Key Points
-
Chemotaxis has long been proposed to be important in helping motile pathogens to locate the appropriate niche for colonization within the host. In the case of many non-invasive enteric pathogens this principle holds true, with one exception — the cholera bacterium Vibrio cholerae.
-
Chemotaxis seems to restrict V. cholerae colonization of the infant-mouse small intestine, the most commonly used model of infection. In the absence of functional chemotaxis, V. cholerae exhibit expanded colonization of the intestinal tract and a concomitant increase in infectivity compared to the wild-type strain.
-
V. cholerae shed from cholera patients have a competitive advantage over their in vitro grown counterparts during the infection of infant mice. This is probably the result of a number of factors, one of which might be a defect in chemotaxis, as suggested by transcriptome analysis. If true, this might have important implications for our understanding of the infectious process.
-
The V. cholerae genome is complex with respect to chemotaxis, having three distinct operons that encode separate chemotaxis systems. Two of these operons are dispensable for chemotaxis in vitro and for infection.
-
The role that chemotaxis and motility play in the environmental stages of V. cholerae has not yet been determined. It is probable that chemotaxis has a role in locating suitable environmental hosts and surfaces. The additional chemotaxis systems might play a role in this aspect of the V. cholerae life cycle by regulating the activity of other functions besides motility.
Abstract
Chemotaxis is the process by which motile cells move in a biased manner both towards favourable and away from unfavourable environments. The requirement of this process for infection has been examined in several bacterial pathogens, including Vibrio cholerae. The single polar flagellum of Vibrio species is powered by a sodium-motive force across the inner membrane, and can rotate to produce speeds of up to 60 cell-body lengths (∼60μm) per second. Investigating the role of the chemotactic control of rapid flagellar motility during V. cholerae infection has revealed some unexpected and intriguing results.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Meeting on the Potential Role of New Cholera Vaccines in the Prevention and Control of Cholera Outbreaks during Acute Emergencies. in Document CDR/GPV/95. 1 (World Health Organization, Geneva, 1995).
Sack, D. A., Sack, R. B., Nair, G. B. & Siddique, A. K. Cholera. Lancet 363, 223–233 (2004). This review provides an overview of cholera, from the disease itself to its epidemiology and virulence gene regulation.
Wachsmuth, I. K., Blake, P. A. & Olsvik, O. Vibrio cholerae and Cholera: Molecular to Global Perspectives (ASM press, Washington DC, 1994).
Sack, D. A. et al. Validation of a volunteer model of cholera with frozen bacteria as the challenge. Infect. Immun. 66, 1968–1972 (1998).
Merrell, D. S. & Camilli, A. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34, 836–849 (1999).
Herrington, D. A. et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168, 1487–1492 (1988).
Taylor, R. K., Miller, V. L., Furlong, D. B. & Mekalanos, J. J. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA 84, 2833–2837 (1987).
Kirn, T. J., Lafferty, M. J., Sandoe, C. M. & Taylor, R. K. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35, 896–910 (2000).
Gill, D. M. Mechanism of action of cholera toxin. Adv. Cyclic Nucleotide Res. 8, 85–118 (1977).
DiRita, V. J. Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol. 6, 451–458 (1992).
Skorupski, K. & Taylor, R. K. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol. Microbiol. 25, 1003–1009 (1997).
Glass, R. I. & Black, R. E. The epidemiology of cholera. In Current Topics in Infectious Disease: Cholera (eds Barua, D. & Greenough, W. B.) 129–154 (Plenum Publishing Corporation, New York, 1992).
Merrell, D. S. et al. Host-induced epidemic spread of the cholera bacterium. Nature 417, 642–645 (2002). The competitive advantage observed with stool V. cholerae during infection, as well as the stool transcriptome analysis, is shown in this paper.
Colwell, R. R. & Spira, W. M. The ecology of Vibrio cholerae. In Current Topics in Infectious Disease: Cholera (eds Barua, D. & Greenough, W. B.) 107–127 (Plenum Publishing Corporation, New York, 1992).
