Genomic Dissection of the O-serogroup Global Reference Strains: Reassessing Our View of Diversity and Plasticity Between Two Chromosomes

Overview

Journal Microb Genom

Specialties Genetics
Microbiology

Date 2022 Aug 5

PMID 35930328

Authors

Kazunori Murase

Eiji Arakawa

Hidemasa Izumiya

Atsushi Iguchi

Taichiro Takemura

Taisei Kikuchi

Ichiro Nakagawa

Nicholas R Thomson

Makoto Ohnishi

Masatomo Morita

Affiliations

Soon will be listed here.

Abstract

Approximately 200 O-serogroups of have already been identified; however, only 2 serogroups, O1 and O139, are strongly related to pandemic cholera. The study of non-O1 and non-O139 strains has hitherto been limited. Nevertheless, there are other clinically and epidemiologically important serogroups causing outbreaks with cholera-like disease. Here, we report a comprehensive genome analysis of the whole set of O-serogroup reference strains to provide an overview of this important bacterial pathogen. It revealed structural diversity of the O-antigen biosynthesis gene clusters located at specific loci on chromosome 1 and 16 pairs of strains with almost identical O-antigen biosynthetic gene clusters but differing in serological patterns. This might be due to the presence of O-antigen biosynthesis-related genes at secondary loci on chromosome 2.

Citing Articles

Genomic and pathogenicity analyses to identify the causative agent from multiple serogroups of non-O1, non-O139 in foodborne outbreaks.

Morita M, Hiyoshi H, Arakawa E, Izumiya H, Ohnishi M, Ogata K Microb Genom. 2025; 11(2).

PMID: 40009544 PMC: 11865499. DOI: 10.1099/mgen.0.001364.

Characterising virulence in a nontoxigenic non-O1/non-O139 isolate imported from Vietnam.

Westerstrom P, Gabrielsen As C, Bak Dragsted U Heliyon. 2024; 10(18):e37205.

PMID: 39309771 PMC: 11416250. DOI: 10.1016/j.heliyon.2024.e37205.

serogroup O5 was responsible for the outbreak of gastroenteritis in Czechoslovakia in 1965.

Rouard C, Njamkepo E, Quilici M, Nguyen S, Knight-Connoni V, Safrankova R Microb Genom. 2024; 10(9).

PMID: 39235832 PMC: 11561587. DOI: 10.1099/mgen.0.001282.

Genomic epidemiology reveals multidrug resistant plasmid spread between Vibrio cholerae lineages in Yemen.

Lassalle F, Al-Shalali S, Al-Hakimi M, Njamkepo E, Bashir I, Dorman M Nat Microbiol. 2023; 8(10):1787-1798.

PMID: 37770747 PMC: 10539172. DOI: 10.1038/s41564-023-01472-1.

Advances in cholera research: from molecular biology to public health initiatives.

Walton M, Cubillejo I, Nag D, Withey J Front Microbiol. 2023; 14:1178538.

PMID: 37283925 PMC: 10239892. DOI: 10.3389/fmicb.2023.1178538.

References

Yamasaki S, Shimizu T, Hoshino K, Ho S, Shimada T, Nair G . The genes responsible for O-antigen synthesis of vibrio cholerae O139 are closely related to those of vibrio cholerae O22. Gene. 1999; 237(2):321-32. DOI: 10.1016/s0378-1119(99)00344-3. View

Iguchi A, Iyoda S, Kikuchi T, Ogura Y, Katsura K, Ohnishi M . A complete view of the genetic diversity of the Escherichia coli O-antigen biosynthesis gene cluster. DNA Res. 2014; 22(1):101-7. PMC: 4379981. DOI: 10.1093/dnares/dsu043. View

Page A, Cummins C, Hunt M, Wong V, Reuter S, Holden M . Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015; 31(22):3691-3. PMC: 4817141. DOI: 10.1093/bioinformatics/btv421. View

