Skip to main content
SpringerLink
Log in

Vibrio cholerae

  • Chapter
  • First Online:
Molecular Typing in Bacterial Infections, Volume II

  • 439 Accesses

Abstract

Cholera caused by toxigenic Vibrio cholerae is a major public health problem in many developing countries, where outbreaks and sporadic infections occur at regular intervals. WHO has registered 499,447 cases, including 2990 deaths with case fatality rate of 0.6% in 2018 [1]. The disease is characterized by profuse watery diarrhea that rapidly leads to dehydration, and death occurs in 50–70% of untreated patients.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. World Health Organization (2019) Cholera 2018. Weekly Epidemiol Rec 94:561–580

    Google Scholar 

  2. Sack DA, Sack RB, Nair GB, Siddique AK (2004) Cholera. Lancet 363:223–233

    Article  CAS  PubMed  Google Scholar 

  3. Pollitzer R (1959) Cholera. World Health Organization, Geneva

    Google Scholar 

  4. Chattopadhyay DJ, Sarkar BL, Ansari MQ, Chakrabarti BK, Roy MK, Ghosh AN, Pal SC (1993) New phage typing scheme for Vibrio cholerae O1 biotype El Tor strains. J Clin Microbiol 31:1579–1585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chakrabarti AK, Ghosh AN, Nair GB, Niyogi SK, Bhattacharya SK, Sarkar BL (2000) Development and evaluation of a phage typing scheme for Vibrio cholerae O139. J Clin Microbiol 38:44–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Makino S, Kurazono T, Okuyama Y, Shimada T, Okada Y, Sasakawa C (1995) Diversity of DNA sequences among Vibrio cholerae O139 Bengal detected by PCR-based DNA fingerprinting. FEMS Microbiol Lett 126:43–48

    Article  CAS  PubMed  Google Scholar 

  7. Radu S, Ho YK, Lihan S, Yuherman RG, Yasin RM, Khair J, Elhadi N (1999) Molecular characterization of Vibrio cholerae O1 and non-O1 from human and environmental sources in Malaysia. Epidemiol Infect 123:225–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Leal NC, Sobreira M, Leal-Balbino TC, de Almeida AM, de Silva MJ, Mello DM, Seki LM, Hofer E (2004) Evaluation of a RAPD-based typing scheme in a molecular epidemiology study of Vibrio cholerae O1, Brazil. J Appl Microbiol 96:447–454

    Article  CAS  PubMed  Google Scholar 

  9. Pourshafie MR, Bakhshi B, Ranjbar R, Sedaghat M, Sadeghifard N, Zaemi Yazdi J, Parzadeh M, Raesi J (2007) Dissemination of a single Vibrio cholerae clone in cholera outbreaks during 2005 in Iran. J Med Microbiol 56:1615–1619

    Article  CAS  PubMed  Google Scholar 

  10. Opintan JA, Newman MJ, Nsiah-Poodoh OA, Okeke IN (2008) Vibrio cholerae O1 from Accra, Ghana carrying a class 2 integron and the SXT element. J Antimicrob Chemother 62:929–933

    Google Scholar 

  11. Jiang SC, Matte M, Matte G, Huq A, Colwell RR (2000) Genetic diversity of clinical and environmental isolates of Vibrio cholerae determined by amplified fragment length polymorphism fingerprinting. Appl Environ Microbiol 66:148–153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Castañeda NC, Pichel M, Orman B, Binsztein N, Roy PH, Centrón D (2005) Genetic characterization of Vibrio cholerae isolates from Argentina by V. cholerae repeated sequences-polymerase chain reaction. Diagn Microbiol Infect Dis 53:175–183

    Article  PubMed  Google Scholar 

  13. Rivera IG, Chowdhury MA, Huq A, Jacobs D, Martins MT, Colwell RR (1995) Enterobacterial repetitive intergenic consensus sequences and the PCR to generate fingerprints of genomic DNAs from Vibrio cholerae O1, O139, and non-O1 strains. Appl Environ Microbiol 61:2898–2904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zo YG, Rivera IN, Russek-Cohen E, Islam MS, Siddique AK, Yunus M, Sack RB, Huq A, Colwell RR (2002) Genomic profiles of clinical and environmental isolates of Vibrio cholerae O1 in cholera-endemic areas of Bangladesh. Proc Natl Acad Sci U S A 99:12409–12414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Shangkuan YH, Tsao CM, Lin HC (1997) Comparison of Vibrio cholerae O1 isolates by polymerase chain reaction fingerprinting and ribotyping. J Med Microbiol 46:941–948

    Article  CAS  PubMed  Google Scholar 

  16. Labbate M, Boucher Y, Joss MJ, Michael CA, Gillings MR, Stokes HW (2007) Use of chromosomal integron arrays as a phylogenetic typing system for Vibrio cholerae pandemic strains. Microbiology 153:1488–1498

    Article  CAS  PubMed  Google Scholar 

  17. Faruque SM, Siddique AK, Saha MN, Asadulghani RMM, Zaman K, Albert MJ, Sack DA, Sack RB (1999) Molecular characterization of a new ribotype of Vibrio cholerae O139 Bengal associated with an outbreak of cholera in Bangladesh. J Clin Microbiol 37:1313–1318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sarkar A, Morita D, Ghosh A, Chowdhury G, Mukhopadhyay AK, Okamoto K, Ramamurthy T (2019) Altered integrative and conjugative elements (ICEs) in recent Vibrio cholerae O1 isolated from cholera cases, Kolkata, India. Front Microbiol 10:2072

    Article  PubMed  PubMed Central  Google Scholar 

  19. McDonald ND, Regmi A, Morreale DP, Borowski JD, Boyd EF (2019) CRISPR-Cas systems are present predominantly on mobile genetic elements in Vibrio species. BMC Genomics 20(1):105