Huq, A. et al. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45, 275–283 (1983).
Chiavelli, D. A., Marsh, J. W. & Taylor, R. K. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67, 3220–3225 (2001).
Islam, M. S., Drasar, B. S. & Bradley, D. J. Long-term persistence of toxigenic Vibrio cholerae O1 in the mucilaginous sheath of a blue-green alga, Anabaena variabilis. J. Trop. Med. Hyg. 93, 133–139 (1990).
Islam, M. S. et al. Role of cyanobacteria in the persistence of Vibrio cholerae O139 in saline microcosms. Can. J. Microbiol. 50, 127–131 (2004).
Broza, M. & Halpern, M. Pathogen reservoirs. Chironomid egg masses and Vibrio cholerae. Nature 412, 40 (2001).
Halpern, M., Broza, Y. B., Mittler, S., Arakawa, E. & Broza, M. Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 47, 341–349 (2004).
Colwell, R. R. & Huq, A. Vibrios in the environment: viable but nonculturable Vibrio cholerae. In Vibrio cholerae and Cholera (eds Wachsmuth, I. K., Blake, P. A. & Olsvik, Ø.) 117–133 (ASM Press, Washington DC, 1994).
Watnick, P. I. & Kolter, R. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34, 586–595 (1999).
Meibom, K. L. et al. The Vibrio cholerae chitin utilization program. Proc. Natl Acad. Sci. USA 101, 2524–2529 (2004).
Watnick, P. I., Lauriano, C. M., Klose, K. E., Croal, L. & Kolter, R. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39, 223–235 (2001).
Zhu, J. & Mekalanos, J. J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell. 5, 647–656 (2003).
Sjoblad, R. D., Emala, C. W. & Doetsch, R. N. Invited review: bacterial flagellar sheaths: structures in search of a function. Cell Motil. 3, 93–103 (1983).
Kojima, S., Yamamoto, K., Kawagishi, I. & Homma, M. The polar flagellar motor of Vibrio cholerae is driven by an Na+ motive force. J. Bacteriol. 181, 1927–1930 (1999).
Häse, C. C. & Mekalanos, J. J. Effects of changes in membrane sodium flux on virulence gene expression in Vibrio cholerae. Proc. Natl Acad. Sci. USA 96, 3183–3187 (1999).
Magariyama, Y. et al. Very fast flagellar rotation. Nature 371, 752 (1994).
McCarter, L. L. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 65, 445–462 (2001).
Wall, D. & Kaiser, D. Type IV pili and cell motility. Mol. Microbiol. 32, 1–10 (1999).
Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289–314 (2002).
McBride, M. J. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55, 49–75 (2001).
Szurmant, H., Muff, T. J. & Ordal, G. W. Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J. Biol. Chem. 279, 21787–21792 (2004).
Kristich, C. J. & Ordal, G. W. Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J. Biol. Chem. 277, 25356–25362 (2002).
Rosario, M. M., Fredrick, K. L., Ordal, G. W. & Helmann, J. D. Chemotaxis in Bacillus subtilis requires either of two functionally redundant CheW homologs. J. Bacteriol. 176, 2736–2739 (1994).
Heidelberg, J. F. et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477–483 (2000).
Bourret, R. B., Charon, N. W., Stock, A. M. & West, A. H. Bright lights, abundant operons — fluorescence and genomic technologies advance studies of bacterial locomotion and signal transduction: review of the BLAST meeting, Cuernavaca, Mexico, 14 to 19 January 2001. J. Bacteriol. 184, 1–17 (2002).
Boin, M. A., Austin, M. J. & Häse, C. C. Chemotaxis in Vibrio cholerae. FEMS Microbiol. Lett. 239, 1–8 (2004).
