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Vibrio cholerae Flagellar Synthesis and Virulence

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Epidemiological and Molecular Aspects on Cholera

Part of the book series: Infectious Disease ((ID))

Abstract

Flagellar-mediated motility has been demonstrated to contribute to the pathogenesis of Vibrio cholerae. Nonmotile mutants of live attenuated cholera vaccine strains are significantly less reactogenic in human volunteers, but the exact contribution of motility to virulence appears to be multi-factorial. The flagellum of V. cholerae is a complex structure made up of multiple structural subunits (>40 proteins). Expression of flagellar genes proceeds via a transcription hierarchy. This flagellar regulatory cascade controls not only flagellar gene expression, but also influences the expression of additional (non-flagellar) genes with proven or implicated roles in virulence. Flagellar-mediated chemotaxis appears to be linked to transmission of V. cholerae from host to host, and thus epidemic spread of cholera. Motility also contributes to biofilm formation, which facilitates environmental persistence. Thus, the flagellum plays an integral part in the lifecycle of V. cholerae, both in the host as well as in the environment.

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References

  1. Moens S, Vanderleyden J. Functions of bacterial flagella. Crit Rev Microbiol. 1996;22: 67–100.

    Article  PubMed  CAS  Google Scholar 

  2. Richardson K. Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect Immun. 1991;59:2727–36.

    PubMed  CAS  Google Scholar 

  3. Silva AJ, Leitch GJ, Camilli A, Benitez JA. Contribution of hemagglutinin/protease and motility to the pathogenesis of El Tor biotype cholera. Infect Immun. 2006;74:2072–9.

    Article  PubMed  CAS  Google Scholar 

  4. Attridge SR, Rowley D. The role of the flagellum in the adherence of Vibrio cholerae. J Infect Dis. 1983;147:864–72.

    Article  PubMed  CAS  Google Scholar 

  5. Coster, TS, Killeen KP, Waldor MK, Beattie D, Spriggs D, Kenner JR, Trofa A, Sadoff J, Mekalanos JJ, Taylor DN. Safety, immunogenicity and efficacy of a live attenuated Vibrio cholerae O139 vaccine prototype, Bengal-15. Lancet. 1995;345:949–52.

    Article  PubMed  CAS  Google Scholar 

  6. Kenner JR, Coster TS, Taylor DN, Trofa AF, Barrera-Oro M, Hyman T, Adams JM, Beattie DT, Killeen, KP, Spriggs DR, Mekalanos JJ, Sadoff JC. Peru-15, an improved live attenuated vaccine candidate for Vibrio cholerae O1. J Infect Dis. 1995;172:1126–9.

    Article  PubMed  CAS  Google Scholar 

  7. Watnick PI, Kolter R. Steps in the development of a Vibrio cholerae biofilm. Mol Microbiol. 1999;34:586–95.

    Article  PubMed  CAS  Google Scholar 

  8. Watnick P, Kolter R. Biofilm, city of microbes. J Bacteriol. 2000;182:2675–9.

    Article  PubMed  CAS  Google Scholar 

  9. Heidelberg JF, Eisen JA, Nelson WC, Clayton RA, Gwinn ML, Dodson RJ, Haft DH, Hickey EK, Peterson JD, Umayam L, Gill, SR, Nelson KE, Read TD, Tettelin H, Richardson D, Ermolaeva MD, Vamathevan J, Bass S, Qin H, Dragoi I, Sellers P, McDonald L, Utterback T, Fleishmann RD, Nierman WC, White O, Salzberg SL, Smith HO, Colwell RR, Mekalanos JJ, Venter, JC., Fraser CM. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature. 2000;406:477–83.

    Article  PubMed  CAS  Google Scholar 

  10. Macnab RM. How bacteria assemble flagella. Annu Rev Microbiol. 2003;57:77–100.

    Article  PubMed  CAS  Google Scholar 

  11. Macnab RM. Type III flagellar protein export and flagellar assembly. Biochim Biophys Acta. 2004;1694:207–17.

    Article  PubMed  CAS  Google Scholar 

  12. Klose KE, Mekalanos JJ. Differential regulation of multiple flagellins in Vibrio cholerae. J Bacteriol. 1998;180:303–16.