    Article  PubMed  PubMed Central  Google Scholar 

  20. Scrascia M, Pugliese N, Maimone F, Mohamud KA, Grimont PA, Materu SF, Pazzani C (2009) Clonal relationship among Vibrio cholerae O1 El Tor strains isolated in Somalia. Int J Med Microbiol 299:203–207

    Article  CAS  PubMed  Google Scholar 

  21. Folster JP, Katz L, McCullough A, Parsons MB, Knipe K, Sammons SA, Boncy J, Tarr CL, Whichard JM (2014) Multidrug-resistant IncA/C plasmid in Vibrio cholerae from Haiti. Emerg Infect Dis 20:1951–1953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wang R, Yu D, Zhu L, Li J, Yue J, Kan B (2015) IncA/C plasmids harboured in serious multidrug-resistant Vibrio cholerae serogroup O139 strains in China. Int J Antimicrob Agents 45:249–254

    Article  CAS  PubMed  Google Scholar 

  23. Bik EM, Gouw RD, Mooi FR (1996) DNA fingerprinting of Vibrio cholerae strains with a novel insertion sequence element: a tool to identify epidemic strains. J Clin Microbiol 34:1453–1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Dumontier S, Trieu-Cuot P, Berche P (1998) Structural and functional characterization of IS1358 from Vibrio cholerae. J Bacteriol 180:6101–6106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Pugliese N, Maimone F, Scrascia M, Materu SF, Pazzani C (2009) SXT-related integrating conjugative element and IncC plasmids in Vibrio cholerae O1 strains in eastern Africa. J Antimicrob Chemother 63:438–442

    Article  CAS  PubMed  Google Scholar 

  26. Mukhopadhyay AK, Basu A, Garg P, Bag PK, Ghosh A, Bhattacharya SK, Takeda Y, Nair GB (1998) Molecular epidemiology of reemergent Vibrio cholerae O139 Bengal in India. J Clin Microbiol 36:2149–2152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Pande K, Mendiratta DK, Vijayashri D, Thamke DC, Narang P (2012) SXT constin among Vibrio cholerae isolates from a tertiary care hospital. Indian J Med Res 135:346–350

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB, Reeves PR (1998) A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 95:3134–3139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Karaolis DK, Lan R, Kaper JB, Reeves PR (2001) Comparison of Vibrio cholerae pathogenicity islands in sixth and seventh pandemic strains. Infect Immun 69:1947–1952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Osin AV, Nefedov KS, Eroshenko GA, Smirnova NI (2005) Comparative genomic analysis of Vibrio cholerae El Tor pre-seventh and seventh pandemic strains isolated in various periods. Genetika 41:53–62. [In Russian]

    CAS  PubMed  Google Scholar 

  31. O’Shea YA, Reen FJ, Quirke AM, Boyd EF (2004) Evolutionary genetic analysis of the emergence of epidemic Vibrio cholerae isolates on the basis of comparative nucleotide sequence analysis and multilocus virulence gene profiles. J Clin Microbiol 42:4657–4671

    Article  PubMed  PubMed Central  Google Scholar 

  32. Rahman MH, Biswas K, Hossain MA, Sack RB, Mekalanos JJ, Faruque SM (2008) Distribution of genes for virulence and ecological fitness among diverse Vibrio cholerae population in a cholera endemic area: tracking the evolution of pathogenic strains. DNA Cell Biol 27:347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Nair GB, Safa A, Bhuiyan NA, Nusrin S, Murphy D, Nicol C, Valcanis M, Iddings S, Kubuabola I, Vally H (2006) Isolation of Vibrio cholerae O1 strains similar to pre-seventh pandemic El Tor strains during an outbreak of gastrointestinal disease in an island resort in Fiji. J Med Microbiol 55:1559–1562

    Article  CAS  PubMed  Google Scholar 

  34. Safa A, Bhuiyan NA, Murphy D, Bates J, Nusrin S, Kong RY, Chongsanguan M, Chaicumpa W, Nair GB (2009) Multilocus genetic analysis reveals that the Australian strains of Vibrio cholerae O1 are similar to the pre-seventh pandemic strains of the El Tor biotype. J Med Microbiol 58:105–111

    Article  CAS  PubMed  Google Scholar 

  35. Li M, Kotetishvili M, Chen Y, Sozhamannan S (2003) Comparative genomic analyses of the vibrio pathogenicity island and cholera toxin prophage regions in nonepidemic serogroup strains of Vibrio cholerae. Appl Environ Microbiol 69:1728–1738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914

    Article  CAS  PubMed  Google Scholar 

  37. Bhattacharya T, Chatterjee S, Mait D, Bhadra RK, Takeda Y, Nair GB, Nandy RK (2006) Molecular analysis of the rstR and orfU genes of the CTX prophages integrated in the small chromosomes of environmental Vibrio cholerae non-O1, non-O139 strains. Environ Microbiol 8:526–634

    Article  CAS  PubMed  Google Scholar 

  38. Kaper JB, Bradford HB, Roberts NC, Falkow S (1982) Molecular epidemiology of Vibrio cholerae in the U.S. Gulf Coast. J Clin Microbiol 16:129–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kaper JB, Nataro JP, Roberts NC, Siebeling RJ, Bradford HB (1986) Molecular epidemiology of non-O1 Vibrio cholerae and Vibrio mimicus in the U.S. Gulf Coast region. J Clin Microbiol 23:652–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Finch MJ, Morris JG, Kaviti J, Kagwanja W, Levine MM (1988) Epidemiology of antimicrobial resistant cholera in Kenya and East Africa. Am J Trop Med Hyg 39:484–490

