Phylogenetic Diversity of Vibrio cholerae Associated with Endemic Cholera in Mexico from 1991 to 2008

doi:10.1128/mBio.02160-15

. 2016 Mar 15;7(2):e02160.

doi: 10.1128/mBio.02160-15.

Phylogenetic Diversity of Vibrio cholerae Associated with Endemic Cholera in Mexico from 1991 to 2008

Seon Young Choi ¹, Shah M Rashed ², Nur A Hasan ³, Munirul Alam ⁴, Tarequl Islam ⁴, Abdus Sadique ⁴, Fatema-Tuz Johura ⁴, Mark Eppinger ⁵, Jacques Ravel ⁶, Anwar Huq ⁷, Alejandro Cravioto ⁸, Rita R Colwell ⁹

Affiliations

¹ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA CosmosID, Inc., Rockville, Maryland, USA.
² Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA.
³ CosmosID, Inc., Rockville, Maryland, USA Center of Bioinformatics and Computational Biology, University of Maryland Institute of Advanced Computer Studies, University of Maryland, College Park, Maryland, USA.
⁴ International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh.
⁵ Department of Biology and South Texas Center for Emerging Infectious Diseases (STCEID), University of Texas at San Antonio, San Antonio, Texas, USA.
⁶ Institute for Genome Sciences (IGS), University of Maryland, School of Medicine, Baltimore, Maryland, USA.
⁷ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA Maryland Institute of Applied Environmental Health, University of Maryland, College Park, Maryland, USA.
⁸ Global Evaluative Sciences USA, Inc., Seattle, Washington, USA.
⁹ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA CosmosID, Inc., Rockville, Maryland, USA Center of Bioinformatics and Computational Biology, University of Maryland Institute of Advanced Computer Studies, University of Maryland, College Park, Maryland, USA Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA rcolwell@umiacs.umd.edu.

PMID: 26980836
PMCID: PMC4807371
DOI: 10.1128/mBio.02160-15

Phylogenetic Diversity of Vibrio cholerae Associated with Endemic Cholera in Mexico from 1991 to 2008

Seon Young Choi et al. mBio. 2016.

. 2016 Mar 15;7(2):e02160.

doi: 10.1128/mBio.02160-15.

Authors

Seon Young Choi ¹, Shah M Rashed ², Nur A Hasan ³, Munirul Alam ⁴, Tarequl Islam ⁴, Abdus Sadique ⁴, Fatema-Tuz Johura ⁴, Mark Eppinger ⁵, Jacques Ravel ⁶, Anwar Huq ⁷, Alejandro Cravioto ⁸, Rita R Colwell ⁹

Affiliations

¹ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA CosmosID, Inc., Rockville, Maryland, USA.
² Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA.
³ CosmosID, Inc., Rockville, Maryland, USA Center of Bioinformatics and Computational Biology, University of Maryland Institute of Advanced Computer Studies, University of Maryland, College Park, Maryland, USA.
⁴ International Centre for Diarrhoeal Disease Research, Bangladesh (icddr,b), Dhaka, Bangladesh.
⁵ Department of Biology and South Texas Center for Emerging Infectious Diseases (STCEID), University of Texas at San Antonio, San Antonio, Texas, USA.
⁶ Institute for Genome Sciences (IGS), University of Maryland, School of Medicine, Baltimore, Maryland, USA.
⁷ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA Maryland Institute of Applied Environmental Health, University of Maryland, College Park, Maryland, USA.
⁸ Global Evaluative Sciences USA, Inc., Seattle, Washington, USA.
⁹ Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland, USA CosmosID, Inc., Rockville, Maryland, USA Center of Bioinformatics and Computational Biology, University of Maryland Institute of Advanced Computer Studies, University of Maryland, College Park, Maryland, USA Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA rcolwell@umiacs.umd.edu.

