1887

Chapter 30 : Evolution of Vibrio cholerae and Cholera Epidemics

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Evolution of Vibrio cholerae and Cholera Epidemics, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815639/9781555814144_Chap30-1.gif /docserver/preview/fulltext/10.1128/9781555815639/9781555814144_Chap30-2.gif

Abstract:

Of more than 200 known serogroups of Vibrio cholerae, only strains of O1 or O139 serogroups cause cholera epidemics. This chapter summarizes information on the evolution of pathogenic V. cholerae with an insight into the significance of virulence factors being encoded by accessory genetic elements, and phages, and into factors associated with the generation of diversity among virulent strains. Although this amazing transformation of V. cholera strains associated with epidemics was observed only once in nearly two centuries of recorded history of cholera, this period is not too long in an evolutionary time frame. Paradoxically, besides virulence genes and genetic elements mediating their transfer, the most important contributor to the evolution of pathogenic V. cholera is the human host itself, which supports the selective enrichment of diverse pathogenic strains. Overall, these molecular epidemiological studies indicated that there are temporal variations in the clones involved with cholera epidemics in particular geographical regions. Phage predation in the environment influences the temporal dynamics of cholera epidemics. The continual emergence of new strains of toxigenic V. cholera and their selective enrichment during cholera outbreaks constitute an essential component of the ecosystem for the survival and evolution of V. cholera and the genetic elements that mediate the transfer of virulence genes. Such studies offer the opportunity to expand our understanding of the phylogenic relationships between pathogenic and nonpathogenic strains of V. cholera and the discovery of new genes that may be involved directly or indirectly in the evolution of pathogenic V. cholera.

Citation: Faruque S, Mekalanos J. 2008. Evolution of Vibrio cholerae and Cholera Epidemics, p 361-371. In Baquero F, Nombela C, Cassell G, Gutiérrez-Fuentes J (ed), Evolutionary Biology of Bacterial and Fungal Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555815639.ch30
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555815639.ch30
1. Attridge, S. R.,, E. Voss, and, P. A. Manning. 1993. The role of toxin co-regulated pili in the pathogenesis of Vibrio cholerae O1 El Tor. Microb. Pathog. 15:421431.
2. Bagchi, K.,, P. Echeverria,, J. D. Authur,, O. Sethabutr,, O. Serichantalergs, and, C. W. Hoge. 1993. Epidemic diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J. Clin. Microbiol. 31:13151317.
3. Baselski, V. S.,, R. A. Medina, and, C. D. Parker. 1979. In vivo and in vitro characterization of virulence-deficient mutants of Vibrio cholerae. Infect. Immun. 24:111116.
4. Baselski, V. S.,, R. A. Medina, and, C. D. Parker. 1978. Survival and multiplication of Vibrio cholerae in the upper bowel of infant mice. Infect. Immun. 22:435440.
5. Bik, E. M.,, A. E. Bunschoten,, R. D. Gouw, and, F. Mooi. 1995. Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis. EMBO J. 14:209216.
6. Boyd, E. F., and, M. K. Waldor. 2002. Evolutionary and functional analyses of variants of the toxin-coregulated pilus protein TcpA from toxigenic Vibrio cholerae non-O1/non-O139 serogroup isolates. Microbiology 148:16551666.
7. Cholera Working Group, ICDDRB. 1993. Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae O139 synonym Bengal. Lancet 342:387390.
8. Chongsa-nguan, M.,, W. Chaicumpa,, P. Moolasart,, P. Kandhasingha,, T. Shimada,, H. Kurazono, and, Y. Takeda. 1993. Vibrio cholerae O139 Bengal in Bangkok. Lancet 342:430431.
9. Dalsgaard, A.,, M. J. Albert,, D. N. Taylor,, T. Shimada,, R. Meza,, O. Serichantalergs, and, P. Echeverria. 1995. Characterization of Vibrio cholerae non-O1 serogroup obtained from an outbreak of diarrhea in Lima, Peru. J. Clin. Microbiol. 33:27152722.
10. Davis, B. M.,, H. H. Kimsey,, W. Chang, and, M. K. Waldor. 1999. The Vibrio cholerae O139 Calcutta bacteriophage CTXΦ is infectious and encodes a novel repressor. J. Bacteriol. 181:67796787.
