83.Google ScholarPubMed
Jobling, M. G. and Holmes, R. K. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Molec. Microbiol. 26: 1023–34.CrossRefGoogle ScholarPubMed
Kjelleberg, S. and Molin, S. 2002. Is there a role for quorum sensing signals in bacterial biofilms?Curr. Opin. Microbiol. 5: 254–8.CrossRefGoogle Scholar
Klose, K. E. 2001. Regulation of virulence in Vibrio cholerae. Int. J. Med. Microbiol. 291: 81–8.CrossRefGoogle ScholarPubMed
Klose, K. E. 2000. The suckling mouse model of cholera. Trends Microbiol. 8: 189–91.CrossRefGoogle ScholarPubMed
Klose, K. E., Novik, V. and Mekalanos, J. J. 1998. Identification of multiple sigma54-dependent transcriptional activators in Vibrio cholerae. J. Bacteriol. 180: 5256–9.Google ScholarPubMed
Kovacikova, G., Lin, W. and Skorupski, K. 2004. Vibrio cholerae AphA uses a novel mechanism for virulence gene activation that involves interaction with the LysR-type regulator AphB at the tcpPH promoter. Molec. Microbiol. 53: 129–42.CrossRefGoogle ScholarPubMed
Kovacikova, G. and Skorupski, K. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Molec. Microbiol. 46: 1135–47.CrossRefGoogle ScholarPubMed
Krukonis, E. S. and DiRita, V. J.. 2003. From motility to virulence: sensing and responding to environmental signals in Vibrio cholerae. Curr. Opin. Microbiol. 6: 186–90.CrossRefGoogle ScholarPubMed
Lauriano, C. M., Ghosh, C., Correa, N. E. and Klose, K. E. 2004. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J. Bacteriol. 186: 4864–74.CrossRefGoogle ScholarPubMed
Lee, S. H., Hava, D. L., Waldor, M. K. and Camilli, A. 1999. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99: 625–34.CrossRefGoogle ScholarPubMed
Lenz, D. H., Mok, K. C., Lilley, B. N.et al. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69–82.CrossRefGoogle ScholarPubMed
Merrell, D. S., Butler, S. M., Qadri, F.et al. 2002. Host-induced epidemic spread of the cholera bacterium. Nature 417: 642–5.CrossRefGoogle ScholarPubMed
Miller, M. B. and Bassler, B. L. 2001. Quorum sensing in bacteria. A. Rev. Microbiol. 55: 165–99.CrossRefGoogle ScholarPubMed
Miller, M. B., Skorupski, K., Lenz, D. H., Taylor, R. K. and Bassler, B. L. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303–14.CrossRefGoogle ScholarPubMed
Miyamoto, C. M., Boylan, M., Graham, A. F. and Meighen, E. A. 1988. Organization of the lux structural genes of Vibrio harveyi. Expression under the T7 bacteriophage promoter, mRNA analysis, and nucleotide sequence of the luxD gene. J. Biol. Chem. 263: 13393–9.Google ScholarPubMed
Nealson, K. H. and Hastings, J. W. 1979. Bacterial bioluminescence: its control and ecological significance. Microbiol. Rev. 43: 496–518.Google ScholarPubMed
World Health Organization 1995. Report meeting: The Potential Role of New Cholera Vaccine in the Prevention and Control of Cholera During Acute Emergencies. World Health Organization.
Reidl, J. and Klose, K. E. 2002. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26: 125–39.CrossRefGoogle Scholar
Schauder, S., Shokat, K., Surette, M. G. and Bassler, B. L. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Molec. Microbiol. 41: 463–76.CrossRefGoogle ScholarPubMed
Schembri, M. A., Givskov, M. and Klemm, P. 2002. An attractive surface: gram-negative bacterial biofilms. Sci. Signal Transduct. Knowl. Environ. 2002: RE6.Google ScholarPubMed
Schoolnik, G. K. and Yildiz, F. H. 2000. The complete genome sequence of Vibrio cholerae: a tale of two chromosomes and of two lifestyles. Genome Biol 1: Reviews, 1016 1–3.CrossRefGoogle ScholarPubMed
Skorupski, K. and Taylor, R. K. 1997. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Molec. Microbiol. 25: 1003–9.CrossRefGoogle ScholarPubMed
Storz, G., Opdyke, J. A. and Zhang, A. 2004. Controlling mRNA stability and translation with small, noncoding RNAs. Curr. Opin. Microbiol. 7: 140–4.CrossRefGoogle ScholarPubMed
Surette, M. G., Miller, M. B. and Bassler, B. L. 1999. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natn. Acad. Sci. USA 96: 1639–44.CrossRefGoogle ScholarPubMed
Tischler, A. D. and Camilli, A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Molec. Microbiol. 53: 857–69.CrossRefGoogle ScholarPubMed
Vance, R. E., Zhu, J. and Mekalanos, J. J. 2003. A constitutively active variant of the quorum-sensing regulator LuxO affects protease production and biofilm formation in Vibrio cholerae. Infect. Immun. 71: 2571–6.CrossRefGoogle ScholarPubMed
Wai, S. N., Mizunoe, Y., Takade, A., Kawabata, S. I. and Yoshida, S. I. 1998. Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl. Environ. Microbiol. 64: 3648–55.Google ScholarPubMed
Watnick, P. and Kolter, R. 2000. Biofilm, city of microbes. J. Bacteriol. 182: 2675–9.CrossRefGoogle ScholarPubMed
Watnick, P. I. and Kolter, R. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Molec. Microbiol. 34: 586–95.CrossRefGoogle ScholarPubMed
Watnick, P. I., Lauriano, C. M., Klose, K. E., Croal, L. and Kolter, R. 2001. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Molec. Microbiol. 39: 223–35.CrossRefGoogle ScholarPubMed
Xavier, K. B. and Bassler, B. L. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6: 191–7.CrossRefGoogle ScholarPubMed
Yildiz, F. H., Dolganov, N. A. and Schoolnik, G. K. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183: 1716–26.CrossRefGoogle ScholarPubMed
Yildiz, F. H., Liu, X. S., Heydorn, A. and Schoolnik, G. K. 2004. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Molec. Microbiol. 53: 497–515.CrossRefGoogle Scholar
Yildiz, F. H. and Schoolnik, G. K. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natn. Acad. Sci. USA 96: 4028–33.CrossRefGoogle ScholarPubMed
Zhu, J. and Mekalanos, J. J. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5: 647–56.CrossRefGoogle ScholarPubMed
Zhu, J., Miller, M. B., Vance, R. E.et al. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natn. Acad. Sci. USA 99: 3129–34.CrossRefGoogle ScholarPubMed

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