Gosink, K. K., Kobayashi, R., Kawagishi, I. & Häse, C. C. Analyses of the roles of the three cheA homologs in chemotaxis of Vibrio cholerae. J. Bacteriol. 184, 1767–1771 (2002). This paper shows that only one of the three chemotaxis operons is required for chemotaxis.
Lee, S. H., Butler, S. M. & Camilli, A. Selection for in vivo regulators of bacterial virulence. Proc. Natl Acad. Sci. USA 98, 6889–6894 (2001).
Yang, Z. et al. Myxococcus xanthus dif genes are required for biogenesis of cell surface fibrils essential for social gliding motility. J. Bacteriol. 182, 5793–5798 (2000).
Sun, H., Zusman, D. R. & Shi, W. Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr. Biol. 10, 1143–1146 (2000).
Vlamakis, H. C., Kirby, J. R. & Zusman, D. R. The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility. Mol. Microbiol. 52, 1799–1811 (2004).
Kirby, J. R. & Zusman, D. R. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 2008–2013 (2003).
Darzins, A. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Mol. Microbiol. 11, 137–153 (1994).
Brown, I. I. & Häse, C. C. Flagellum-independent surface migration of Vibrio cholerae and Escherichia coli. J. Bacteriol. 183, 3784–3790 (2001).
Josenhans, C. & Suerbaum, S. The role of motility as a virulence factor in bacteria. Int. J. Med. Microbiol. 291, 605–614 (2002). This review covers the topic of motility and its role in virulence in several bacterial pathogens.
Lockman, H. A. & Curtiss, R. Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect. Immun. 58, 137–143 (1990).
Cossart, P. & Sansonetti, P. J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242–248 (2004).
Forstner, J. F., Oliver, M. G. & Sylvester, F. A. Production, structure, and biologic relevance of gastrointestinal mucins. In Infections of the Gastrointestinal Tract (eds Blaser, M. J., Smith, P. D., Ravdin, J. I., Greenberg H. B. & Guerrant, R. L.) 71–88 (Raven Press, New York, 1995).
Young, G. M., Badger, J. L. & Miller, V. L. Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect. Immun. 68, 4323–4326 (2000).
Blaser, M. J. Ecology of Helicobacter pylori in the human stomach. J. Clin. Invest. 100, 759–762 (1997).
Lee, A., O'Rourke, J. L., Barrington, P. J. & Trust, T. J. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect. Immun. 51, 536–546 (1986).
Butler, S. M. & Camilli, A. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl Acad. Sci. USA 101, 5018–5023 (2004). This paper shows that the competitive advantage associated with non-chemotactic mutants is only observed in the presence of CCW-biased flagellar rotation and that net motility affects the infectivity of this bacterium.
Hang, L. et al. Use of in vivo-induced antigen technology (IVIAT) to identify genes uniquely expressed during human infection with Vibrio cholerae. Proc. Natl Acad. Sci. USA 100, 8508–8513 (2003). Using the IVIAT technique, this paper identifies proteins that are expressed during infection in cholera patients, five of which are chemotaxis proteins.
Everiss, K. D., Hughes, K. J., Kovach, M. E. & Peterson, K. M. The Vibrio cholerae acfB colonization determinant encodes an inner membrane protein that is related to a family of signal-transducing proteins. Infect. Immun. 62, 3289–3298 (1994).
Harkey, C. W., Everiss, K. D. & Peterson, K. M. The Vibrio cholerae toxin-coregulated-pilus gene tcpI encodes a homolog of methyl-accepting chemotaxis proteins. Infect. Immun. 62, 2669–2678 (1994).
O'Toole, R., Milton, D. L. & Wolf-Watz, H. Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum. Mol. Microbiol. 19, 625–637 (1996).
Millikan, D. S. & Ruby, E. G. Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects. Appl. Environ. Microbiol. 68, 2519–2528 (2002).
DeLoney-Marino, C. R., Wolfe, A. J. & Visick, K. L. Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl. Environ. Microbiol. 69, 7527–7530 (2003).