11. Davis, B. M.,, H. H. Kimsey,, A. V. Kane, and, M. K. Waldor. 2002. A satellite phage-encoded antirepressor induces repressor aggregation and cholera toxin gene transfer. EMBO J. 21:42404249.
12. DiRita, V. J. 1992. Co-ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol. Microbiol. 6:451458.
13. Duffy, J. 1971. The history of Asiatic cholera in the United States. Bull. NY Acad. Med. 47:11521168.
14. Dziejman, M.,, E. Balon,, D. Boyd,, C. M. Fraser,, J. F. Heidelberg, and, J. J. Mekalanos. 2002. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc. Natl. Acad. Sci. USA 99:15561561.
15. Faruque, S. M.,, M. J. Albert, and, J. J. Mekalanos. 1998a. Epidemiology, genetics and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62:13011314.
16. Faruque, S. M.,, K. M. Ahmed,, A. R. M. A. Alim,, A. K. Siddique, and, M. J. Albert. 1997a. Emergence of a new clone of toxigenic Vibrio cholerae O1 biotype El Tor displacing V. cholerae O139 Bengal in Bangladesh. J. Clin. Microbiol. 35:624630.
17. Faruque, S. M.,, K. M. Ahmed,, A. K. Siddique,, K. Zaman,, A. R. M. A. Alim, and, M. J. Albert. 1997b. Molecular analysis of toxigenic Vibrio cholerae O139 Bengal strains isolated in Bangladesh between 1993 and 1996: evidence for emergence of a new clone of the Bengal vibrios. J. Clin. Microbiol. 35:22992306.
18. Faruque, S. M., and, M. J. Albert. 1992. Genetic relation between Vibrio cholerae O1 strains in Ecuador and Bangladesh. Lancet 339:740741.
19. Faruque, S. M.,, A. R. M. A. Alim,, S. K. Roy,, F. Khan,, G. B. Nair,, R. B. Sack, and, M. J. Albert. 1994. Molecular analysis of rRNA and cholera toxin genes carried by the new epidemic strain of toxigenic Vibrio cholerae O139 synonym Bengal. J. Clin. Microbiol. 32:10501053.
20. Faruque, S. M.,, Asadulghani, A. R., M. A. Alim,, M. J. Albert,, K. M. N. Islam, and, J. J. Mekalanos. 1998b. Induction of the lysogenic phage encoding cholera toxin in naturally occurring strains of toxigenic Vibrio cholerae O1 and O139. Infect. Immun. 66:37523757.
21. Faruque, S. M.,, M. Asadulghani. Kamruzzaman,, R. K. Nandi,, A. N. Ghosh,, G. B. Nair,, J. J. Mekalanos, and, D. A. Sack. 2002. RS1 element of Vibrio cholerae can propagate horizontally as a filamentous phage exploiting the morphogenesis genes of CTXΦ. Infect. Immun. 70:163170.
22. Faruque, S. M.,, Asadulghani, M., N. Saha,, A. R. M. A. Alim,, M. J. Albert,, K. M. N. Islam, and, J. J. Mekalanos. 1998c. Analysis of clinical and environmental strains of nontoxigenic Vibrio cholerae for susceptibility to CTXΦ: molecular basis for origination of new strains with epidemic potential. Infect. Immun. 66:58195825.
23. Faruque, S. M.,, Asadulghani,, J. Zhu,, M. Kamruzzaman, and, J. J. Mekalanos. 2003a. Examination of diverse toxin-coregulated pilus-positive Vibrio cholerae strains fails to demonstrate evidence for Vibrio pathogenicity island phage. Infect. Immun. 71:29932999.
24. Faruque, S. M.,, N. Chowdhury,, M. Kamruzzaman,, Q. S. Ahmad,, A. S. G. Faruque,, M. A. Salam,, T. Ramamurthy,, G. B. Nair,, A. Weintraub, and, D. A. Sack. 2003b. Reemergence of epidemic Vibrio cholerae O139, Bangladesh. Emerg. Infect. Dis. 9:11161122.
25. Faruque, S. M.,, N. Chowdhury,, M. Kamruzzaman,, M. Dziejman,, M. H. Rahman,, D. A. Sack,, G. B. Nair, and, J. J. Mekalanos. 2004a. Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc. Natl. Acad. Sci. USA 101:21232128.