    Article  CAS  PubMed  Google Scholar 

  41. Desmarchelier PM, Senn CR (1989) A molecular epidemiological study of V. cholerae in Australia. Med J Aust 150:631–634

    Article  CAS  PubMed  Google Scholar 

  42. Yam WC, Lung ML, Ng KY, Ng MH (1989) Molecular epidemiology of Vibrio cholerae in Hong Kong. J Clin Microbiol 27:1900–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wachsmuth IK, Evins GM, Fields PI, Olsvik O, Popovic T, Bopp CA, Wells JG, Carrillo C, Blake PA (1993) The molecular epidemiology of cholera in Latin America. J Infect Dis 167:621–626

    Article  CAS  PubMed  Google Scholar 

  44. Faruque SM, Abdul Alim AR, Roy SK, Khan F, Nair GB, Sack RB, Albert MJ (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 32:1050–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sharma C, Maiti S, Mukhopadhyay AK, Basu A, Basu I, Nair GB, Mukhopadhyaya R, Das B, Kar S, Ghosh RK, Ghosh A (1997) Unique organization of the CTX genetic element in Vibrio cholerae O139 strains which reemerged in Calcutta, India, in September 1996. J Clin Microbiol 35:3348–3350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Basu A, Mukhopadhyay AK, Sharma C, Jyot J, Gupta N, Ghosh A, Bhattacharya SK, Takeda Y, Faruque AS, Albert MJ, Balakrish Nair G (1998) Heterogeneity in the organization of the CTX genetic element in strains of Vibrio cholerae O139 Bengal isolated from Calcutta, India and Dhaka, Bangladesh and its possible link to the dissimilar incidence of O139 cholera in the two locales. Microb Pathog 24:175–183

    Article  CAS  PubMed  Google Scholar 

  47. Basu A, Garg P, Datta S, Chakraborty S, Bhattacharya T, Khan A, Ramamurthy T, Bhattacharya SK, Yamasaki S, Takeda Y, Nair GB (2000) Vibrio cholerae O139 in Calcutta, 1992–1998: incidence, antibiograms, and genotypes. Emerg Infect Dis 6:139–147

    Google Scholar 

  48. Qu M, Xu J, Ding Y, Wang R, Liu P, Kan B, Qi G, Liu Y, Gao S (2003) Molecular epidemiology of Vibrio cholerae O139 in China: polymorphism of ribotypes and CTX elements. J Clin Microbiol 41:2306–2310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pourshafie MR, Grimont F, Saifi M, Grimont PA (2000) Molecular epidemiological study of Vibrio cholerae isolates from infected patients in Teheran, Iran. J Med Microbiol 49:1085–1090

    Article  CAS  PubMed  Google Scholar 

  50. Raychoudhuri A, Chatterjee S, Pazhani GP, Nandy RK, Bhattacharya MK, Bhattacharya SK, Ramamurthy T, Mukhopadhyay AK (2007) Molecular characterization of recent Vibrio cholerae O1, El Tor, Inaba strains isolated from hospitalized patients in Kolkata, India. J Infect 55:431–438

    Article  PubMed  Google Scholar 

  51. Lee JH, Han KH, Choi SY, Lucas ME, Mondlane C, Ansaruzzaman M, Nair GB, Sack DA, von Seidlein L, Clemens JD, Song M, Chun J, Kim DW (2006) Mozambique cholera vaccine demonstration project coordination group. Multilocus sequence typing (MLST) analysis of Vibrio cholerae O1 El Tor isolates from Mozambique that harbour the classical CTX prophage. J Med Microbiol 55:165–170

    Article  CAS  PubMed  Google Scholar 

  52. Faruque SM, Tam VC, Chowdhury N, Diraphat P, Dziejman M, Heidelberg JF, Clemens JD, Mekalanos JJ, Nair GB (2007) Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. Proc Natl Acad Sci U S A 104:5151–5156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zahid MS, Udden SM, Faruque AS, Calderwood SB, Mekalanos JJ, Faruque SM (2008) Effect of phage on the infectivity of Vibrio cholerae and emergence of genetic variants. Infect Immun 76:5266–5273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Olsvik O, Wahlberg J, Petterson B, Uhlén M, Popovic T, Wachsmuth IK, Fields PI (1993) Use of automated sequencing of polymerase chain reaction-generated amplicons to identify three types of cholera toxin subunit B in Vibrio cholerae O1 strains. J Clin Microbiol 31:22–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Nair GB, Qadri F, Holmgren J, Svennerholm AM, Safa A, Bhuiyan NA, Ahmad QS, Faruque SM, Faruque AS, Takeda Y, Sack DA (2006) Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol 44:4211–4213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Raychoudhuri A, Patra T, Ghosh K, Ramamurthy T, Nandy RK, Takeda Y, Balakrish Nair G, Mukhopadhyay AK (2009) Classical ctxB in Vibrio cholerae O1, Kolkata, India. Emerg Infect Dis 15:131–132

    Article  PubMed  PubMed Central  Google Scholar 

  57. Kumar P, Jain M, Goel AK et al (2009) A large cholera outbreak due to a new cholera toxin variant of the Vibrio cholerae O1 El Tor biotype in Orissa, eastern India. J Med Microbiol 58:234–238

    Article  CAS  PubMed  Google Scholar 

  58. Taneja N, Mishra A, Sangar G, Singh G, Sharma M (2009) Outbreak caused by new variants of Vibrio cholerae O1 El Tor, India. Emerg Infect Dis 15:352–354