Jones, B. D., Lee, C. A. & Falkow, S. Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect. Immun. 60, 2475–2480 (1992).
Freter, R., Allweiss, B., O'Brien, P. C., Halstead, S. A. & Macsai, M. S. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vitro studies. Infect. Immun. 34, 241–249 (1981).
Freter, R., O'Brien, P. C. & Macsai, M. S. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34, 234–240 (1981).
Freter, R. & O'Brien, P. C. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonchemotactic Vibrio cholerae mutants in infant mice. Infect. Immun. 34, 222–233 (1981). This is the first time that non-chemotactic mutants were shown to have a competitive advantage during experimental infection. The authors show that wild-type V. cholerae penetrate into the intestinal crypts, whereas non-chemotactic mutants remain confined to the luminal half of the villi.
Ouellette, A. J. Defensin-mediated innate immunity in the small intestine. Best Pract. Res. Clin. Gastroenterol. 18, 405–419 (2004).
Ouellette, A. J. et al. Developmental regulation of cryptdin, a corticostatin/defensin precursor mRNA in mouse small intestinal crypt epithelium. J. Cell Biol. 108, 1687–1695 (1989).
Worku, M. L., Karim, Q. N., Spencer, J. & Sidebotham, R. L. Chemotactic response of Helicobacter pylori to human plasma and bile. J. Med. Microbiol. 53, 807–811 (2004).
O'Toole, R. et al. The chemotactic response of Vibrio anguillarum to fish intestinal mucus is mediated by a combination of multiple mucus components. J. Bacteriol. 181, 4308–4317 (1999).
Prouty, A. M. et al. Transcriptional regulation of Salmonella enterica serovar Typhimurium genes by bile. FEMS Immunol. Med. Microbiol. 41, 177–185 (2004).
Gupta, S. & Chowdhury, R. Bile affects production of virulence factors and motility of Vibrio cholerae. Infect. Immun. 65, 1131–1134 (1997).
Schuhmacher, D. A. & Klose, K. E. Environmental signals modulate ToxT-dependent virulence factor expression in Vibrio cholerae. J. Bacteriol. 181, 1508–1514 (1999).
Ottemann, K. M. & Miller, J. F. Roles for motility in bacterial-host interactions. Mol. Microbiol. 24, 1109–1117 (1997). An overview of motility and infection is given in this review.
Giron, J. A., Torres, A. G., Freer, E. & Kaper, J. B. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44, 361–379 (2002).
Jones, G. W. & Freter, R. Adhesive properties of Vibrio cholerae: nature of the interaction with isolated rabbit brush border membranes and human erythrocytes. Infect. Immun. 14, 240–245 (1976).
Freter, R. & Jones, G. W. Adhesive properties of Vibrio cholerae: nature of the interaction with intact mucosal surfaces. Infect. Immun. 14, 246–256 (1976).
Richardson, K. Roles of motility and flagellar structure in pathogenicity of Vibrio cholerae: analysis of motility mutants in three animal models. Infect. Immun. 59, 2727–2736 (1991).
Gardel, C. L. & Mekalanos, J. J. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect. Immun. 64, 2246–2255 (1996).
Klose, K. E. & Mekalanos, J. J. Distinct roles of an alternative σ factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28, 501–520 (1998).
Mekalanos, J. J. & Sadoff, J. C. Cholera vaccines: fighting an ancient scourge. Science 265, 1387–1389 (1994).
Kenner, J. R. et al. Peru-15, an improved live attenuated oral vaccine candidate for Vibrio cholerae O1. J. Infect. Dis. 172, 1126–1129 (1995).
Coster, T. S. et al. Safety, immunogenicity, and efficacy of live attenuated Vibrio cholerae O139 vaccine prototype. Lancet 345, 949–952 (1995).
Mekalanos, J. J. et al. Live cholera vaccines: perspectives on their construction and safety. Bull. Inst. Pasteur 93, 255–262 (1995).