    PubMed  CAS  Google Scholar 

  13. Fuerst JA, Perry JW. Demonstration of lipopolysaccharide on sheathed flagella of Vibrio cholerae O1 by protein A-gold immunoelectron microscopy. J Bacteriol. 1988;170:1488–94.

    PubMed  CAS  Google Scholar 

  14. Prouty MG, Correa NE, Klose KE. The novel s54- and s28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol Microbiol. 2001;39:1595–609.

    Article  PubMed  CAS  Google Scholar 

  15. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, Lory S, Ramphal, R. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol. 2003;50:809–24.

    Article  PubMed  CAS  Google Scholar 

  16. Macnab RM. Flagella and motility. In: Neidhardt FC, Curtiss, RI, Ingraham, JL, Lin ECC, Low, KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE, editors. Escherichia coli and Salmonella: cellular and molecular biology. Washington, DC: ASM Press; 1996. pp. 123–45.

    Google Scholar 

  17. Dasgupta N, Ferrell EP, Kanack KJ, West SE, Ramphal R. fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is sigma70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J Bacteriol. 2002;184:5240–50.

    Article  PubMed  CAS  Google Scholar 

  18. Correa NE, Peng F, Klose KE. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J Bacteriol. 2005;187:6324–32.

    Article  PubMed  CAS  Google Scholar 

  19. Correa NE, Lauriano CM, McGee R, Klose KE. Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol Microbiol. 2000;35:743–55.

    Article  PubMed  CAS  Google Scholar 

  20. Hendrixson DR, DiRita VJ. Transcription of sigma54-dependent but not sigma28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol. 2003;50:687–702.

    Article  PubMed  CAS  Google Scholar 

  21. Hughes KT, Gillen KL, Semon MJ, Karlinsey JE. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science. 1993;262:1277–80.

    Article  PubMed  CAS  Google Scholar 

  22. Correa NE, Barker JR, Klose KE. The Vibrio cholerae FlgM homologue is an anti-sigma28 factor that is secreted through the polar sheathed flagellum. J Bacteriol. 2004;186:4613–9.

    Article  PubMed  CAS  Google Scholar 

  23. Freter R, O’Brien PCM, Macsai MS. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect Immun. 1981;34:234–40.

    PubMed  CAS  Google Scholar 

  24. Lee SH, Butler SM, Camilli A. Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci USA. 2001;98:6889–94.

    Article  PubMed  CAS  Google Scholar 

  25. Gardel CL Mekalanos JJ. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun. 1996;64:2246–55.

    Google Scholar 

  26. Ghosh A, Paul K, Chowdhury R. Role of the histone-like nucleoid structuring protein in colonization, motility, and bile-dependent repression of virulence gene expression in Vibrio cholerae. Infect Immun. 2006;74:3060–4.

    Article  PubMed  CAS  Google Scholar 

  27. Lim B, Beyhan S, Meir J, Yildiz FH. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol Microbiol. 2006;60:331–48.

    Article  PubMed  CAS  Google Scholar 

  28. Tischler AD, Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 2004;53:857–69.

    Article  PubMed  CAS  Google Scholar 

  29. Tischler, AD, Camilli A. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun. 2005;73:5873–82.

    Article  PubMed  CAS  Google Scholar 

  30. Akerley BJ, Cotter PA, Miller JF. Ectopic expression of the flagellar regulon alters development of the Bordetella–host interaction. Cell. 1995;80:611–20.

    Article  PubMed  CAS  Google Scholar 

  31. Goodier RI, Ahmer, BM. SirA orthologs affect both motility and virulence. J Bacteriol. 2001;183:2249–58.

    Article  PubMed  CAS  Google Scholar 

  32. Quinones B, Dulla G, Lindow SE. Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact. 2005;18:682–93.

    Article  PubMed  CAS  Google Scholar 

  33. Dasgupta, N, Ferrell EP, Kanack KJ, West SE, Ramphal R. fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is sigma70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J Bacteriol. 2002;184:5240–50.