26. Faruque, S. M.,, M. J. Islam,, Q. S. Ahmad,, A. S. G. Faruque,, D. A. Sack,, G. B. Nair, and, J. J. Mekalanos. 2005a. Self-limiting nature of seasonal cholera epidemics: role of host-mediated amplification of phage. Proc. Natl. Acad. Sci. USA 102:61196124.
27. Faruque, S. M.,, M. Kamruzzaman,, Asadulghani, D., A. Sack,, J. J. Mekalanos, and, G. B. Nair. 2003c. CTXΦ-independent production of RS1 satellite phage by Vibrio cholerae. Proc. Natl. Acad. Sci. USA 100:12801285.
28. Faruque, S. M.,, M. Kamruzzaman,, I. M. Meraj,, N. Chowdhury,, G. B. Nair,, R. B. Sack,, R. R. Colwell, and, D. A. Sack. 2003d. Pathogenic potential of environmental Vibrio cholerae strains carrying genetic variants of the toxin-coregulated pilus pathogenicity island. Infect. Immun. 71:10201025.
29. Faruque, S. M., and, J. J. Mekalanos. 2003e. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends. Microbiol. 11:505510.
30. Faruque, S. M.,, G. B. Nair, and, J. J. Mekalanos. 2004b. Genetics of stress-adaptation and virulence in toxigenic Vibrio cholerae. DNA Cell Biol. 23:723741.
31. Faruque, S. M.,, I. B. Nase,, M. J. Islam,, A. S. G. Faruque,, A. N. Ghosh,, G. B. Nair,, D. A. Sack, and, J. J. Mekalanos. 2005b. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc. Natl. Acad. Sci. USA 102:17021707.
32. Faruque, S. M.,, M. N. Saha,, Asadulghani,, K. Bag,, R. K. Bhadra,, S. K. Bhattacharya,, R. B. Sack,, Y. Takeda, and, G. B. Nair. 2000a. Genomic diversity among Vibrio cholerae O139 strains isolated in Bangladesh and India between 1992 and 1998. FEMS Microbiol. Lett. 184:279284.
33. Faruque, S. M.,, M. N. Saha,, Asadulghani, D., A. Sack,, R. B. Sack,, Y. Takeda, and, G. B. Nair. 2000b. The O139 serogroup of Vibrio cholerae comprises diverse clones of epidemic and nonepidemic strains derived from multiple V. cholerae O1 and non-O1 progenitors. J. Infect. Dis. 182:11611168.
34. Finkelstein, R. A.,, M. L. Vasil, and, R. K. Holmes. 1974. Studies on toxinogenesis in Vibrio cholerae. I. Isolation of mutants with altered toxinogenicity. J. Infect. Dis. 129:117123.
35. Franzon, V. L.,, A. Baker, and, P. A. Manning. 1993. Nucleotide sequence encoding the mannose-fucose-resistant hemagglutinin (MFRHA) of Vibrio cholerae O1 and construction of a mutant. Infect. Immun. 61:30323037.
36. Fullner, K. J., and, J. J. Mekalanos. 1999. Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae. Infect. Immun. 67:13931404.
37. Glass, R. I.,, I. Huq,, A. R. M. A. Alim, and, M. Yunus. 1980. Emergence of multiple antibiotic-resistant Vibrio cholerae in Bangladesh. Infect. Dis. 142:939942.
38. Glass, R. I.,, M. I. Huq,, J. V. Lee,, E. J. Threlfall,, M. R. Khan,, A. R. M. A. Alim,, B. Rowe, and, R. J. Gross. 1983. Plasmid-borne multiple drug resistance in Vibrio cholerae serogroup O1, biotype El Tor: evidence of a point-source outbreak in Bangladesh. J. Infect. Dis. 147:204209.
39. Häse, C. C., and, J. J. Mekalanos. 1998. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 95:730734.
40. Heidelberg, J. F.,, J. A. Eisen,, W. C. Nelson,, R. A. Clayton,, M. L. Gwinn,, R. J. Dodson,, D. H. Haft,, E. K. Hickey,, J. D. Peterson,, L. Umayam,, S. R. Gill,, K. E. Nelson,, T. D. Read,, H. Tettelin,, D. Richardson,, M. D. Ermolaeva,, J. Vamathevan,, S. Bass,, H. Qin,, I. Dragoi,, P. Sellers,, L. McDonald,, T. Utterback,, R. D. Fleishman,, W. C. Nierman,, O. White,, S. L. Salzberg,, H. O. Smith,, R. R. Colwell,, J. J. Mekalanos,, J. C. Ventor, and, C. M. Frasier. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477483.