    Article  PubMed  PubMed Central  Google Scholar 

  59. Bhuiyan NA, Nusrin S, Alam M, Morita M, Watanabe H, Ramamurthy T, Cravioto A, Nair GB (2009) Changing genotypes of cholera toxin (CT) of Vibrio cholerae O139 in Bangladesh and description of three new CT genotypes. FEMS Immunol Med Microbiol 57:136–141

    Article  CAS  PubMed  Google Scholar 

  60. Kim EJ, Lee CH, Nair GB, Kim DW (2015) Whole-genome sequence comparisons reveal the evolution of Vibrio cholerae O1. Trends Microbiol 23:479–489

    Article  CAS  PubMed  Google Scholar 

  61. Naha A, Pazhani GP, Ganguly M, Ghosh S, Ramamurthy T, Nandy RK, Nair GB, Takeda Y, Mukhopadhyay AK (2012) Development and evaluation of a PCR assay for tracking the emergence and dissemination of Haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata, India. J Clin Microbiol 50:1733–1736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Hasan NA, Choi SY, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine E, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett CM, Cravioto A, Huq A, Ravel J, Cebula TA, Colwell RR (2012) Genomic diversity of 2010 Haitian cholera outbreak strains. Proc Natl Acad Sci U S A 109:E2010–E2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Rashed SM, Mannan SB, Johura FT, Islam MT, Sadique A, Watanabe H, Sack RB, Huq A, Colwell RR, Cravioto A, Alam M (2012) Genetic characteristics of drug-resistant Vibrio cholerae O1 causing endemic cholera in Dhaka, 2006–2011. J Med Microbiol 61:1736–1745

    Article  PubMed  PubMed Central  Google Scholar 

  64. Rashid MU, Rashed SM, Islam T, Johura FT, Watanabe H, Ohnishi M, Alam M (2016) CtxB1 outcompetes CtxB7 in Vibrio cholerae O1, Bangladesh. J Med Microbiol 65:101–103

    Article  PubMed  Google Scholar 

  65. Momen H, Salles CA (1985) Enzyme markers for Vibrio cholerae: identification of classical, El Tor and environmental strains. Trans R SocTrop Med Hyg 79:773–776

    Article  CAS  Google Scholar 

  66. Freitas FS, Momen H, Salles CA (2002) The zymovars of Vibrio cholerae: multilocus enzyme electrophoresis of Vibrio cholerae. Mem Inst Oswaldo Cruz 97:511–516

    Article  CAS  PubMed  Google Scholar 

  67. Lan R, Reeves PR (1998) Recombination between rRNA operons created most of the ribotype variation observed in the seventh pandemic clone of Vibrio cholerae. Microbiology 144:1213–1221

    Article  CAS  PubMed  Google Scholar 

  68. Popovic T, Bopp C, Olsvik O, Wachsmuth K (1993) Epidemiologic application of a standardized ribotype scheme for Vibrio cholerae O1. J Clin Microbiol 31:2474–2482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Karaolis DK, Lan R, Reeves PR (1994) Molecular evolution of the seventh-pandemic clone of Vibrio cholerae and its relationship to other pandemic and epidemic V. cholerae isolates. J Bacteriol 176:6199–6206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Desmarchelier PM, Wong FY, Mallard K (1995) An epidemiological study of Vibrio cholerae O1 in the Australian environment based on rRNA gene polymorphisms. Epidemiol Infect 115:435–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Faruque SM, Ahmed KM, Abdul Alim AR, Qadri F, Siddique AK, Albert MJ (1997) Emergence of a new clone of toxigenic Vibrio cholerae O1 biotype El Tor displacing V. cholerae O139 Bengal in Bangladesh. J Clin Microbiol 35:624–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Bag PK, Maiti S, Sharma C, Ghosh A, Basu A, Mitra R, Bhattacharya SK, Nakamura S, Yamasaki S, Takeda Y, Balakrish Nair G (1998) Rapid spread of the new clone of Vibrio cholerae O1 biotype El Tor in cholera endemic areas in India. Epidemiol Infect 121:245–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Dalsgaard A, Serichantalergs O, Forslund A, Pitarangsi C, Echeverria P (1998) Phenotypic and molecular characterization of Vibrio cholerae O1 isolated in Samutsakorn, Thailand before, during and after the emergence of V. cholerae O139. Epidemiol Infect 121:259–268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Faruque SM, Ahmed KM, Siddique AK, Zaman K, Alim AR, Albert MJ (1997) 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 35:2299–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Damian M, Koblavi S, Carle I, Nacescu N, Grimont F, Ciufecu C, Grimont PA (1998) Molecular characterization of Vibrio cholerae O1 strains isolated in Romania. Res Microbiol 149:745–755

    Article  CAS  PubMed  Google Scholar 

  76. Dutta B, Ghosh R, Sharma NC, Pazhani GP, Taneja N, Raychowdhuri A, Sarkar BL, Mondal SK, Mukhopadhyay AK, Nandy RK, Bhattacharya MK, Bhattacharya SK, Ramamurthy T (2006) Spread of cholera with newer clones of Vibrio cholerae O1 El Tor, serotype Inaba, in India. J Clin Microbiol 44:3391–3393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Scrascia M, Maimone F, Mohamud KA, Materu SF, Grimont F, Grimont PA, Pazzani C (2006) Clonal relationship among Vibrio cholerae O1 El Tor strains causing the largest cholera epidemic in Kenya in the late 1990s. J Clin Microbiol 44:3401–3404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Tapchaisri P, Na-Ubol M, Jaipaew J, Srimanote P, Chongsa-Nguan M, Yamasaki S, Hayashi H, Nair GB, Kurazono H, Chaicumpa W (2007) Virulence genes of clinical Vibrio cholerae O1 isolates in Thailand and their ribotypes. J Infect 55:557–565

