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Volume 9, Issue 4

O37: one of the exceptions that prove the rule Open Access

Abstract

Between 1965 and 1968, outbreaks of cholera in Sudan and former Czechoslovakia provoked considerable public health concern. These still represent important historical events that need to be linked to the growing genomic evidence describing the aetiological agent of cholera, . Whilst O1 serogroup are canonically associated with epidemic and pandemic cholera, these events were caused by a clone of toxigenic O37 that may be more globally distributed than just to Europe and North Africa. Understanding the biology of these non-O1 strains of is key to understanding how diseases like cholera continue to be globally important. In this article, we consolidate epidemiological, molecular and genomic descriptions of the bacteria responsible for these outbreaks. We attempt to resolve discrepancies in order to summarize the history and provenance of as many commonly used serogroup O37 strains as possible. Finally, we highlight the potential for whole-genome sequencing of O37 isolates from strain collections to shed light on the open questions that we identify.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cholera , epidemic , serogroup O37 , Sudan and Vibrio cholerae
Funding
This study was supported by the:
  • Wellcome Trust (Award 108413/A/15/D)
    • Principle Award Recipient: NicholasR. Thomson
  • Wellcome Trust (Award 206194)
    • Principle Award Recipient: NicholasR. Thomson
  • Churchill College, University of Cambridge (Award Junior Research Fellowship)
    • Principle Award Recipient: MatthewJ. Dorman
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-05-04
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References

  1. Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. Cholera. Lancet 2017; 390:1539–1549 [View Article] [PubMed]
     [Google Scholar]
  2. Mekalanos JJ. Duplication and amplification of toxin genes in Vibrio cholerae. Cell 1983; 35:253–263 [View Article]
     [Google Scholar]
  3. Pearson GD, Mekalanos JJ. Molecular cloning of Vibrio cholerae enterotoxin genes in Escherichia coli K-12. Proc Natl Acad Sci U S A 1982; 79:2976–2980 [View Article]
     [Google Scholar]
  4. Karaolis DKR, Johnson JA, Bailey CC, Boedeker EC, Kaper JB et al. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci USA 1998; 95:3134–3139 [View Article]
     [Google Scholar]
  5. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996; 272:1910–1914 [View Article] [PubMed]
     [Google Scholar]
  6. Iredell JR, Manning PA. Biotype-specific tcpA genes in Vibrio cholerae. FEMS Microbiol Lett 1994; 121:47–54 [View Article]
     [Google Scholar]
  7. Chatterjee SN, Chaudhuri K. Lipopolysaccharides of Vibrio cholerae. Biochim Biophys Acta 2003; 1639:65–79 [View Article]
     [Google Scholar]
  8. Shimada T, Arakawa E, Itoh K, Okitsu T, Matsushima A et al. Extended serotyping scheme for Vibrio cholerae. Curr Microbiol 1994; 28:175–178 [View Article]
     [Google Scholar]
  9. Domman D, Quilici ML, Dorman MJ, Njamkepo E, Mutreja A et al. Integrated view of Vibrio cholerae in the Americas. Science 2017; 358:789–793 [View Article]
     [Google Scholar]
  10. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477:462–465 [View Article] [PubMed]
     [Google Scholar]
  11. Faruque SM, Chowdhury N, Kamruzzaman M, Ahmad QS, Faruque ASG et al. Reemergence of epidemic Vibrio cholerae O139, Bangladesh. Emerg Infect Dis 2003a; 9:1116–1122 [View Article]