41. Herrington, D. A,, R. H. Hall,, G. Losonsky,, J. J. Mekalanos,, R. K. Taylor, and, M. M. Levine. 1998. Toxin, toxin-coregulated pili and ToxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168:14871492.
42. Hochhut, B.,, Y. Lotfi,, D. Mazel,, S. M. Faruque,, R. Woodgate, and, M. K. Waldor. 2002. Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1 SXT constins. Antimicrob. Agents Chemother. 45:29913000.
43. Holmes, R. K.,, M. L. Vasil, and, R. A. Finkelstein. 1975. Studies on toxino-genesis in Vibrio cholerae. III. Characterization of nontoxigenic mutants in vitro and in experimental animals. J. Clin. Invest. 55:551556.
44. Janda, J. M.,, C. Powers,, R. G. Bryant, and, S. L. Abbott. 1988. Current perspective on the epidemiology and pathogenesis of clinically significant Vibrio spp. Clin. Microbiol. Rev. 1:245267.
45. Jermyn, W. S., and, E. F. Boyd. 2002. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology 148:36813693.
46. Jesudason, M. V., and, R. Saaya. 1997. Resistance of Vibrio cholerae O1 to nalidixic acid. Indian J. Med. Res. 105:153154.
47. Jonson, G.,, J. Holmgren, and, A. M. Svennerholm. 1991. Identification of a mannose-binding pilus on V. cholerae El Tor. Microb. Pathog. 11:433441.
48. Jonson, G.,, M. Lebens, and, J. Holmgren. 1994. Cloning and sequencing of Vibrio cholerae mannose-sensitive hemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes. Mol. Microbiol. 13:109108.
49. Kaper, J. B.,, H. B. Bradford,, N. C. Roberts, and, S. Falkow. 1982. Molecular epidemiology of Vibrio cholerae in the U.S. Gulf Coast. J. Clin. Microbiol. 16:129134.
50. Kaper, J. B.,, J. G. Morris, Jr., and, M. M. Levine. Clin. Microbiol. Rev. 8:4886.
51. Karaolis, D. K.,, R. Lan, and, P. R. Reeves. 1995. The sixth and seventh cholera pandemics are due to independent clones separately derived from environmental, nontoxigenic, non-O1 Vibrio cholerae. J. Bacteriol. 177:31913198.
52. Karaolis, D. K.,, S. Somara,, D. R. Maneval, Jr.,, J. A. Johnson, and, J. B. Kaper. 1999. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature 399:375379.
53. Khan, M. U.,, A. R. Samadi,, M. I. Huq, and, W. B. Greenough. 1986. Reappearance of classical Vibrio cholerae in Bangladesh, pp. 312. In Advances in Research on Cholera and Related Diarrheas, vol. 3. KTK Scientific Publishers, Tokyo, Japan.
54. Khan, M. U.,, M. Shahidullah,, M. S. Haque, and, W. U. Ahmed. 1984. Presence of vibrios in surface water and their relation with cholera in a community. Trop. Geogr. Med. 36:335340.
55. Kimsey, H. H., and, M. K. Waldor. 1998. CTXΦ immunity: application in the development of cholera vaccines. Proc. Natl. Acad. Sci. USA 95:70357039.
56. Kovach, M. E.,, M. D. Shaffer, and, K. M. Peterson. 1996. A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae. Microbiology 142:21652174.
57. Lin, W.,, K. J. Fullner,, R. Clayton,, J. A. Sexton,, M. B. Rogers,, K. E. Calia,, S. B. Calderwood,, C. Fraser, and, J. J. Mekalanos. 1999. Identification of a vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc. Natl. Acad. Sci. USA 96:10711076.
58. Materu, S. F.,, O. E. Lema,, H. M. Mukunza,, C. G. Adhiambo, and, J. Y. Carter. 1997. Antibiotic resistance pattern of Vibrio cholerae and Shigella causing diarrhoea outbreaks in the eastern Africa region: 1994-1996. East Afr. Med. J. 74:193197.