    Article  PubMed  CAS  Google Scholar 

  34. Bren A, Eisenbach M. How signals are heard during bacterial chemotaxis: protein–protein interactions in sensory signal propagation. J Bacteriol. 2000;182:6865–73.

    Article  PubMed  CAS  Google Scholar 

  35. Butler SM, Camilli A. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci USA. 2004;101:5018–23.

    Article  PubMed  CAS  Google Scholar 

  36. Butler SM, Nelson EJ, Chowdhury N, Faruque SM, Calderwood SB, Camilli A. Cholera stool bacteria repress chemotaxis to increase infectivity. Mol Microbiol. 2006;60:417–26.

    Article  PubMed  CAS  Google Scholar 

  37. Gosink KK, Kobayashi R, Kawagishi I, Hase CC. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J Bacteriol. 2002;184:1767–71.

    Article  PubMed  CAS  Google Scholar 

  38. Hyakutake A, Homma M, Austin MJ, Boin MA, Hase CC, Kawagishi I. Only one of the five CheY homologs in Vibrio cholerae directly switches flagellar rotation. J Bacteriol. 2005;187:8403–10.

    Article  PubMed  CAS  Google Scholar 

  39. Merrell DS, Butler SM, Qadri F, Dolganov NA, Alam A, Cohen MB, Calderwood SB, Schoolnik GK, Camilli A. Host-induced epidemic spread of the cholera bacterium. Nature. 2002;417:642–5.

    Article  PubMed  CAS  Google Scholar 

  40. Davey ME, O’Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev. 2000;64:847–67.

    Article  PubMed  CAS  Google Scholar 

  41. Wai SN, Mizunoe Y, Takade A, Kawabata SI, Yoshida SI. Vibrio cholerae O1 strain TSI-4 produces the exopolysaccharide materials that determine colony morphology, stress resistance, and biofilm formation. Appl Environ Microbiol. 1998;64:3648–55.

    PubMed  CAS  Google Scholar 

  42. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol. 2001;39:223–35.

    Article  PubMed  CAS  Google Scholar 

  43. Yildiz FH, Schoolnik GK. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA. 1999;96:4028–33.

    Article  PubMed  CAS  Google Scholar 

  44. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms. Annu Rev Microbiol. 1995;49:711–45.

    Article  PubMed  CAS  Google Scholar 

  45. Moorthy S, Watnick PI. Genetic evidence that the Vibrio cholerae monolayer is a distinct stage in biofilm development. Mol Microbiol. 2004;52:573–87.

    Article  PubMed  CAS  Google Scholar 

  46. Moorthy S, Watnick, PI. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol Microbiol. 2005;57:1623–35.

    Article  PubMed  CAS  Google Scholar 

  47. Yildiz FH, Liu, XS, Heydorn A, Schoolnik GK. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol Microbiol. 2004;53:497–515.

    Article  PubMed  CAS  Google Scholar 

  48. Lauriano CM, Ghosh C, Correa NE, Klose, KE. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J Bacteriol. 2004;186:4864–74.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

K.E. Klose is funded by NIH AI43486 and AI51333.

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Authors and Affiliations

  1. South Texas Center for Emerging Infectious Diseases and Department of Biology, University of Texas San Antonio, San Antonio, TX, 78249, USA

    Khalid Ali Syed

  2. Department of Biology, South Texas Center for Emerging Infectious Diseases, University of Texas San Antonio, San Antonio, TX, 78249-1644, USA

    Karl E. Klose

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  1. Khalid Ali Syed
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Correspondence to Karl E. Klose .

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Editors and Affiliations

  1. National Institute of Cholera and Enteri, P-33 C.I.T. Road Scheme XM, Calcutta, 700010, India

    T. Ramamurthy

  2. Indian Council of Medical Research, New Delhi, 110029, India

    S.K. Bhattacharya

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Syed, K.A., Klose, K.E. (2011). Vibrio cholerae Flagellar Synthesis and Virulence. In: Ramamurthy, T., Bhattacharya, S. (eds) Epidemiological and Molecular Aspects on Cholera. Infectious Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-60327-265-0_11

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  • DOI: https://doi.org/10.1007/978-1-60327-265-0_11

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  • Online ISBN: 978-1-60327-265-0

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