     [Google Scholar]
  12. Faruque SM, Sack DA, Sack RB, Colwell RR, Takeda Y et al. Emergence and evolution of Vibrio cholerae O139. Proc Natl Acad Sci U S A 2003b; 100:1304–1309 [View Article]
     [Google Scholar]
  13. Stroeher UH, Jedani KE, Manning PA. Genetic organization of the regions associated with surface polysaccharide synthesis in Vibrio cholerae O1, O139 and Vibrio anguillarum O1 and O2: a review. Gene 1998; 223:269–282 [View Article]
     [Google Scholar]
  14. Ramamurthy T, Pragasam AK, Taylor-Brown A, Will RC, Vasudevan K et al. Vibrio cholerae O139 genomes provide a clue to why it may have failed to usher in the eighth cholera pandemic. Nat Commun 2022; 13:3864 [View Article]
     [Google Scholar]
  15. Centers for Disease Control and Prevention (CDC) Diagnosis and Detection | Cholera | CDC; 2018 www.cdc.gov/cholera/diagnosis.html accessed 25 July 2020
  16. Centers for Disease Control and Prevention (CDC) Chapter 6 – Laboratory Identification of Vibrio cholerae. In Laboratory Methods for the Diagnosis of Vibrio Cholerae Centers for Disease Control and Prevention;
     [Google Scholar]
  17. Ali M, Nelson AR, Lopez AL, Sack DA, Remais JV. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis 2015; 9:e0003832 [View Article]
     [Google Scholar]
  18. Cheasty T, Said B, Threlfall EJ. V. cholerae non-O1: implications for man?. Lancet 1999; 354:89–90 [View Article]
     [Google Scholar]
  19. Piergentili P, Castellani-Pastoris M, Fellini RD, Farisano G, Bonello C et al. Transmission of non O group 1 Vibrio cholerae by raw oyster consumption. Int J Epidemiol 1984; 13:340–343 [View Article]
     [Google Scholar]
  20. Dakin WP, Howell DJ, Sutton RG, O’Keefe MF, Thomas P. Gastroenteritis due to non-agglutinable (non-cholera) Vibrios. Med J Aust 1974; 2:487–490 [View Article]
     [Google Scholar]
  21. Kamal A. Outbreak of gastroenteritis by non-agglutinable (NAG) vibrios in the republic of the Sudan. J Egypt Public Health Assoc 1971; 46:125–133
     [Google Scholar]
  22. World Health Organization Weekly epidemiological record. Weekly Epidemiological Record 1969; 44:1–27
     [Google Scholar]
  23. Furniss AL, Lee JV, Donovan TJ. The Vibrios London: H.M.S.O; 1978
     [Google Scholar]
  24. Sakazaki R, Tamura K, Gomez CZ, Sen R. Serological studies on the cholera group of vibrios. Jpn J Med Sci Biol 1970; 23:13–20 [View Article] [PubMed]
     [Google Scholar]
  25. Beltrán P, Delgado G, Navarro A, Trujillo F, Selander RK et al. Genetic diversity and population structure of Vibrio cholerae. J Clin Microbiol 1999a; 37:581–590 [View Article]
     [Google Scholar]
  26. Chapman C, Henry M, Bishop-Lilly KA, Awosika J, Briska A et al. Scanning the landscape of genome architecture of non-O1 and non-O139 Vibrio cholerae by whole genome mapping reveals extensive population genetic diversity. PLoS One 2015; 10:e0120311 [View Article]
     [Google Scholar]
  27. Shimada T, Sakazaki R. Additional serovars and inter-O antigenic relationships of Vibrio cholerae. Jpn J Med Sci Biol 1977; 30:275–277 [View Article]
     [Google Scholar]
  28. Aldová E, Láznicková K, Stĕpánková E, Lietava J. Isolation of nonagglutinable Vibrios from an enteritis outbreak in Czechoslovakia. J Infect Dis 1968; 118:25–31 [View Article]
     [Google Scholar]
  29. Felsenfeld O, Stegherr-Barrios A, Aldová E, Holmes J, Parrott MW. In vitro and in vivo studies of streptomycin-dependent cholera vibrios. Appl Microbiol 1970; 19:463–469 [View Article]
     [Google Scholar]
