Tweet
mBio. Evolutionary Dynamics of Vibrio cholerae O1 following a Single-Source Introduction to Haiti
[Source: mBio, full page: (LINK). Abstract, edited.]
Evolutionary Dynamics of Vibrio cholerae O1 following a Single-Source Introduction to Haiti
Lee S. Katz <SUP>a</SUP>, Aaron Petkau<SUP>b</SUP>, John Beaulaurier<SUP>c</SUP>, Shaun Tyler<SUP>b</SUP>, Elena S. Antonova<SUP>d</SUP>, Maryann A. Turnsek<SUP>a</SUP>, Yan Guo<SUP>e</SUP>, Susana Wang <SUP>e</SUP>, Ellen E. Paxinos<SUP>e</SUP>, Fabini Orata <SUP>f</SUP>, Lori M. Gladney<SUP>a</SUP>, Steven Stroika<SUP>a</SUP>, Jason P. Folster<SUP>a</SUP>, Lori Rowe<SUP>a</SUP>, Molly M. Freeman<SUP>a</SUP>, Natalie Knox<SUP>b</SUP>, Mike Frace<SUP>a</SUP>, Jacques Boncy<SUP>g</SUP>, Morag Graham<SUP>b</SUP>, Brian K. Hammer<SUP>d</SUP>, Yan Boucher<SUP>f</SUP>, Ali Bashir<SUP>c</SUP>, William P. Hanage<SUP>h</SUP>, Gary Van Domselaar<SUP>b</SUP>, Cheryl L. Tarr<SUP>a</SUP>
<SUP></SUP>
Centers for Disease Control and Prevention, Atlanta, Georgia, USA<SUP>a </SUP>National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada<SUP>b </SUP>Department of Genetics and Genomics Sciences, Mount Sinai School of Medicine, New York, New York, USA<SUP>c </SUP>School of Biology, Georgia Institute of Technology, Atlanta, Georgia, USA<SUP>d </SUP>Pacific Biosciences, Menlo Park, California, USA<SUP>e </SUP>Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada<SUP>f </SUP>National Public Health Laboratory, Port-au-Prince, Haiti<SUP>g </SUP>Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard University, Boston, Massachusetts, USA<SUP>h</SUP>
<SUP></SUP>
Address correspondence to Cheryl L. Tarr, ctarr{at}cdc.gov.
Editor John Mekalanos, Harvard Medical School
ABSTRACT
Prior to the epidemic that emerged in Haiti in October of 2010, cholera had not been documented in this country. After its introduction, a strain of Vibrio cholerae O1 spread rapidly throughout Haiti, where it caused over 600,000 cases of disease and >7,500 deaths in the first two years of the epidemic. We applied whole-genome sequencing to a temporal series of V. cholerae isolates from Haiti to gain insight into the mode and tempo of evolution in this isolated population of V. cholerae O1. Phylogenetic and Bayesian analyses supported the hypothesis that all isolates in the sample set diverged from a common ancestor within a time frame that is consistent with epidemiological observations. A pangenome analysis showed nearly homogeneous genomic content, with no evidence of gene acquisition among Haiti isolates. Nine nearly closed genomes assembled from continuous-long-read data showed evidence of genome rearrangements and supported the observation of no gene acquisition among isolates. Thus, intrinsic mutational processes can account for virtually all of the observed genetic polymorphism, with no demonstrable contribution from horizontal gene transfer (HGT). Consistent with this, the 12 Haiti isolates tested by laboratory HGT assays were severely impaired for transformation, although unlike previously characterized noncompetent V. cholerae isolates, each expressed hapR and possessed a functional quorum-sensing system. Continued monitoring ofV. cholerae in Haiti will illuminate the processes influencing the origin and fate of genome variants, which will facilitate interpretation of genetic variation in future epidemics.
IMPORTANCE
Vibrio cholerae is the cause of substantial morbidity and mortality worldwide, with over three million cases of disease each year. An understanding of the mode and rate of evolutionary change is critical for proper interpretation of genome sequence data and attribution of outbreak sources. The Haiti epidemic provides an unprecedented opportunity to study an isolated, single-source outbreak of Vibrio cholerae O1 over an established time frame. By using multiple approaches to assay genetic variation, we found no evidence that the Haiti strain has acquired any genes by horizontal gene transfer, an observation that led us to discover that it is also poorly transformable. We have found no evidence that environmental strains have played a role in the evolution of the outbreak strain.
FOOTNOTES
Citation Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CL. 2013. Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. mBio 4(4):e00398-13. doi:10.1128/mBio.00398-13.
