Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection

ABSTRACT Phylodynamic analysis of genome-wide single-nucleotide polymorphism (SNP) data is a powerful tool to investigate underlying evolutionary processes of bacterial epidemics. The method was applied to investigate a collection of 65 clinical and environmental isolates of Vibrio cholerae from Hai...

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Autores principales: Taj Azarian, Afsar Ali, Judith A. Johnson, David Mohr, Mattia Prosperi, Nazle M. Veras, Mohammed Jubair, Samantha L. Strickland, Mohammad H. Rashid, Meer T. Alam, Thomas A. Weppelmann, Lee S. Katz, Cheryl L. Tarr, Rita R. Colwell, J. Glenn Morris, Marco Salemi
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Publicado: American Society for Microbiology 2014
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spelling oai:doaj.org-article:804f55a9a3d049a7867db3f81f4d37802021-11-15T15:47:03ZPhylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection10.1128/mBio.01824-142150-7511https://doaj.org/article/804f55a9a3d049a7867db3f81f4d37802014-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01824-14https://doaj.org/toc/2150-7511ABSTRACT Phylodynamic analysis of genome-wide single-nucleotide polymorphism (SNP) data is a powerful tool to investigate underlying evolutionary processes of bacterial epidemics. The method was applied to investigate a collection of 65 clinical and environmental isolates of Vibrio cholerae from Haiti collected between 2010 and 2012. Characterization of isolates recovered from environmental samples identified a total of four toxigenic V. cholerae O1 isolates, four non-O1/O139 isolates, and a novel nontoxigenic V. cholerae O1 isolate with the classical tcpA gene. Phylogenies of strains were inferred from genome-wide SNPs using coalescent-based demographic models within a Bayesian framework. A close phylogenetic relationship between clinical and environmental toxigenic V. cholerae O1 strains was observed. As cholera spread throughout Haiti between October 2010 and August 2012, the population size initially increased and then fluctuated over time. Selection analysis along internal branches of the phylogeny showed a steady accumulation of synonymous substitutions and a progressive increase of nonsynonymous substitutions over time, suggesting diversification likely was driven by positive selection. Short-term accumulation of nonsynonymous substitutions driven by selection may have significant implications for virulence, transmission dynamics, and even vaccine efficacy. IMPORTANCE Cholera, a dehydrating diarrheal disease caused by toxigenic strains of the bacterium Vibrio cholerae, emerged in 2010 in Haiti, a country where there were no available records on cholera over the past 100 years. While devastating in terms of morbidity and mortality, the outbreak provided a unique opportunity to study the evolutionary dynamics of V. cholerae and its environmental presence. The present study expands on previous work and provides an in-depth phylodynamic analysis inferred from genome-wide single nucleotide polymorphisms of clinical and environmental strains from dispersed geographic settings in Haiti over a 2-year period. Our results indicate that even during such a short time scale, V. cholerae in Haiti has undergone evolution and diversification driven by positive selection, which may have implications for understanding the global clinical and epidemiological patterns of the disease. Furthermore, the continued presence of the epidemic strain in Haitian aquatic environments has implications for transmission.Taj AzarianAfsar AliJudith A. JohnsonDavid MohrMattia ProsperiNazle M. VerasMohammed JubairSamantha L. StricklandMohammad H. RashidMeer T. AlamThomas A. WeppelmannLee S. KatzCheryl L. TarrRita R. ColwellJ. Glenn MorrisMarco SalemiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 6 (2014)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Taj Azarian
Afsar Ali
Judith A. Johnson
David Mohr
Mattia Prosperi
Nazle M. Veras
Mohammed Jubair
Samantha L. Strickland
Mohammad H. Rashid
Meer T. Alam
Thomas A. Weppelmann
Lee S. Katz
Cheryl L. Tarr
Rita R. Colwell
J. Glenn Morris
Marco Salemi
Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
description ABSTRACT Phylodynamic analysis of genome-wide single-nucleotide polymorphism (SNP) data is a powerful tool to investigate underlying evolutionary processes of bacterial epidemics. The method was applied to investigate a collection of 65 clinical and environmental isolates of Vibrio cholerae from Haiti collected between 2010 and 2012. Characterization of isolates recovered from environmental samples identified a total of four toxigenic V. cholerae O1 isolates, four non-O1/O139 isolates, and a novel nontoxigenic V. cholerae O1 isolate with the classical tcpA gene. Phylogenies of strains were inferred from genome-wide SNPs using coalescent-based demographic models within a Bayesian framework. A close phylogenetic relationship between clinical and environmental toxigenic V. cholerae O1 strains was observed. As cholera spread throughout Haiti between October 2010 and August 2012, the population size initially increased and then fluctuated over time. Selection analysis along internal branches of the phylogeny showed a steady accumulation of synonymous substitutions and a progressive increase of nonsynonymous substitutions over time, suggesting diversification likely was driven by positive selection. Short-term accumulation of nonsynonymous substitutions driven by selection may have significant implications for virulence, transmission dynamics, and even vaccine efficacy. IMPORTANCE Cholera, a dehydrating diarrheal disease caused by toxigenic strains of the bacterium Vibrio cholerae, emerged in 2010 in Haiti, a country where there were no available records on cholera over the past 100 years. While devastating in terms of morbidity and mortality, the outbreak provided a unique opportunity to study the evolutionary dynamics of V. cholerae and its environmental presence. The present study expands on previous work and provides an in-depth phylodynamic analysis inferred from genome-wide single nucleotide polymorphisms of clinical and environmental strains from dispersed geographic settings in Haiti over a 2-year period. Our results indicate that even during such a short time scale, V. cholerae in Haiti has undergone evolution and diversification driven by positive selection, which may have implications for understanding the global clinical and epidemiological patterns of the disease. Furthermore, the continued presence of the epidemic strain in Haitian aquatic environments has implications for transmission.
format article
author Taj Azarian
Afsar Ali
Judith A. Johnson
David Mohr
Mattia Prosperi
Nazle M. Veras
Mohammed Jubair
Samantha L. Strickland
Mohammad H. Rashid
Meer T. Alam
Thomas A. Weppelmann
Lee S. Katz
Cheryl L. Tarr
Rita R. Colwell
J. Glenn Morris
Marco Salemi
author_facet Taj Azarian
Afsar Ali
Judith A. Johnson
David Mohr
Mattia Prosperi
Nazle M. Veras
Mohammed Jubair
Samantha L. Strickland
Mohammad H. Rashid
Meer T. Alam
Thomas A. Weppelmann
Lee S. Katz
Cheryl L. Tarr
Rita R. Colwell
J. Glenn Morris
Marco Salemi
author_sort Taj Azarian
title Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
title_short Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
title_full Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
title_fullStr Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
title_full_unstemmed Phylodynamic Analysis of Clinical and Environmental <named-content content-type="genus-species">Vibrio cholerae</named-content> Isolates from Haiti Reveals Diversification Driven by Positive Selection
title_sort phylodynamic analysis of clinical and environmental <named-content content-type="genus-species">vibrio cholerae</named-content> isolates from haiti reveals diversification driven by positive selection
publisher American Society for Microbiology
publishDate 2014
url https://doaj.org/article/804f55a9a3d049a7867db3f81f4d3780
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