  30. American Type Culture Collection Vibrio cholerae Pacini ATCC ® 25873TM; 2016a www.lgcstandards-atcc.org/Products/All/25873.aspx?geo_country=gb#history accessed 1 February 2021
  31. American Type Culture Collection Vibrio cholerae Pacini ATCC ® 25874TM; 2016b www.lgcstandards-atcc.org/Products/All/25874.aspx?geo_country=gb#history accessed 1 February 2021
  32. Blokesch M, Schoolnik GK. Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog 2007; 3:e81 [View Article]
     [Google Scholar]
  33. Chun J, Huq A, Colwell RR. Analysis of 16S-23S rRNA intergenic spacer regions of Vibrio cholerae and Vibrio mimicus. Appl Environ Microbiol 1999; 65:2202–2208 [View Article]
     [Google Scholar]
  34. Rahaman Md.H, Islam T, Colwell RR, Alam M. Molecular tools in understanding the evolution of Vibrio cholerae. Front Microbiol 2015; 6: [View Article]
     [Google Scholar]
  35. Bik EM, Gouw RD, Mooi FR. DNA fingerprinting of Vibrio cholerae strains with a novel insertion sequence element: a tool to identify epidemic strains. J Clin Microbiol 1996; 34:1453–1461 [View Article]
     [Google Scholar]
  36. Nakasone N, Iwanaga M. Pili of Vibrio cholerae non-O1. Infect Immun 1990; 58:1640–1646 [View Article]
     [Google Scholar]
  37. Zinnaka Y, Carpenter CC. An enterotoxin produced by noncholera vibrios. Johns Hopkins Med J 1972; 131:403–411 [PubMed]
     [Google Scholar]
  38. Yamai S, Okitsu T, Shimada T, Katsube Y. Distribution of serogroups of Vibrio cholerae non-O1 non-O139 with specific reference to their ability to produce cholera toxin, and addition of novel serogroups. Kansenshogaku Zasshi 1997; 71:1037–1045 [View Article]
     [Google Scholar]
  39. Beltrán P, Delgado G, Navarro A, Trujillo F, Selander RK et al. Author’s correction - genetic diversity and population structure of Vibrio cholerae. J Clin Microbiol 1999b; 37:2125
     [Google Scholar]
  40. Boyd EF, Heilpern AJ, Waldor MK. Molecular analyses of a putative CTXφ precursor and evidence for independent acquisition of distinct CTXφs by toxigenic Vibrio cholerae. J Bacteriol 2000; 182:5530–5538 [View Article]
     [Google Scholar]
  41. 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; 148:1655–1666 [View Article]
     [Google Scholar]
  42. Mukhopadhyay AK, Garg S, Mitra R, Basu A, Rajendran K et al. Temporal shifts in traits of Vibrio cholerae strains isolated from hospitalized patients in Calcutta: a 3-year (1993 to 1995) analysis. J Clin Microbiol 1996; 34:2537–2543 [View Article]
     [Google Scholar]
  43. Novais RC, Coelho A, Salles CA, Vicente ACP. Toxin-co-regulated pilus cluster in non-O1, non-toxigenic Vibrio cholerae: evidence of a third allele of pilin gene. FEMS Microbiol Lett 1999; 171:49–55 [View Article]
     [Google Scholar]
  44. Morris JG, Black RE. Cholera and other vibrioses in the United States. N Engl J Med 1985; 312:343–350 [View Article] [PubMed]
     [Google Scholar]
  45. Sakazaki R, Shimada T. Serovars of Vibrio cholerae identified during 1970-1975. Jpn J Med Sci Biol 1977; 30:279–282 [View Article]
     [Google Scholar]
  46. Smith HL. Serotyping of non-cholera vibrios. J Clin Microbiol 1979; 10:85–90 [View Article] [PubMed]
     [Google Scholar]
  47. O’Shea YA, Reen FJ, Quirke AM, Boyd EF. 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 2004; 42:4657–4671 [View Article]
     [Google Scholar]
  48. Reen FJ, Boyd EF. Molecular typing of epidemic and nonepidemic Vibrio cholerae isolates and differentiation of V. cholerae and V. mimicus isolates by PCR-single-strand conformation polymorphism analysis. J Appl Microbiol 2005; 98:544–555 [View Article]