Received 24 May 2013 Accepted 3 June 2013 Published 2 July 2013
Copyright ? 2013 Katz et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
-
-------
Evolutionary Dynamics of Vibrio cholerae O1 following a Single-Source Introduction to Haiti
Lee S. Katz <SUP>a</SUP>, Aaron Petkau<SUP>b</SUP>, John Beaulaurier<SUP>c</SUP>, Shaun Tyler<SUP>b</SUP>, Elena S. Antonova<SUP>d</SUP>, Maryann A. Turnsek<SUP>a</SUP>, Yan Guo<SUP>e</SUP>, Susana Wang <SUP>e</SUP>, Ellen E. Paxinos<SUP>e</SUP>, Fabini Orata <SUP>f</SUP>, Lori M. Gladney<SUP>a</SUP>, Steven Stroika<SUP>a</SUP>, Jason P. Folster<SUP>a</SUP>, Lori Rowe<SUP>a</SUP>, Molly M. Freeman<SUP>a</SUP>, Natalie Knox<SUP>b</SUP>, Mike Frace<SUP>a</SUP>, Jacques Boncy<SUP>g</SUP>, Morag Graham<SUP>b</SUP>, Brian K. Hammer<SUP>d</SUP>, Yan Boucher<SUP>f</SUP>, Ali Bashir<SUP>c</SUP>, William P. Hanage<SUP>h</SUP>, Gary Van Domselaar<SUP>b</SUP>, Cheryl L. Tarr<SUP>a</SUP>
<SUP></SUP>
Centers for Disease Control and Prevention, Atlanta, Georgia, USA<SUP>a </SUP>National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada<SUP>b </SUP>Department of Genetics and Genomics Sciences, Mount Sinai School of Medicine, New York, New York, USA<SUP>c </SUP>School of Biology, Georgia Institute of Technology, Atlanta, Georgia, USA<SUP>d </SUP>Pacific Biosciences, Menlo Park, California, USA<SUP>e </SUP>Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada<SUP>f </SUP>National Public Health Laboratory, Port-au-Prince, Haiti<SUP>g </SUP>Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard University, Boston, Massachusetts, USA<SUP>h</SUP>
<SUP></SUP>
Address correspondence to Cheryl L. Tarr, ctarr{at}cdc.gov.
Editor John Mekalanos, Harvard Medical School
ABSTRACT
Prior to the epidemic that emerged in Haiti in October of 2010, cholera had not been documented in this country. After its introduction, a strain of Vibrio cholerae O1 spread rapidly throughout Haiti, where it caused over 600,000 cases of disease and >7,500 deaths in the first two years of the epidemic. We applied whole-genome sequencing to a temporal series of V. cholerae isolates from Haiti to gain insight into the mode and tempo of evolution in this isolated population of V. cholerae O1. Phylogenetic and Bayesian analyses supported the hypothesis that all isolates in the sample set diverged from a common ancestor within a time frame that is consistent with epidemiological observations. A pangenome analysis showed nearly homogeneous genomic content, with no evidence of gene acquisition among Haiti isolates. Nine nearly closed genomes assembled from continuous-long-read data showed evidence of genome rearrangements and supported the observation of no gene acquisition among isolates. Thus, intrinsic mutational processes can account for virtually all of the observed genetic polymorphism, with no demonstrable contribution from horizontal gene transfer (HGT). Consistent with this, the 12 Haiti isolates tested by laboratory HGT assays were severely impaired for transformation, although unlike previously characterized noncompetent V. cholerae isolates, each expressed hapR and possessed a functional quorum-sensing system. Continued monitoring ofV. cholerae in Haiti will illuminate the processes influencing the origin and fate of genome variants, which will facilitate interpretation of genetic variation in future epidemics.
IMPORTANCE
Vibrio cholerae is the cause of substantial morbidity and mortality worldwide, with over three million cases of disease each year. An understanding of the mode and rate of evolutionary change is critical for proper interpretation of genome sequence data and attribution of outbreak sources. The Haiti epidemic provides an unprecedented opportunity to study an isolated, single-source outbreak of Vibrio cholerae O1 over an established time frame. By using multiple approaches to assay genetic variation, we found no evidence that the Haiti strain has acquired any genes by horizontal gene transfer, an observation that led us to discover that it is also poorly transformable. We have found no evidence that environmental strains have played a role in the evolution of the outbreak strain.
FOOTNOTES
Citation Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CL. 2013. Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. mBio 4(4):e00398-13. doi:10.1128/mBio.00398-13.
Received 24 May 2013 Accepted 3 June 2013 Published 2 July 2013
Copyright ? 2013 Katz et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
-
-------