Goodier, R. I. & Ahmer, B. M. SirA orthologs affect both motility and virulence. J. Bacteriol. 183, 2249–2258 (2001).
Ellermeier, C. D. & Slauch, J. M. RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185, 5096–5108 (2003).
Akerley, B. J., Monack, D. M., Falkow, S. & Miller, J. F. The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J. Bacteriol. 174, 980–990 (1992).
McCarter, L., Hilmen, M. & Silverman, M. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell 54, 345–351 (1988).
Kawagishi, I., Imagawa, M., Imae, Y., McCarter, L. & Homma, M. The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression. Mol. Microbiol. 20, 693–699 (1996).
Lauriano, C. M., Ghosh, C., Correa, N. E. & Klose, K. E. The sodium-driven flagellar motor controls exopolysaccharide expression in Vibrio cholerae. J. Bacteriol. 186, 4864–4874 (2004).
Häse, C. C. Analysis of the role of flagellar activity in virulence gene expression in Vibrio cholerae. Microbiology 147, 831–837 (2001). This work disproves the earlier hypothesis that the V. cholerae flagellum acts as a mechanosensor that is involved in regulating virulence gene expression.
Bina, J. et al. ToxR regulon of Vibrio cholerae and its expression in vibrios shed by cholera patients. Proc. Natl Acad. Sci. USA 100, 2801–2806 (2003).
Klose, K. E. The suckling mouse model of cholera. Trends Microbiol. 8, 189–191 (2000).
Lee, S. H., Hava, D. L., Waldor, M. K. & Camilli, A. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99, 625–634 (1999).
Pennisi, E. Cholera strengthened by trip through gut. Science 296, 1783–1784 (2002).
Bourret, R. B. & Stock, A. M. Molecular information processing: lessons from bacterial chemotaxis. J. Biol. Chem. 277, 9625–9628 (2002).
Manson, M. D., Armitage, J. P., Hoch, J. A. & Macnab, R. M. Bacterial locomotion and signal transduction. J. Bacteriol. 180, 1009–1022 (1998).
Bren, A. & Eisenbach, M. How signals are heard during bacterial chemotaxis: protein–protein interactions in sensory signal propagation. J. Bacteriol. 182, 6865–6873 (2000).
Szurmant, H. & Ordal, G. W. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol. Mol. Biol. Rev. 68, 301–319 (2004). This review covers chemotaxis components present in B. subtilis , but absent from E. coli , that are also shared by V. cholerae.
Lux, R. & Shi, W. Chemotaxis-guided movements in bacteria. Crit. Rev. Oral Biol. Med. 15, 207–220 (2004).
Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol. 5, 1024–1037 (2004). This review covers bacterial chemotaxis, with a focus on the E. coli literature.
Berg, H. C. & Brown, D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239, 500–504 (1972).
Falke, J. J. & Hazelbauer, G. L. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26, 257–265 (2001).
Wadhams, G. H. et al. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol. Microbiol. 46, 1211–1221 (2002).
Maddock, J. R. & Shapiro, L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717–1723 (1993).
Sourjik, V. & Berg, H. C. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol. Microbiol. 37, 740–751 (2000).
Sourjik, V. & Berg, H. C. Receptor sensitivity in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 99, 123–127 (2002).
Mao, H., Cremer, P. S. & Manson, M. D. A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc. Natl Acad. Sci. USA 100, 5449–5454 (2003).
Bray, D., Levin, M. D. & Morton-Firth, C. J. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88 (1998).
Bourret, R. B., Davagnino, J. & Simon, M. I. The carboxy-terminal portion of the CheA kinase mediates regulation of autophosphorylation by transducer and CheW. J. Bacteriol. 175, 2097–2101 (1993).
Kim, K. K., Yokota, H. & Kim, S. H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400, 787–792 (1999).