     [Google Scholar]
  49. Li M, Shimada T, Morris JG, Sulakvelidze A, Sozhamannan S. Evidence for the emergence of non-O1 and non-O139 Vibrio cholerae strains with pathogenic potential by exchange of O-antigen biosynthesis regions. Infect Immun 2002; 70:2441–2453 [View Article]
     [Google Scholar]
  50. Octavia S, Salim A, Kurniawan J, Lam C, Leung Q et al. Population structure and evolution of non-O1/non-O139 Vibrio cholerae by multilocus sequence typing. PLoS One 2013; 8:e65342 [View Article]
     [Google Scholar]
  51. Aydanian A, Tang L, Chen Y, Morris JG, Olsen P et al. Genetic relatedness of selected clinical and environmental non-O1/O139 Vibrio cholerae. Int J Infect Dis 2015; 37:152–158 [View Article]
     [Google Scholar]
  52. Chun J, Grim CJ, Hasan NA, Lee JH, Choi SY et al. Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A 2009; 106:15442–15447 [View Article]
     [Google Scholar]
  53. Watve SS, Chande AT, Rishishwar L, Mariño-Ramírez L, Jordan IK et al. Whole-genome sequences of 26 Vibrio cholerae isolates. Genome Announc 2016; 4:e01396-16 [View Article]
     [Google Scholar]
  54. Dziejman M, Serruto D, Tam VC, Sturtevant D, Diraphat P et al. Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc Natl Acad Sci U S A 2005; 102:3465–3470 [View Article]
     [Google Scholar]
  55. Farina C, Marini F, Schiaffino E, Luzzi I, Dionisi AM et al. A fatal Vibrio cholerae O37 enteritis. J Med Microbiol 2010; 59:1538–1540 [View Article]
     [Google Scholar]
  56. Yamamoto K, Takeda Y, Miwatani T, Craig JP. Evidence that a non-O1 Vibrio cholerae produces enterotoxin that is similar but not identical to cholera enterotoxin. Infect Immun 1983; 41:896–901 [View Article]
     [Google Scholar]
  57. Yamamoto K, Do Valle GRF, Xu M, Miwatani T, Honda T. Amino acids of the cholera toxin from Vibrio cholerae O37 strain S7 which differ from those of strain O1. Gene 1995; 163:155–156 [View Article]
     [Google Scholar]
  58. Safa A, Nair GB, Kong RYC. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 2010; 18:46–54 [View Article]
     [Google Scholar]
  59. Drebes Dörr NC, Blokesch M. Interbacterial competition and anti-predatory behaviour of environmental Vibrio cholerae strains. Environ Microbiol 2020; 22:4485–4504 [View Article]
     [Google Scholar]
  60. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 2006; 103:1528–1533 [View Article]
     [Google Scholar]
  61. Van der Henst C, Vanhove AS, Drebes Dörr NC, Stutzmann S, Stoudmann C et al. Molecular insights into Vibrio cholerae’s intra-amoebal host-pathogen interactions. Nat Commun 2018; 9:3460 [View Article]
     [Google Scholar]
  62. Metzger LC, Stutzmann S, Scrignari T, Van der Henst C, Matthey N et al. Independent regulation of type VI secretion in Vibrio cholerae by TfoX and TfoY. Cell Rep 2016; 15:951–958 [View Article]
     [Google Scholar]
  63. Stutzmann S, Blokesch M. Circulation of a quorum-sensing-impaired variant of Vibrio cholerae strain C6706 masks important phenotypes. mSphere 2016; 1:e00098-16 [View Article]
     [Google Scholar]
  64. Jers C, Ravikumar V, Lezyk M, Sultan A, Sjöling Å et al. The global acetylome of the human pathogen Vibrio cholerae V52 reveals lysine acetylation of major transcriptional regulators. Front Cell Infect Microbiol 2018; 7: [View Article]
     [Google Scholar]
  65. Dong TG, Mekalanos JJ. Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Res 2012; 40:7766–7775 [View Article]
     [Google Scholar]