    Article  PubMed  Google Scholar 

  79. Lizárraga-Partida ML, Quilici ML (2009) Molecular analyses of Vibrio cholerae O1 clinical strains, including new nontoxigenic variants isolated in Mexico during the cholera epidemic years between 1991 and 2000. J Clin Microbiol 47:1364–1371

    Article  PubMed  PubMed Central  Google Scholar 

  80. Cooper KL, Luey CK, Bird M, Terajima J, Nair GB, Kam KM, Arakawa E, Safa A, Cheung DT, Law CP, Watanabe H, Kubota K, Swaminathan B, Ribot EM (2006) Development and validation of a PulseNet standardized pulsed-field gel electrophoresis protocol for subtyping of Vibrio cholerae. Foodborne Pathog Dis 3:51–58

    Article  CAS  PubMed  Google Scholar 

  81. Iwanaga M, Honma Y, Enami M (1997) Molecular epidemiology of Vibrio cholerae O1 isolated from sporadic cholera cases in Okinawa, Japan. Microbiol Immunol 41:861–864

    Article  CAS  PubMed  Google Scholar 

  82. Arakawa E, Murase T, Matsushita S, Shimada T, Yamai S, Ito T, Watanabe H (2000) Pulsed-field gel electrophoresis-based molecular comparison of Vibrio cholerae O1 isolates from domestic and imported cases of cholera in Japan. J Clin Microbiol 38:424–426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Garg P, Nandy RK, Chaudhury P, Chowdhury NR, De K, Ramamurthy T, Yamasaki S, Bhattacharya SK, Takeda Y, Nair GB (2000) Emergence of Vibrio cholerae O1 biotype El Tor serotype Inaba from the prevailing O1 Ogawa serotype strains in India. J Clin Microbiol 38:4249–4253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Chakraborty S, Deokule JS, Garg P, Bhattacharya SK, Nandy RK, Nair GB, Yamasaki S, Takeda Y, Ramamurthy T (2001) Concomitant infection of enterotoxigenic Escherichia coli in an outbreak of cholera caused by Vibrio cholerae O1 and O139 in Ahmedabad, India. J Clin Microbiol 39:3241–3246

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Miyagi K, Nakano T, Yagi T, Hanafusa M, Imura S, Honda T, Nakano Y, Sano K (2003) Survey of Vibrio cholerae O1 and its survival over the winter in marine water of Port of Osaka. Epidemiol Infect 131:613–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kam KM, Luey CK, Tsang YM, Law CP, Chu MY, Cheung TL, Chiu AW (2003) Molecular subtyping of Vibrio cholerae O1 and O139 by pulsed-field gel electrophoresis in Hong Kong: correlation with epidemiological events from 1994 to 2002. J Clin Microbiol 41:4502–4511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Tapchaisri P, Na-Ubol M, Tiyasuttipan W, Chaiyaroj SC, Yamasaki S, Wongsaroj T, Hayashi H, Nair GB, Chongsa-Nguan M, Kurazono H, Chaicumpa W (2008) Molecular typing of Vibrio cholerae O1 isolates from Thailand by pulsed-field gel electrophoresis. J Health Popul Nutr 26:79–87

    PubMed  PubMed Central  Google Scholar 

  88. Ansaruzzaman M, Bhuiyan NA, Safa A, Sultana M, McUamule A, Mondlane C, Wang XY, Deen JL, von Seidlein L, Clemens JD, Lucas M, Sack DA, Balakrish Nair G (2007) Genetic diversity of El Tor strains of Vibrio cholerae O1 with hybrid traits isolated from Bangladesh and Mozambique. Int J Med Microbiol 297:443–449

    Article  CAS  PubMed  Google Scholar 

  89. Keddy KH, Nadan S, Govind C, Sturm AW, Group for Enteric, Respiratory and Meningeal Disease Surveillance in South Africa (2007) Evidence for a clonally different origin of the two cholera epidemics of 2001–2002 and 1980–1987 in South Africa. J Med Microbiol 56:1644–1650

    Article  CAS  PubMed  Google Scholar 

  90. Chomvarin C, Jumroenjit W, Wongboot W, Kanoktippornchai B, Chaimanee P, Jamjane O, Huttayananont S, Tangkanakul W (2012) Molecular analysis and antimicrobial resistance of Vibrio cholerae O1 in northeastern Thailand. Southeast Asian J Trop Med Public Health 43:1437–1446

    CAS  PubMed  Google Scholar 

  91. Ismail H, Smith AM, Tau NP, Sooka A, Keddy KH, Group for Enteric, Respiratory and Meningeal Disease Surveillance in South Africa (2013) Cholera outbreak in South Africa, 2008–2009: laboratory analysis of Vibrio cholerae O1 strains. J Infect Dis 208(Suppl 1):S39–S45

    Article  CAS  PubMed  Google Scholar 

  92. Mahmud ZH, Islam S, Zaman RU, Akter M, Talukder KA, Bardhan PK, Khan AI, Rhodes FC, Kamara A, Wurie IM, Alemu W, Jambai A, Faruque SM, Clemens JD, Islam MS (2014) Phenotypic and genotypic characteristics of Vibrio cholerae O1 isolated from the Sierra Leone cholera outbreak in 2012. Trans R Soc Trop Med Hyg 108:715–720

    Article  CAS  PubMed  Google Scholar 

  93. Mercy N, Mohamed AA, Zipporah N, Chowdhury G, Pazhani GP, Ramamurthy T, Boga HI, Kariuki SM, Joseph O (2014) Phenotypic and genetic characterization of Vibrio cholerae O1 isolated from various regions of Kenya between 2007 and 2010. Pan Afr Med J 19:8