Li, J., Swanson, R. V., Simon, M. I. & Weis, R. M. The response regulators CheB and CheY exhibit competitive binding to the kinase CheA. Biochemistry 34, 14626–14636 (1995).
Bren, A. & Eisenbach, M. The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J. Mol. Biol. 278, 507–514 (1998).
Bren, A. & Eisenbach, M. Changing the direction of flagellar rotation in bacteria by modulating the ratio between the rotational states of the switch protein FliM. J. Mol. Biol. 312, 699–709 (2001).
Hess, J. F., Oosawa, K., Kaplan, N. & Simon, M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53, 79–87 (1988).
Springer, W. R. & Koshland, D. E. Jr. Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system. Proc. Natl Acad. Sci. USA 74, 533–537 (1977).
Yonekawa, H., Hayashi, H. & Parkinson, J. S. Requirement of the cheB function for sensory adaptation in Escherichia coli. J. Bacteriol. 156, 1228–1235 (1983).
Anand, G. S., Goudreau, P. N. & Stock, A. M. Activation of methylesterase CheB: evidence of a dual role for the regulatory domain. Biochemistry 37, 14038–14047 (1998).
Yao, R., Burr, D. H. & Guerry, P. CheY-mediated modulation of Campylobacter jejuni virulence. Mol. Microbiol. 23, 1021–1031 (1997).
Hendrixson, D. R. & DiRita, V. J. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52, 471–484 (2004).
Foynes, S. et al. Helicobacter pylori possesses two CheY response regulators and a histidine kinase sensor, CheA, which are essential for chemotaxis and colonization of the gastric mucosa. Infect. Immun. 68, 2016–2023 (2000).
Andermann, T. M., Chen, Y. T. & Ottemann, K. M. Two predicted chemoreceptors of Helicobacter pylori promote stomach infection. Infect. Immun. 70, 5877–5881 (2002).
Guo, B. P. & Mekalanos, J. J. Rapid genetic analysis of Helicobacter pylori gastric mucosal colonization in suckling mice. Proc. Natl Acad. Sci. USA 99, 8354–8359 (2002).
Dons, L. et al. Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect. Immun. 72, 3237–3244 (2004).
Burall, L. S. et al. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect. Immun. 72, 2922–2938 (2004).
Stecher, B. et al. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72, 4138–4150 (2004).
Halpern, M., Gancz, H., Broza, M. & Kashi, Y. Vibrio cholerae hemagglutinin/protease degrades chironomid egg masses. Appl. Environ. Microbiol. 69, 4200–4204 (2003).
Acknowledgements
We thank M. Angelichio for the scanning electron micrographs of Vibrio cholerae during infection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Glossary
- BIOFILM
-
Microbial biofilms are populations of microorganisms that are concentrated at an interface (usually solid–liquid) and typically surrounded by an extracellular polymeric substance matrix. Aggregates of cells that are not attached to a surface are sometimes termed 'flocs' and have many of the characteristics of biofilms.
- PLANKTONIC CELLS
-
Single cells in suspension, instead of in a biofilm.
- PERISTALSIS
-
Successive contractions of the muscular walls of the gut that move gut contents along.
Rights and permissions
About this article
Cite this article
Butler, S., Camilli, A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3, 611–620 (2005). https://doi.org/10.1038/nrmicro1207
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrmicro1207
This article is cited by
-
Development of a smart pH-responsive nano-polymer drug, 2-methoxy-4-vinylphenol conjugate against the intestinal pathogen, Vibrio cholerae
Scientific Reports (2023)
-
The implication of viability and pathogenicity by truncated lipopolysaccharide in Yersinia enterocolitica
Applied Microbiology and Biotechnology (2023)
-
Collective responses of bacteria to a local source of conflicting effectors
Scientific Reports (2022)
-
Biofilm formation and inhibition mediated by bacterial quorum sensing
Applied Microbiology and Biotechnology (2022)
-
Microscale tracking of coral-vibrio interactions
ISME Communications (2021)