Genetic Determinants Differences between Vibrio cholerae Biotypes

Authors
H. Mohammadi barzelighi 1
H. Mohammadi barzelighi 1
B. Bakhshi 2
M. Boustanshenas 3
1 Department of Bacteriology, Faculty of Medicine, Isfahan University of Medical sciences, Isfahan, IR Iran
2 Department of Bacteriology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, IR Iran
3 Antimicrobial Resistance Research Center, Iran University of Medical Sciences, Tehran, IR Iran
Abstract
Vibrio cholerae O1 are classified into two biotypes, classical and El Tor based on susceptibility to bacteriophages and some biochemical properties, each encoding a biotype-specific genetic determinants. Before 1961, most epidemics had been caused by the classical biotype. However, with the passage of time, the classical biotype missed from the scenario and the El Tor emerged as the major biotype causing the cholera in humans. The present cholera global pandemic is attributed to a change among seventh pandemic strains and emergence of V. cholerae O139, V. cholerae O1 El Tor hybrid, and V. cholera O1 El Tor with altered cholera toxin subunit B. The V. cholerae biotypes are not only different in phenotype but also human infections caused by them are different clinically. Infection with classical V. cholerae O1 more frequently produces severe infection than does El Tor, suggesting that the genetic and phenotypic differences between the two biotypes may also be reflected in their pathogenic potential. Considering the recent emergence of “hybrid biotype” and “El Tor variant” in different areas and in our country, we reviewed differences in genetic structure of V. cholerae biotypes.

Keywords

  1. Pourshafie MR, grimont F, saifi M, grimont PA. Molecular epidemiological study of Vibrio cholerae isolates from infected patients in Teheran, Iran. J Med Microbiol. 2000; 49(12):1085-90.

  2. Kaper J, Morris JG, Levine M. Cholera. Clin Microbiol Rev. 1995; 8(1): 48-86.

  3. Sakazaki R. Classification and characteristics of vibrios. Public health papers. 1970;40:33.

  4. Faruque SM, Sack DA, Sack RB, Colwell RR, Takeda Y, Nair GB. Emergence and evolution of Vibrio cholerae O139. Proc Natl Acad Sci. 2003; 100(3):1304-9.

  5. Faruque SM, Albert MJ, Mekalanos JJ. Epidemiology, Genetics and Ecology of Toxigenic Vibriocholerae. Microbiol Mol Biol Rev. 1998; 62(4):1301-14.

  6. Bakhshi B, Boustanshenas M, Mahmoudi‐aznaveh A. Emergence of Vibrio cholerae O1 classical biotype in 2012 in Iran. Lett Appl Microbiol. 2014;58(2):145-9.

  7. Ramamurthy T, Garg S, Sharma R, Bhattacharya S, Balakrish Nair G, Shimada T, et al. Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. The Lancet 1993; 341(8846):703-4.

  8. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY, Haley BJ, et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci. 2009; 106(36):15442-7.

  9. Raychoudhuri A, Mukhopadhyay A, Ramamurthy T, Nandy R, Takeda Y, Nair GB. Biotyping of Vibrio cholerae O1: time to redefine the scheme. Indian J Med Res. 2008; 128(6):695-8.

  10. Gangarosa E, Saghari H, Emile J, Siadat H. Detection of Vibrio cholerae biotype El Tor by purging. Bull World Health Organ. 1966; 34(3):363-9.

  11. Comstock LE, Johnson JA, Michalski JM, Morris Jr JG, Kaper JB. Cloning and sequence of a region encoding a surface polysaccharide of Vibrio cholerae O139 and characterization of the insertion site in the chromosome of Vibrio cholerae O1. Mol Microbiol. 1996; 19(4):815-26.

  12. Calia KE, Waldor MK, Calderwood SB. Use of representational difference analysis to identify genomic differences between pathogenic strains of Vibrio cholerae. Infect Immun.1998; 66(2):849-52.

  13. Johnson JA, Salles CA, Panigrahi P, Albert MJ, Wright AC, Johnson RJ, et al. Vibrio cholerae O139 synonym bengal is closely related to Vibrio cholerae El Tor but has important differences. Infect Immun. 1994; 62(5):2108-10.

  14. Barua D. History of cholera. In: Cholera: Springer; 1992. p. 1-36.

  15. Sen A, Ghosh AN. New Vibrio cholerae O1 biotype ElTor bacteriophages. Virol J. 2005; 2(1):28.

  16. DiRita VJ, Neely M, Taylor RK, Bruss PM. Differential expression of the ToxR regulon in classical and E1 Tor biotypes of Vibrio cholerae is due to biotype-specific control over toxT expression. Proc Natl Acad Sci. 1996; 93(15):7991-5.

  17. Morita M, Ohnishi M, Arakawa E, Yamamoto S, Nair GB, Matsushita S, et al. Emergence and genetic diversity of El Tor Vibrio cholerae O1 that possess classical biotype ctxB among travel-associated cases of cholera in Japan. J Med Microbiol. 2010; 59(6):708-12.