PMID: 26980836
PMCID: PMC4807371
DOI: 10.1128/mBio.02160-15

Abstract

An outbreak of cholera occurred in 1991 in Mexico, where it had not been reported for more than a century and is now endemic. Vibrio cholerae O1 prototype El Tor and classical strains coexist with altered El Tor strains (1991 to 1997). Nontoxigenic (CTX(-)) V. cholerae El Tor dominated toxigenic (CTX(+)) strains (2001 to 2003), but V. cholerae CTX(+) variant El Tor was isolated during 2004 to 2008, outcompeting CTX(-) V. cholerae. Genomes of six Mexican V. cholerae O1 strains isolated during 1991 to 2008 were sequenced and compared with both contemporary and archived strains of V. cholerae. Three were CTX(+) El Tor, two were CTX(-) El Tor, and the remaining strain was a CTX(+) classical isolate. Whole-genome sequence analysis showed the six isolates belonged to five distinct phylogenetic clades. One CTX(-) isolate is ancestral to the 6th and 7th pandemic CTX(+) V. cholerae isolates. The other CTX(-) isolate joined with CTX(-) non-O1/O139 isolates from Haiti and seroconverted O1 isolates from Brazil and Amazonia. One CTX(+) isolate was phylogenetically placed with the sixth pandemic classical clade and the V. cholerae O395 classical reference strain. Two CTX(+) El Tor isolates possessing intact Vibrio seventh pandemic island II (VSP-II) are related to hybrid El Tor isolates from Mozambique and Bangladesh. The third CTX(+) El Tor isolate contained West African-South American (WASA) recombination in VSP-II and showed relatedness to isolates from Peru and Brazil. Except for one isolate, all Mexican isolates lack SXT/R391 integrative conjugative elements (ICEs) and sensitivity to selected antibiotics, with one isolate resistant to streptomycin. No isolates were related to contemporary isolates from Asia, Africa, or Haiti, indicating phylogenetic diversity.

Importance: Sequencing of genomes of V. cholerae is critical if genetic changes occurring over time in the circulating population of an area of endemicity are to be understood. Although cholera outbreaks occurred rarely in Mexico prior to the 1990s, genetically diverse V. cholerae O1 strains were isolated between 1991 and 2008. Despite the lack of strong evidence, the notion that cholera was transmitted from Africa to Latin America has been proposed in the literature. In this study, we have applied whole-genome sequence analysis to a set of 124 V. cholerae strains, including six Mexican isolates, to determine their phylogenetic relationships. Phylogenetic analysis indicated the six V. cholerae O1 isolates belong to five phylogenetic clades: i.e., basal, nontoxigenic, classical, El Tor, and hybrid El Tor. Thus, the results of phylogenetic analysis, coupled with CTXφ array and antibiotic susceptibility, do not support single-source transmission of cholera to Mexico from African countries. The association of indigenous populations of V. cholerae that has been observed in this study suggests it plays a significant role in the dynamics of cholera in Mexico.

PubMed Disclaimer

Figures

FIG 1

FIG 1

Vibrio pathogenicity island 1 (VPI-1) of V. cholerae O1 strains isolated in Mexico and reference El Tor strain N16961. Mexican CTX⁻ V. cholerae O1 strain CP1037 contains GI-47 in the upstream region of VPI-1.

FIG 2

FIG 2

Vibrio seventh pandemic island II (VSP-II) of V. cholerae O1 strains isolated in Mexico and Brazil. VSP-II of hybrid V. cholerae O1 El Tor (CP1032 and CP1033) was similar to that of reference El Tor N16961. However, it is different from those of prototype El Tor isolates (CP1030, ICE224, and INDRE 91/1) in Mexico and Brazil.

FIG 3

FIG 3

O antigen biosynthetic genes of V. cholerae O1 strains CP1035, TM11079, and N16961. The wav and wb* gene clusters of CP1035 are homologous to those of TM11079 and different from those of reference El Tor N16961.

FIG 4

FIG 4

Neighbor-joining trees showing phylogenetic relationships of 124 V. cholerae genomes based on 905 orthologs of protein-coding genes (~897,461 bp). The two V. cholerae non-O1/O139 strains (HE09 and HE16) isolated from surface water during the 2010 cholera epidemic in Haiti were used as an outgroup of the tree, and bootstrap values are percentages of 1,000 replications. Mexican V. cholerae O1 strains are shown in blue, indicating the distribution among five distinct phylogenetic clades. The top node represents the genomes of isolates from Haiti, Bangladesh, Nepal, the United States, Cameroon, South Africa, the Russian Federation, Zimbabwe, and the Dominican Republic obtained between 2005 and 2011.