    Article  PubMed  PubMed Central  Google Scholar 

  94. Ghosh R, Sharma NC, Halder K, Bhadra RK, Chowdhury G, Pazhani GP, Shinoda S, Mukhopadhyay AK, Nair GB, Ramamurthy T (2016) Phenotypic and genetic heterogeneity in Vibrio cholerae O139 isolated from cholera cases in Delhi, India during 2001–2006. Front Microbiol 7:1250

    Article  PubMed  PubMed Central  Google Scholar 

  95. Nguyen VH, Pham HT, Diep TT, Phan CD, Nguyen TQ, Nguyen NT, Ngo TC, Nguyen TV, Do QK, Phan HC, Nguyen BM, Ehara M, Ohnishi M, Yamashiro T, Nguyen LT, Izumiya H (2016) Vibrio cholerae O1 El Tor from southern Vietnam in 2010 was molecularly distinct from that present from 1999 to 2004. Epidemiol Infect 144:1241–1247

    Google Scholar 

  96. Lü H, Yuan Y, Sun N, Bi Z, Guan B, Shao K, Wang T, Bi Z (2017) Characterization of Vibrio cholerae isolates from 1976 to 2013 in Shandong Province, China. Braz J Microbiol 48:173–179

    Article  PubMed  Google Scholar 

  97. Hajia M, Sohrabi A (2019) In silico characteristics for reemerging possibility of Vibrio cholerae genotypes in Iran. New Microbes New Infect 31:100577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Feglo PK, Sewurah M (2018) Characterization of highly virulent multidrug resistant Vibrio cholerae isolated from a large cholera outbreak in Ghana. BMC Res Notes 11(1):45

    Article  PubMed  PubMed Central  Google Scholar 

  99. Roobthaisong A, Okada K, Htun N, Aung WW, Wongboot W, Kamjumphol W, Han AA, Yi Y, Hamada S (2017) Molecular epidemiology of cholera outbreaks during the rainy season in Mandalay, Myanmar. Am J Trop Med Hyg 97:1323–1328

    Article  PubMed  PubMed Central  Google Scholar 

  100. Liao F, Mo Z, Chen M, Pang B, Fu X, Xu W, Jing H, Kan B, Gu W (2018) Comparison and evaluation of the molecular typing methods for toxigenic Vibrio cholerae in Southwest China. Front Microbiol 9:905

    Article  PubMed  PubMed Central  Google Scholar 

  101. Reimer AR, Van Domselaar G, Stroika S, Walker M, Kent H, Tarr C, Talkington D, Rowe L, Olsen-Rasmussen M, Frace M, Sammons S, Dahourou GA, Boncy J, Smith AM, Mabon P, Petkau A, Graham M, Gilmour MW, Gerner-Smidt P, V. cholerae Outbreak Genomics Task Force (2011) Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. Emerg Infect Dis 17:2113–2121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Díaz-Quiñonez JA (2017) Genome sequence analysis of Vibrio cholerae clinical isolates from 2013 in Mexico reveals the presence of the strain responsible for the 2010 Haiti outbreak. Gac Med Mex 153(Supl. 2):S91–S101. [in Spanish]

    PubMed  Google Scholar 

  103. Alam M, Islam MT, Rashed SM, Johura FT, Bhuiyan NA, Delgado G, Morales R, Mendez JL, Navarro A, Watanabe H, Hasan NA, Colwell RR, Cravioto A (2012) Vibrio cholerae classical biotype strains reveal distinct signatures in Mexico. J Clin Microbiol 50:2212–2216

    Google Scholar 

  104. Kotetishvili M, Stine OC, Chen Y, Kreger A, Sulakvelidze A, Sozhamannan S, Morris JG Jr (2003) Multilocus sequence typing has better discriminatory ability for typing Vibrio cholerae than does pulsed-field gel electrophoresis and provides a measure of phylogenetic relatedness. J Clin Microbiol 41:2191–2196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Farfán M, Miñana-Galbis D, Fusté MC, Lorén JG (2002) Allelic diversity and population structure in Vibrio cholerae O139 Bengal based on nucleotide sequence analysis. J Bacteriol 184:1304–1313

    Article  PubMed  PubMed Central  Google Scholar 

  106. Salim A, Lan R, Reeeves PR (2005) Vibrio cholerae pathogenic clones. Emerg Infect Dis 11:1758–1760

    Google Scholar 

  107. Greig DR, Schaefer U, Octavia S, Hunter E, Chattaway MA, Dallman TJ, Jenkins C (2018) Evaluation of whole-genome sequencing for identification and typing of Vibrio cholerae. J Clin Microbiol 56(11):pii: e00831-18

    Article  Google Scholar 

  108. Tu YH, Chen BH, Hong YP, Liao YS, Chen YS, Liu YY, Teng RH, Wang YW, Chiou CS (2020) Emergence of Vibrio cholerae O1 sequence type 75 in Taiwan. Emerg Infect Dis 26:164–166

    Article  PubMed  PubMed Central  Google Scholar 

  109. Garrine M, Mandomando I, Vubil D, Nhampossa T, Acacio S, Li S, Paulson JN, Almeida M, Domman D, Thomson NR, Alonso P, Stine OC (2017) Minimal genetic change in Vibrio cholerae in Mozambique over time: multilocus variable number tandem repeat analysis and whole genome sequencing. PLoS Negl Trop Dis 11(6):e0005671

    Article  PubMed  PubMed Central  Google Scholar 

  110. Garg P, Aydanian A, Smith DJ, Glenn M Jr, Nair GB, Stine OC (2003) Molecular epidemiology of O139 Vibrio cholerae: mutation, lateral gene transfer, and founder flush. Emerg Infect Dis 9:810–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Ghosh R, Nair GB, Tang L, Morris JG, Sharma NC, Ballal M, Garg P, Ramamurthy T, Stine OC (2008) Epidemiological study of Vibrio cholerae using variable number of tandem repeats. FEMS Microbiol Lett 288:196–201