Morita M, Yamamoto S, Hiyoshi H, Kodama T, Okura M, Arakawa E . Horizontal gene transfer of a genetic island encoding a type III secretion system distributed in Vibrio cholerae. Microbiol Immunol. 2013; 57(5):334-9. DOI: 10.1111/1348-0421.12039. View

Labbate M, Orata F, Petty N, Jayatilleke N, King W, Kirchberger P . A genomic island in Vibrio cholerae with VPI-1 site-specific recombination characteristics contains CRISPR-Cas and type VI secretion modules. Sci Rep. 2016; 6:36891. PMC: 5109276. DOI: 10.1038/srep36891. View

Marin M, Vicente A . Architecture of the superintegron in Vibrio cholerae: identification of core and unique genes. F1000Res. 2015; 2:63. PMC: 4032106. DOI: 10.12688/f1000research.2-63.v1. View

Egan E, Waldor M . Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell. 2003; 114(4):521-30. DOI: 10.1016/s0092-8674(03)00611-1. View

Meibom K, Blokesch M, Dolganov N, Wu C, Schoolnik G . Chitin induces natural competence in Vibrio cholerae. Science. 2005; 310(5755):1824-7. DOI: 10.1126/science.1120096. View

Emms D, Kelly S . OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019; 20(1):238. PMC: 6857279. DOI: 10.1186/s13059-019-1832-y. View

10.

Metzger L, Blokesch M . Regulation of competence-mediated horizontal gene transfer in the natural habitat of Vibrio cholerae. Curr Opin Microbiol. 2015; 30:1-7. DOI: 10.1016/j.mib.2015.10.007. View

11.

Blokesch M, Schoolnik G . Serogroup conversion of Vibrio cholerae in aquatic reservoirs. PLoS Pathog. 2007; 3(6):e81. PMC: 1891326. DOI: 10.1371/journal.ppat.0030081. View

12.

Juhas M, van der Meer J, Gaillard M, Harding R, Hood D, Crook D . Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol Rev. 2009; 33(2):376-93. PMC: 2704930. DOI: 10.1111/j.1574-6976.2008.00136.x. View

13.

Chin C, Alexander D, Marks P, Klammer A, Drake J, Heiner C . Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods. 2013; 10(6):563-9. DOI: 10.1038/nmeth.2474. View

14.

Coil D, Jospin G, Darling A . A5-miseq: an updated pipeline to assemble microbial genomes from Illumina MiSeq data. Bioinformatics. 2014; 31(4):587-9. DOI: 10.1093/bioinformatics/btu661. View

15.

Donati C, Hiller N, Tettelin H, Muzzi A, Croucher N, Angiuoli S . Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol. 2010; 11(10):R107. PMC: 3218663. DOI: 10.1186/gb-2010-11-10-r107. View

16.

Tobin-DAngelo M, Smith A, Bulens S, Thomas S, Hodel M, Izumiya H . Severe diarrhea caused by cholera toxin-producing vibrio cholerae serogroup O75 infections acquired in the southeastern United States. Clin Infect Dis. 2008; 47(8):1035-40. DOI: 10.1086/591973. View

17.

Inouye M, Dashnow H, Raven L, Schultz M, Pope B, Tomita T . SRST2: Rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 2014; 6(11):90. PMC: 4237778. DOI: 10.1186/s13073-014-0090-6. View

18.

Udden S, Hasan Zahid M, Biswas K, Ahmad Q, Cravioto A, Nair G . Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc Natl Acad Sci U S A. 2008; 105(33):11951-6. PMC: 2575248. DOI: 10.1073/pnas.0805560105. View

19.

Keymer D, Miller M, Schoolnik G, Boehm A . Genomic and phenotypic diversity of coastal Vibrio cholerae strains is linked to environmental factors. Appl Environ Microbiol. 2007; 73(11):3705-14. PMC: 1932678. DOI: 10.1128/AEM.02736-06. View

20.

Ryan E . The cholera pandemic, still with us after half a century: time to rethink. PLoS Negl Trop Dis. 2011; 5(1):e1003. PMC: 3026764. DOI: 10.1371/journal.pntd.0001003. View