  66. Li Z, Lu X, Wang D, Liang WL, Zhang J et al. Genomic comparison of serogroups O159 and O170 with other Vibrio cholerae serogroups. BMC Genomics 2019; 20:241 [View Article]
     [Google Scholar]
  67. Mooi FR, Bik EM. The evolution of epidemic Vibrio cholerae strains. Trends Microbiol 1997; 5:161–165 [View Article]
     [Google Scholar]
  68. Stroeher UH, Manning PA. Vibrio cholerae serotype O139: swapping genes for surface polysaccharide biosynthesis. Trends Microbiol 1997; 5:178–180 [View Article]
     [Google Scholar]
  69. González-Fraga S, Pichel M, Binsztein N, Johnson JA, Morris JG et al. Lateral gene transfer of O1 serogroup encoding genes of Vibrio cholerae. FEMS Microbiol Lett 2008; 286:32–38 [View Article]
     [Google Scholar]
  70. Chowdhury F, Mather AE, Begum YA, Asaduzzaman M, Baby N et al. Vibrio cholerae serogroup O139: isolation from cholera patients and asymptomatic household family members in Bangladesh between 2013 and 2014. PLoS Negl Trop Dis 2015; 9:e0004183 [View Article]
     [Google Scholar]
  71. Dorman MJ, Domman D, Uddin MI, Sharmin S, Afrad MH et al. High quality reference genomes for toxigenic and non-toxigenic Vibrio cholerae serogroup O139. Sci Rep 2019; 9:5865 [View Article]
     [Google Scholar]
  72. Siriphap A, Leekitcharoenphon P, Kaas RS, Theethakaew C, Aarestrup FM et al. Characterization and genetic variation of Vibrio cholerae isolated from clinical and environmental sources in Thailand. PLoS One 2017; 12:e0169324 [View Article]
     [Google Scholar]
  73. Kaper JB, Bradford HB, Roberts NC, Falkow S. Molecular epidemiology of Vibrio cholerae in the U.S. Gulf Coast. J Clin Microbiol 1982; 16:129–134 [View Article]
     [Google Scholar]
  74. Wang H, Yang C, Sun Z, Zheng W, Zhang W et al. Genomic epidemiology of Vibrio cholerae reveals the regional and global spread of two epidemic non-toxigenic lineages. PLoS Negl Trop Dis 2020; 14:e0008046 [View Article]
     [Google Scholar]
  75. Chen Y, Johnson JA, Pusch GD, Morris JG, Stine OC. The genome of non-O1 Vibrio cholerae NRT36S demonstrates the presence of pathogenic mechanisms that are distinct from those of O1 Vibrio cholerae. Infect Immun 2007; 75:2645–2647 [View Article]
     [Google Scholar]
  76. Dorman MJ, Domman D, Poklepovich T, Tolley C, Zolezzi G et al. Genomics of the Argentinian cholera epidemic elucidate the contrasting dynamics of epidemic and endemic Vibrio cholerae. Nat Commun 2020a; 11:4918 [View Article]
     [Google Scholar]
  77. Dorman MJ, Thomson NR. “Community evolution” - laboratory strains and pedigrees in the age of genomics. Microbiology 2020; 166:000869 [View Article]
     [Google Scholar]
  78. Fennell TG, Blackwell GA, Thomson NR, Dorman MJ. gbpA and chiA genes are not uniformly distributed amongst diverse Vibrio cholerae. Microb Genom 2021; 7:000594 [View Article]
     [Google Scholar]
  79. Jaskólska M, Adams DW, Blokesch M. Two defence systems eliminate plasmids from seventh pandemic Vibrio cholerae. Nature 2022; 604:323–329 [View Article]
     [Google Scholar]
  80. Dorman MJ, Domman D, Poklepovich T, Tolley C, Zolezzi G et al. Supporting data for “Genomics of the Argentinian cholera epidemic elucidate the contrasting dynamics of epidemic and endemic Vibrio cholerae”. Figshare 2020b [View Article]
     [Google Scholar]
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Vibrio cholerae O37: one of the exceptions that prove the rule
M Gen 9, 000980 (2023); https://doi.org/10.1099/mgen.0.000980
/content/journal/mgen/10.1099/mgen.0.000980
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