    Article  CAS  PubMed  Google Scholar 

  112. Stine OC, Alam M, Tang L, Nair GB, Siddique AK, Faruque SM, Huq A, Colwell R, Sack RB, Morris JG Jr (2008) Seasonal cholera from multiple small outbreaks, rural Bangladesh. Emerg Infect Dis 14:831–833

    Article  PubMed  PubMed Central  Google Scholar 

  113. Ambroise J, Irenge LM, Durant JF, Bearzatto B, Bwire G, Stine OC, Gala JL (2019) Backward compatibility of whole genome sequencing data with MLVA typing using a new MLVAtype shiny application for Vibrio cholerae. PLoS One 14(12):e0225848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Sharma C, Ghosh A, Dalsgaard A, Forslund A, Ghosh RK, Bhattacharya SK, Nair GB (1998) Molecular evidence that a distinct Vibrio cholerae O1 biotype El Tor strain in Calcutta may have spread to the African continent. J Clin Microbiol 36:843–844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Clark CG, Kravetz AN, Dendy C, Wang G, Tyler KD, Johnson WM (1998) Investigation of the 1994–5 Ukrainian Vibrio cholerae epidemic using molecular methods. Epidemiol Infect 12:15–29

    Article  Google Scholar 

  116. Pazzani C, Scrascia M, Dionisi AM, Maimone F, Luzzi I (2006) Molecular epidemiology and origin of cholera reemergence in Italy and Albania in the 1990s. Res Microbiol 157:508–512

    Article  CAS  PubMed  Google Scholar 

  117. Chatterjee S, Patra T, Ghosh K, Raychoudhuri A, Pazhani GP, Das M, Sarkar B, Bhadra RK, Mukhopadhyay AK, Takeda Y, Nair GB, Ramamurthy T, Nandy RK (2009) Vibrio cholerae O1 clinical strains isolated in 1992 in Kolkata with progenitor traits of the 2004 Mozambique variant. J Med Microbiol 58:239–247

    Google Scholar 

  118. Joelsson A, Liu Z, Zhu J (2006) Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect Immun 74:1141–1147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ (2002) Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci U S A 99:1556–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Pang B, Yan M, Cui Z, Ye X, Diao B, Ren Y, Gao S, Zhang L, Kan B (2007) Genetic diversity of toxigenic and nontoxigenic Vibrio cholerae serogroups O1 and O139 revealed by array-based comparative genomic hybridization. J Bacteriol 189:4837–4849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Dziejman M, Serruto D, Tam VC, Sturtevant D, Diraphat P, Faruque SM, Rahman MH, Heidelberg JF, Decker J, Li L, Montgomery KT, Grills G, Kucherlapati R, Mekalanos JJ (2005) Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc Natl Acad Sci U S A 102:3465–3470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Feng L, Reeves PR, Lan R, Ren Y, Gao C, Zhou Z, Ren Y, Cheng J, Wang W, Wang J, Qian W, Li D, Wang L (2008) A recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS One 3:e4053

    Article  PubMed  PubMed Central  Google Scholar 

  123. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY, Haley BJ, Taviani E, Jeon YS, Kim DW, Lee JH, Brettin TS, Bruce DC, Challacombe JF, Detter JC, Han CS, Munk AC, Chertkov O, Meincke L, Saunders E, Walters RA, Huq A, Nair GB, Colwell RR (2009) Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 106:15442–15447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, Croucher NJ, Choi SY, Harris SR, Lebens M, Niyogi SK, Kim EJ, Ramamurthy T, Chun J, Wood JL, Clemens JD, Czerkinsky C, Nair GB, Holmgren J, Parkhill J, Dougan G (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477(7365):462–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Weill FX, Domman D, Njamkepo E, Tarr C, Rauzier J, Fawal N, Keddy KH, Salje H, Moore S, Mukhopadhyay AK, Bercion R, Luquero FJ, Ngandjio A, Dosso M, Monakhova E, Garin B, Bouchier C, Pazzani C, Mutreja A, Grunow R, Sidikou F, Bonte L, Breurec S, Damian M, Njanpop-Lafourcade BM, Sapriel G, Page AL, Hamze M, Henkens M, Chowdhury G, Mengel M, Koeck JL, Fournier JM, Dougan G, Grimont PAD, Parkhill J, Holt KE, Piarroux R, Ramamurthy T, Quilici ML, Thomson NR (2017) Genomic history of the seventh pandemic of cholera in Africa. Science 358(6364):785–789

    Article  CAS  PubMed  Google Scholar 

  126. Bwire G, Sack DA, Almeida M, Li S, Voeglein JB, Debes AK, Kagirita A, Buyinza AW, Orach CG, Stine OC (2018) Molecular characterization of Vibrio cholerae responsible for cholera epidemics in Uganda by PCR, MLVA and WGS. PLoS Negl Trop Dis 12(6):e0006492

    Article  PubMed  PubMed Central  Google Scholar 

  127. Domman D, Quilici ML, Dorman MJ, Njamkepo E, Mutreja A, Mather AE, Delgado G, Morales-Espinosa R, Grimont PAD, Lizárraga-Partida ML, Bouchier C, Aanensen DM, Kuri-Morales P, Tarr CL, Dougan G, Parkhill J, Campos J, Cravioto A, Weill FX, Thomson NR (2017) Integrated view of Vibrio cholerae in the Americas. Science 358(6364):789–793