  18. Manning PA. The tcp gene cluster of Vibrio cholerae. Gene. 1997; 192(1):63-70.

  19. Bakhshi B, Pourshafie M, Navabakbar F, Tavakoli A. Genomic organisation of the CTX element among toxigenic Vibrio cholerae isolates. Clin Microbiol Infect. 2008; 14(6):562-8.

  20. Safa A, Bhuyian N, Nusrin S, Ansaruzzaman M, Alam M, Hamabata T, et al. Genetic characteristics of Matlab variants of Vibrio cholerae O1 that are hybrids between classical and El Tor biotypes. J Med Microbiol. 2006; 55(11):1563-9.

  21. Murley YM, Carroll PA, Skorupski K, Taylor RK, Calderwood SB. Differential Transcription of the tcpPHOperon Confers Biotype-Specific Control of the Vibrio cholerae ToxR Virulence Regulon. Infect Immun. 1999; 67(10):5117-23.

  22. Colwell RR, Spira WM. The ecology of Vibrio cholerae. In: Cholera: Springer; 1992. p. 107-27.

  23. Herrington DA, Hall RH, Losonsky G, Mekalanos JJ, Taylor R, Levine MM. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J Exp Med 1988; 168(4):1487-92.

  24. Kovach ME, Shaffer MD, Peterson KM. A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae. Microbiology. 1996; 142(Pt 8): 2165-74.

  25. Faruque SM, Mekalanos JJ. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol. 2003; 11(11): 505-10.

  26. Karaolis DK, Lan R, Kaper JB, Reeves PR. Comparison of Vibrio cholerae Pathogenicity Islands in Sixth and Seventh Pandemic Strains. Infect Immun. 2001; 69(3):1947-52.

  27. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci. 1987; 84(9): 2833-7.

  28. Faruque SM, Asadulghani, Alim AR, Albert MJ, Islam KM, Mekalanos JJ. Induction of the lysogenic phage encoding cholera toxin in naturally occurring strains of toxigenic Vibrio cholerae O1 and O139. Infect Immun. 1998; 66(8): 3752-7.

  29. Albert M, Ansaruzzaman M, Bardhan P, Faruque A, Faruque S, Islam M, et al. Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae 0139 synonym Bengal. Lancet. 1993; 342(8868): 387-90.

  30. 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.1999; 96(7): 4028-33.

  31. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science. 1996; 272(5270):1910-4.

  32. Pearson GD, Woods A, Chiang SL, Mekalanos JJ. CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor. Proc National Acad Sci USA. 1993; 90(8): 3750-4.

  33. Waldor MK, Rubin EJ, Pearson GD, Kimsey H, Mekalanos JJ. Regulation, replication and integration functions of the Vibrio cholerae CTXΦ are encoded by region RS2. Mol Microbiol. 1997; 24(5):917-26.

  34. Kimsey HH, Waldor MK. CTXφ immunity: application in the development of cholera vaccines. Proc Natl Acad Sci. 1998; 95(12): 7035-9.

  35. Davis BM, Moyer KE, Boyd EF, Waldor MK. CTX prophages in classical biotype Vibrio cholerae: functional phage genes but dysfunctional phage genomes. J Bacteriol. 2000; 182(24): 6992-8.

  36. Lin W, Fullner KJ, Clayton R, Sexton JA, Rogers MB, Calia KE, et al. Identification of a Vibrio cholerae RTX toxin gene cluster that is tightly linked to the cholera toxin prophage. Proc Natl Acad Sci. 1999; 96(3):1071-6.

  37. van Heyningen S. The subunits of cholera toxin: structure, stoichiometry and function. J Infect Dis. 1976; 133(1):5-13.

  38. Nair GB, Qadri F, Holmgren J, Svennerholm A-M, Safa A, Bhuiyan NA, et al. Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol. 2006; 44(11):4211-3.

  39. Safa A, Sultana J, Dac Cam P, Mwansa JC, KONG YCR. Vibrio cholerae O1 hybrid El Tor strains, Asia and Africa. Emerg Infect Dis. 2008; 14(6):987-8.

  40. Nguyen BM, Lee JH, Cuong NT, Choi SY, Hien NT, Anh DD, et al. Cholera outbreaks caused by an altered Vibrio cholerae O1 El Tor biotype strain producing classical cholera toxin B in Vietnam in 2007 to 2008. J Clin Microbiol. 2009; 47(5):1568-71.

  41. Raychoudhuri A, Patra T, Ghosh K, Ramamurthy T, Nandy RK, Takeda Y, et al. Classical ctxB in Vibrio cholerae O1, Kolkata, India. Emerg Infect Dis. 2009; 15(1):131.

  42. Hammer BK, Bassler BL. Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J Bacteriol. 2009; 191(1):169-77.

  43. Siddique A, Nair G, Alam M, Sack D, Huq A, Nizam A, et al. El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect. 2010; 138(3):347-52.

  44. Ghosh-Banerjee J, Senoh M, Takahashi T, Hamabata T, Barman S, Koley H, et al. Cholera toxin production by the El Tor variant of Vibrio cholerae O1 compared to prototype El Tor and classical biotypes. J Clin Microbiol. 2010; 48(11):4283-6.