59. Mazel, D.,, B. Dychinco,, V. A. Webb, and, J. Davies. 1998. A distinctive class of integron in the Vibrio cholerae genome. Science 280:605608.
60. Mekalanos, J. J.,, R. J. Collier, and, W. R. Roming. 1978. Affinity filters, a new approach to the isolation of tox mutants of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 75:941945.
61. Mekalanos, J. J. 1985. Cholera toxin: genetic analysis, regulation and role in pathogenesis. Curr. Top. Microbiol. Immunol. 118:97118.
62. Mekalanos, J. J. 1983. Duplication and amplification of toxin genes in Vibrio cholerae. Cell. 35:253263.
63. Miwatani, T., and, Y. Takeda. 1975. Vibrio parahaemolyticus epidemiology ecology and biology. pp. 2224. In T. Miwatani,, Y. Takeda (ed.), Vibrio Parahaemolyticus: A Causative Bacterium of Seafood Poisoning. Saiko, Tokyo, Japan.
64. Morris, J. G., Jr. 1990. Non-O group 1 Vibrio cholerae: a look at the epidemiology of an occasional pathogen. Epidemiol. Rev. 12:179191.
65. Mukhopadhyay, A. K.,, S. Chakraborty,, Y. Takeda,, G. B. Nair, and, D. E. Berg. 2001. Characterization of VPI pathogenicity island and CTXphi prophage in environmental strains of Vibrio cholerae. J. Bacteriol. 183:47374746.
66. Nakasone, N.,, M. Iwanaga, and, R. Eeckels. 1987. Characterization of Vibrio cholerae O1 recently isolated in Bangladesh. Trans. R. Soc. Trop. Med. Hyg. 81:876878.
67. Nandi, B.,, R. K. Nandy,, A. C. Vicente, and, A. C. Ghose. 2000. Molecular characterization of a new variant of toxin-coregulated pilus protein (TcpA) in a toxigenic non-O1/non-O139 strain of Vibrio cholerae. Infect. Immun. 68:948952.
68. Novais, R. C.,, A. Coelho,, C. A. Salles, and, A. C. Vicente. 1999. Toxin coregulated pilus cluster in non-O1, non-toxigenic Vibrio cholerae: evidence of a third allele of pilin gene. FEMS Microbiol. Lett. 171:4955.
69. O’Toole, G.,, H. B. Kaplan, and, R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:4979.
70. Ogg, J. E.,, T. L. Timme, and, M. M. Alemohammad. 1981. General transduction in Vibrio cholerae. Infect. Immun. 31:737741.
71. Parsot, C., and, J. J. Mekalanos. 1990. Expression of ToxR, the transcriptional activator of the virulence factors in Vibrio cholerae, is modulated by the heat shock response. Proc. Natl. Acad. Sci. USA 87:98989902.
72. Peterson, K. M., and, J. J. Mekalanos. 1998. Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization. Infect. Immun. 56:28222829.
73. Ramamurthy, T.,, M. J. Albert,, A. Huq,, R. R. Colwell,, Y. Takeda,, T. Takeda,, T. Shimada,, B. K. Mandal, and, G. B. Nair. 1994. Vibrio mimicus with multiple toxin types isolated from human and environmental sources. J. Med. Microbiol. 40:194196.
74. Ramamurthy, T.,, P. K. Bag,, A. Pal,, S. K. Bhattacharya,, M. K. Bhattacharya,, T. Shimada,, T. Takeda,, T. Karasawa,, H. Kurazono, and, Y. Takeda. 1993a. Virulence patterns of Vibrio cholerae non-O1 strains isolated from hospitalized patients with acute diarrhea in Calcutta, India. J. Med. Microbiol. 39:310317.
75. Ramamurthy, T.,, S. Garg,, R. Sharma,, S. K. Bhattacharya,, G. B. Nair,, T. Shimada,, T. Takeda,, T. Karasawa,, H. Kurazano,, A. Pal, and, Y. Takeda. 1993b. Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. Lancet. 341:703704.
76. Reguera, G., and, R. Kolter. 2005. Virulence and the environment: a novel role for Vibrio cholerae toxin-coregulated pili in biofilm formation on chitin. J. Bacteriol. 187:35513555.