    Article  CAS  PubMed  Google Scholar 

  128. Mironova LV, Gladkikh AS, Ponomareva AS, Feranchuk SI, Bochalgin NО, Basov EA, Yu Khunkheeva Z, Balakhonov SV (2018) Comparative genomics of Vibrio cholerae El Tor strains isolated at epidemic complications in Siberia and at the Far East. Infect Genet Evol 60:80–88

    Article  CAS  PubMed  Google Scholar 

  129. Weill FX, Domman D, Njamkepo E, Almesbahi AA, Naji M, Nasher SS, Rakesh A, Assiri AM, Sharma NC, Kariuki S, Pourshafie MR, Rauzier J, Abubakar A, Carter JY, Wamala JF, Seguin C, Bouchier C, Malliavin T, Bakhshi B, Abulmaali HHN, Kumar D, Njoroge SM, Malik MR, Kiiru J, Luquero FJ, Azman AS, Ramamurthy T, Thomson NR, Quilici ML (2019) Genomic insights into the 2016–2017 cholera epidemic in Yemen. Nature 565(7738):230–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Hounmanou YMG, Leekitcharoenphon P, Kudirkiene E, Mdegela RH, Hendriksen RS, Olsen JE, Dalsgaard A (2019) Genomic insights into Vibrio cholerae O1 responsible for cholera epidemics in Tanzania between 1993 and 2017. PLoS Negl Trop Dis 13(12):e0007934

    Article  PubMed  PubMed Central  Google Scholar 

  131. Hu D, Yin Z, Yuan C, Yang P, Qian C, Wei Y, Zhang S, Wang Y, Yuan J, Wang M, Reeves PR, Tu L, Chen M, Huang D, Liu B (2019) Changing molecular epidemiology of Vibrio cholerae outbreaks in Shanghai, China. mSystems 4(6):pii: e00561-19

    Article  Google Scholar 

  132. Greenhill AR, Mutreja A, Bulach D, Belousoff MJ, Jonduo MH, Collins DA, Kas MP, Wapling J, Seemann T, Lafana A, Dougan G, Brown MV, Horwood PF (2019) Wave 2 strains of atypical Vibrio cholerae El Tor caused the 2009–2011 cholera outbreak in Papua New Guinea. Microb Genome 5(3)

    Google Scholar 

  133. Li Z, Pang B, Wang D, Li J, Xu J, Fang Y, Lu X, Kan B (2019) Expanding dynamics of the virulence-related gene variations in the toxigenic Vibrio cholerae serogroup O1. BMC Genomics 20(1):360

    Article  PubMed  PubMed Central  Google Scholar 

  134. 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 (2000) DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406(6795):477–483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Hur Y, Chalita M, Ha SM, Baek I, Chun J (2019) VCGIDB: a database and web resource for the genomic islands from Vibrio Cholerae. Pathogens. 8(4):pii: E261

    Google Scholar 

  136. Blokesch M, Schoolnik GK (2008) The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J Bacteriol 190:7232–7240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Meibom KL, Blokesch M, Dolganov NA, Wu CY, Schoolnik GK (2005) Chitin induces natural competence in Vibrio cholerae. Science 310(5755):1824–1827

    Article  CAS  PubMed  Google Scholar 

  138. Dalia AB, Dalia TN (2019) Spatiotemporal analysis of DNA integration during natural transformation reveals a mode of nongenetic inheritance in bacteria. Cell 179(7):1499–1511.e10

    Google Scholar 

  139. Das B, Pazhani GP, Sarkar A, Mukhopadhyay AK, Nair GB, Ramamurthy T (2016) Molecular evolution and functional divergence of Vibrio cholerae. Curr Opin Infect Dis 29:520–527

    Article  CAS  PubMed  Google Scholar 

  140. Das B (2019) Insights into TLCPhi lysogeny: a twist in the mechanism of IMEX integration. Proc Natl Acad Sci U S A 116:18159–18161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Safa A, Sultana J, Dac Cam P, Mwansa JC, Kong RY (2008) Vibrio cholerae O1 hybrid El Tor strains, Asia and Africa. Emerg Infect Dis 14:987–988

    Google Scholar 

  142. Siddique AK, Nair GB, Alam M, Sack DA, Huq A, Nizam A, Longini IM, Qadri F, Faruque SM, Colwell RR, Ahmed S, Iqbal A, Bhuiyan NA, Sack RB (2009) El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect 14:1–6

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Bacteriology, National Institute of Cholera and Enteric Diseases, Kolkata, India

    Thandavarayan Ramamurthy, Asish K. Mukhopadhyay & Ranjan K. Nandy

  2. Infection and Immunity Division, Translational Health Science and Technology Institute, Faridabad, India

    Bhabatosh Das

  3. Department of Medicine, Addenbrooke’s Hospital, University of Cambridge, Cambridge, UK

    Ankur Mutreja

  4. Rajiv Gandhi Centre for Biotechnology, Trivandrum, India

    G. Balakrish Nair

Authors
  1. Thandavarayan Ramamurthy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Asish K. Mukhopadhyay
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bhabatosh Das
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ranjan K. Nandy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ankur Mutreja
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. G. Balakrish Nair
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thandavarayan Ramamurthy .

Editor information

Editors and Affiliations

  1. Instituto Nacional de Controle de, Qualidade em Saude (INCQS), Fundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, Rio de Janeiro, Brazil

    Ivano de Filippis

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ramamurthy, T., Mukhopadhyay, A.K., Das, B., Nandy, R.K., Mutreja, A., Nair, G.B. (2022). Vibrio cholerae . In: de Filippis, I. (eds) Molecular Typing in Bacterial Infections, Volume II. Springer, Cham. https://doi.org/10.1007/978-3-030-83217-9_5

Download citation

Publish with us

Policies and ethics

Search

Navigation