  45. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci. 1998; 95(6):3134-9.

  46. Karaolis DK, Somara S, Maneval DR, Johnson JA, Kaper JB. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature. 1999; 399(6734): 375-9.

  47. Mohammadi-Barzelighi H, Bakhshi B, Lari AR, Pourshafie MR. Characterization of pathogenicity island prophage in clinical and environmental strains of Vibrio cholerae. J Med Microbiol. 2011; 60(12):1742-9.

  48. Carroll PA, Tashima KT, Rogers MB, DiRita VJ, Calderwood SB. Phase variation in tcpH modulates expression of the ToxR regulon in Vibrio cholerae. Mol Microbiol. 1997;2 5(6):1099-111.

  49. DiRita VJ. Co‐ordinate expression of virulence genes by ToxR in Vibrio cholerae. Mol Microbiol. 1992; 6(4):451-8.

  50. DiRita VJ, Parsot C, Jander G, Mekalanos JJ. Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci. 1991; 88(12):5403-7.

  51. Häse CC, Mekalanos JJ. TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci. 1998; 95(2):730-4.

  52. Boyd EF, Waldor MK. Evolutionary and functional analyses of variants of the toxin-coregulated pilus protein TcpA from toxigenic Vibrio cholerae non-O1/non-O139 serogroup isolates. Microbiology. 2002; 148(6):1655-66.

  53. Rhine JA, Taylor RK. TcpA pilin sequences and colonization requirements for O1 and O139 Vibrio cholerae. Mol Microbiol. 1994; 13(6):1013-20.

  54. Alam M, Islam MT, Rashed SM, Johura F-t, Bhuiyan NA, Delgado G, et al. Vibrio cholerae classical biotype strains reveal distinct signatures in Mexico. J Clin Microbiol. 2012;50(7):2212-6.

  55. Dashtbani‐Roozbehani A, Bakhshi B, Katouli M, Pourshafie M. Comparative sequence analysis of recA gene among Vibrio cholerae isolates from Iran with globally reported sequences. Lett Appl Microbiol. 2011; 53(3):313-23.

  56. Sun D, Seyer J, Kovari I, Sumrada R, Taylor R. Localization of protective epitopes within the pilin subunit of the Vibrio cholerae toxin-coregulated pilus. Infect Immun. 1991; 59(1):114-18.

  57. Iredell JR, Manning PA. Translocation failure in a type-4 pilin operon: rfb and tcpT mutants in Vibrio cholerae. Gene. 1997; 192(1):71-7.

  58. Ogierman MA, Zabihi S, Mourtzios L, Manning PA. Genetic organization and sequence of the promoter-distal region of the tcp gene cluster ofVibrio cholerae. Gene. 1993; 126(1):51-60.

  59. Jermyn WS, Boyd EF. Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology. 2002; 148(Pt 11):3681-93.

  60. Thelin KH, Taylor RK. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun. 1996; 64(7):2853-6.

  61. Rader AE, Murphy JR. Nucleotide sequences and comparison of the hemolysin determinants of Vibrio cholerae El Tor RV79 (Hly+) and RV79 (Hly-) and classical 569B (Hly-). Infect Immun. 1988; 56(6):1414-9.

  62. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci. 2002; 99(3):1556-61.

  63. Beyhan S, Tischler AD, Camilli A, Yildiz FH. Differences in gene expression between the classical and El Tor biotypes of Vibrio cholerae O1. Infect Immun. 2006; 74(6):3633-42.

  64. Son MS, Megli CJ, Kovacikova G, Qadri F, Taylor RK. Characterization of Vibrio cholerae O1 El Tor biotype variant clinical isolates from Bangladesh and Haiti, including a molecular genetic analysis of virulence genes. J Clin Microbiol. 2011; 49(11):3739-49.

  65. Krukonis ES, Yu RR, DiRita VJ. The Vibrio cholerae ToxR/TcpP/ToxT virulence cascade: distinct roles for two membrane‐localized transcriptional activators on a single promoter. Mol Microbiol. 2000; 38(1):67-84.

  66. Rosa RY, DiRita VJ. Analysis of an autoregulatory loop controlling ToxT, cholera toxin, and toxin-coregulated pilus production inVibrio cholerae. J Bacteriol. 1999; 181(8):2584-92.

  67. Kovacikova G, Skorupski K. Overlapping binding sites for the virulence gene regulators AphA, AphB and cAMP‐CRP at the Vibrio cholerae tcpPH promoter. Mol Microbiol. 2001; 41(2):393-407.

  68. Miller VL, Mekalanos JJ. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988; 170(6):2575-83.

  69. Kovacikova G, Skorupski K. Binding site requirements of the virulence gene regulator AphB: differential affinities for the Vibrio cholerae classical and El Tor tcpPH promoters. Mol Microbiol. 2002; 44(2):533-47.

  70. Murley YM, Behari J, Griffin R, Calderwood SB. Classical and El Tor Biotypes of Vibrio cholerae Differ in Timing of Transcription of tcpPH during Growth in Inducing Conditions. Infect Immun. 2000; 68(5): 3010-4.