77. Rudra, S.,, R. Mahajan,, M. Mathur,, K. Kathuria, and, V. Talwar. 1996. Cluster of cases of clinical cholera due to Vibrio cholerae O10 in East Delhi. Indian J. Med. Res. 103:7173.
78. Samadi, A. R.,, M. I. Huq,, N. Shahid,, M. U. Khan,, A. Eusof,, A. S. Rahman,, M. Yunus, and, A. S. Faruque. 1983. Classical Vibrio cholerae biotype displaces El Tor in Bangladesh. Lancet. 1:805807.
79. Sengupta, D. K.,, T. K. Sengupta, and, A. C. Ghose. 1992. Major outer membrane proteins of Vibrio cholerae and their role in induction of protective immunity through inhibition of intestinal colonization. Infect. Immun. 60:48484855.
80. Siddique, A. K.,, K. Zaman,, A. H. Baqui,, K. Akram,, P. Mutsuddy,, A. Eusof,, K. Haider,, S. Islam, and, R. B. Sack. 1992. Cholera epidemics in Bangladesh: 1985–1991. J. Diarrhoeal. Dis. Res. 10:7986.
81. Siddique, A. K.,, K. Zaman,, Y. Majumder,, Q. Islam,, I. Bashir,, P. Mutsuddy, and, A. Eusof. 1989. Simultaneous outbreaks of contrasting drug resistant classic and El Tor Vibrio cholerae O1 in Bangladesh. Lancet. 2:396.
82. Sigel, S. P., and, S. M. Payne. 1982. Effect of iron limitation on growth, siderophore production, and expression of outer membrane proteins of Vibrio cholerae. J. Bacteriol. 150:14855.
83. Skorupski, K., and, R. K. Taylor. 1997. Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli. Mol. Microbiol. 25:10031009.
84. Swerdlow, D. L., and, A. A. Ries. 1993. Vibrio cholerae non-O1—the eighth pandemic? Lancet 342:382383.
85. Tacket, C. O.,, F. Brenner, and, P. A. Blake. 1984. Clinical features and an epidemiological study of Vibrio vulnificus infections. J. Infect. Dis. 149:558561.
86. Trucksis, M.,, J. Michalski,, Y. K. Deng, and, J. B. Kaper. 1998. The Vibrio cholerae genome contains two unique circular chromosomes. Proc. Natl. Acad. Sci. USA 95:1446414469.
87. Wachsmuth, I. K.,, C. A. Bopp,, P. I. Fields, and, C. Carrillo. 1991. Difference between toxigenic Vibrio cholerae O1 from South America and US gulf coast [letter]. Lancet 337:10971098.
88. Wachsmuth, I. K.,, G. M. Evins,, P. I. Fields,, Ø. Olsvik,, T. Popovic,, C. A. Bopp,, J. G. Wells,, C. Carrillo, and, P. A. Blake. 1993. The molecular epidemiology of cholera in Latin America. J. Infect. Dis. 167:621626.
89. Wachsmuth, I. K.,, O. Olsvik,, G. M. Evins, and, T. Popovic. 1994. Molecular epidemiology of cholera, pp. 357370. In K. Wachsmuth,, P. A. Blake, and, O. Olsvik (ed.), Vibrio Cholerae and Cholera: Molecular to Global Perspectives. ASM Press, Washington D.C.
90. Waldor, M. K.,, R. Colwell, and, J. J. Mekalanos. 1994. The Vibrio cholerae 0139 serogroup antigen includes O-antigen capsule and lipopolysaccharide virulence determinants. Proc. Natl. Acad. Sci. USA 91:1138811392.
91. Waldor, M. K., and, J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous bacteriophage encoding cholera toxin. Science 272:19101914.
92. Waldor, M. K.,, E. J. Rubin,, G. D. N. Pearson,, H. Kimsey, and, J. J. Mekalanos. 1997. Regulation, replication, and integration functions of the Vibrio cholerae CTXΦ are encoded by regions RS2. Mol. Microbiol. 24:917926.
93. Watnick, P. I.,, K. J. Fullner, and, R. Kolter. 1999. A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181:36063609.
94. West, P. A. 1989. The human pathogenic vibrios—a public health update with environmental perspectives. Epidemiol. Inf. 103:134.
95. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler, and, J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:31293134.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error