See this image and copyright information in PMC

Comment in

Sustained Local Diversity of Vibrio cholerae O1 Biotypes in a Previously Cholera-Free Country.
Boucher Y. Boucher Y. mBio. 2016 May 3;7(3):e00570-16. doi: 10.1128/mBio.00570-16. mBio. 2016. PMID: 27143391 Free PMC article.

References

1. Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363:223–233. doi: 10.1016/S0140-6736(03)15328-7. - DOI - PubMed
1. Kaper JB, Morris JG Jr, Levine MM. 1995. Cholera. Clin Microbiol Rev 8:48–86. - PMC - PubMed
1. Sepúlveda J, Valdespino JL, García-García L. 2006. Cholera in Mexico: the paradoxical benefits of the last pandemic. Int J Infect Dis 10:4–13. doi: 10.1016/j.ijid.200505005. - DOI - PubMed
1. Olsvik O. 1992. The cholera epidemic in Latin America. Tidsskr Nor Laegeforen 112:1843–1846. - PubMed
1. Alam M, Nusrin S, Islam A, Bhuiyan NA, Rahim N, Delgado G, Morales R, Mendez JL, Navarro A, Gil AI, Watanabe H, Morita M, Nair GB, Cravioto A. 2010. Cholera between 1991 and 1997 in Mexico was associated with infection by classical, El Tor, and El Tor variants of Vibrio cholerae. J Clin Microbiol 48:3666–3674. doi: 10.1128/JCM.00866-10. - DOI - PMC - PubMed

Publication types

Actions
Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

Grants and funding

HHSN2722009000/PHS HHS/United States

LinkOut - more resources

Full Text Sources
Other Literature Sources
- scite Smart Citations
Medical
- MedlinePlus Health Information
Molecular Biology Databases
- SILVA

[1] Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363:223–233. doi: 10.1016/S0140-6736(03)15328-7. - DOI - PubMed

[2] Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363:223–233. doi: 10.1016/S0140-6736(03)15328-7. - DOI - PubMed

[3] Kaper JB, Morris JG Jr, Levine MM. 1995. Cholera. Clin Microbiol Rev 8:48–86. - PMC - PubMed

[4] Kaper JB, Morris JG Jr, Levine MM. 1995. Cholera. Clin Microbiol Rev 8:48–86. - PMC - PubMed

[5] Sepúlveda J, Valdespino JL, García-García L. 2006. Cholera in Mexico: the paradoxical benefits of the last pandemic. Int J Infect Dis 10:4–13. doi: 10.1016/j.ijid.200505005. - DOI - PubMed

[6] Sepúlveda J, Valdespino JL, García-García L. 2006. Cholera in Mexico: the paradoxical benefits of the last pandemic. Int J Infect Dis 10:4–13. doi: 10.1016/j.ijid.200505005. - DOI - PubMed

[7] Olsvik O. 1992. The cholera epidemic in Latin America. Tidsskr Nor Laegeforen 112:1843–1846. - PubMed

[8] Olsvik O. 1992. The cholera epidemic in Latin America. Tidsskr Nor Laegeforen 112:1843–1846. - PubMed

[9] Alam M, Nusrin S, Islam A, Bhuiyan NA, Rahim N, Delgado G, Morales R, Mendez JL, Navarro A, Gil AI, Watanabe H, Morita M, Nair GB, Cravioto A. 2010. Cholera between 1991 and 1997 in Mexico was associated with infection by classical, El Tor, and El Tor variants of Vibrio cholerae. J Clin Microbiol 48:3666–3674. doi: 10.1128/JCM.00866-10. - DOI - PMC - PubMed

[10] Alam M, Nusrin S, Islam A, Bhuiyan NA, Rahim N, Delgado G, Morales R, Mendez JL, Navarro A, Gil AI, Watanabe H, Morita M, Nair GB, Cravioto A. 2010. Cholera between 1991 and 1997 in Mexico was associated with infection by classical, El Tor, and El Tor variants of Vibrio cholerae. J Clin Microbiol 48:3666–3674. doi: 10.1128/JCM.00866-10. - DOI - PMC - PubMed

Account

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Phylogenetic Diversity of Vibrio cholerae Associated with Endemic Cholera in Mexico from 1991 to 2008

Affiliations

Phylogenetic Diversity of Vibrio cholerae Associated with Endemic Cholera in Mexico from 1991 to 2008

Authors

Affiliations

Abstract

Figures

Comment in

References

Publication types

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Molecular Biology Databases