Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104
Abstract
It has been 30 years since the initial emergence and subsequent rapid global spread of multidrug-resistantSalmonella entericaserovar Typhimurium DT104 (MDR DT104). Nonetheless, its origin and transmission route have never been revealed. We used whole-genome sequencing (WGS) and temporally structured sequence analysis within a Bayesian framework to reconstruct temporal and spatial phylogenetic trees and estimate the rates of mutation and divergence times of 315S. Moreover, typhimurium DT104 isolates sampled from 1969 to 2012 from 21 countries on six continents. DT104 was estimated to have emerged initially as antimicrobial susceptible in ~1948 (95% credible interval [CI], 1934 to 1962) and later became MDR DT104 in ~1972 (95% CI, 1972 to 1988) through horizontal transfer of the 13-kbSalmonellagenomic island 1 (SGI1) MDR region into susceptible strains already containing SGI1. This was followed by multiple transmission events, initially from central Europe and later between several European countries. An independent transmission to the United States and another to Japan occurred, and from there MDR DT104 was probably transmitted to Taiwan and Canada. An independent acquisition of resistance genes took place in Thailand in ~1975 (95% CI, 1975 to 1990). In Denmark, WGS analysis provided evidence for transmission of the organism between herds of animals. Interestingly,more »
- Authors:
-
[6];
- Technical Univ. of Denmark, Lyngby (Denmark). National Food Inst.. Research Group for Genomic Epidemiology; Technical Univ. of Denmark, Lyngby (Denmark). Dept. of System Biology. Center for Biological Sequence Analysis
- Technical Univ. of Denmark, Lyngby (Denmark). National Food Inst.. Research Group for Genomic Epidemiology
- Inst. Pasteur, Paris (France). Centre National de Reference des Salmonella. Unite des Bacteries Pathogenes Enteriques
- Technical Univ. of Denmark, Soborg (Denmark). National Food Inst.
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division. Comparative Genomics Group
- Technical Univ. of Denmark, Lyngby (Denmark). Dept. of System Biology. Center for Biological Sequence Analysis; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division. Comparative Genomics Group
- Technical Univ. of Denmark, Lyngby (Denmark). Dept. of System Biology. Center for Biological Sequence Analysis
- Univ. of Oxford (United Kingdom). John Radcliffe Hospital. Nuffield Dept. of Medicine
- Univ. of Oxford (United Kingdom). John Radcliffe Hospital. Nuffield Dept. of Medicine; Univ. of Oxford (United Kingdom). Wellcome Trust Centre for Human Genetics
- Publication Date:
- Research Org.:
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- Center for Genomic Epidemiology (CGE) (Denmark); Wellcome Trust (United Kingdom); The Royal Society (United Kingdom); USDOE
- OSTI Identifier:
- 1185725
- Alternate Identifier(s):
- OSTI ID: 1286993
- Grant/Contract Number:
- 09-067103/DSF; 101237/Z/13/Z; AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied and Environmental Microbiology
- Additional Journal Information:
- Journal Volume: 82; Journal Issue: 8; Journal ID: ISSN 0099-2240
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Whole genome sequence typing; SNPs; Salmonella; DT104; evolution
Citation Formats
Leekitcharoenphon, Pimlapas, Hendriksen, Rene S., Le Hello, Simon, Weill, François-Xavier, Baggesen, Dorte Lau, Jun, Se-Ran, Ussery, David W., Lund, Ole, Crook, Derrick W., Wilson, Daniel J., and Aarestrup, Frank M. Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104. United States: N. p., 2016.
Web. doi:10.1128/AEM.03821-15.
Leekitcharoenphon, Pimlapas, Hendriksen, Rene S., Le Hello, Simon, Weill, François-Xavier, Baggesen, Dorte Lau, Jun, Se-Ran, Ussery, David W., Lund, Ole, Crook, Derrick W., Wilson, Daniel J., & Aarestrup, Frank M. Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104. United States. https://doi.org/10.1128/AEM.03821-15
Leekitcharoenphon, Pimlapas, Hendriksen, Rene S., Le Hello, Simon, Weill, François-Xavier, Baggesen, Dorte Lau, Jun, Se-Ran, Ussery, David W., Lund, Ole, Crook, Derrick W., Wilson, Daniel J., and Aarestrup, Frank M. Fri .
"Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104". United States. https://doi.org/10.1128/AEM.03821-15. https://www.osti.gov/servlets/purl/1185725.
@article{osti_1185725,
title = {Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104},
author = {Leekitcharoenphon, Pimlapas and Hendriksen, Rene S. and Le Hello, Simon and Weill, François-Xavier and Baggesen, Dorte Lau and Jun, Se-Ran and Ussery, David W. and Lund, Ole and Crook, Derrick W. and Wilson, Daniel J. and Aarestrup, Frank M.},
abstractNote = {It has been 30 years since the initial emergence and subsequent rapid global spread of multidrug-resistantSalmonella entericaserovar Typhimurium DT104 (MDR DT104). Nonetheless, its origin and transmission route have never been revealed. We used whole-genome sequencing (WGS) and temporally structured sequence analysis within a Bayesian framework to reconstruct temporal and spatial phylogenetic trees and estimate the rates of mutation and divergence times of 315S. Moreover, typhimurium DT104 isolates sampled from 1969 to 2012 from 21 countries on six continents. DT104 was estimated to have emerged initially as antimicrobial susceptible in ~1948 (95% credible interval [CI], 1934 to 1962) and later became MDR DT104 in ~1972 (95% CI, 1972 to 1988) through horizontal transfer of the 13-kbSalmonellagenomic island 1 (SGI1) MDR region into susceptible strains already containing SGI1. This was followed by multiple transmission events, initially from central Europe and later between several European countries. An independent transmission to the United States and another to Japan occurred, and from there MDR DT104 was probably transmitted to Taiwan and Canada. An independent acquisition of resistance genes took place in Thailand in ~1975 (95% CI, 1975 to 1990). In Denmark, WGS analysis provided evidence for transmission of the organism between herds of animals. Interestingly, the demographic history of Danish MDR DT104 provided evidence for the success of the program to eradicateSalmonellafrom pig herds in Denmark from 1996 to 2000. Our refute several hypotheses on the evolution of DT104 and suggest that WGS may be useful in monitoring emerging clones and devising strategies for prevention ofSalmonellainfections.},
doi = {10.1128/AEM.03821-15},
journal = {Applied and Environmental Microbiology},
number = 8,
volume = 82,
place = {United States},
year = {Fri Mar 04 00:00:00 EST 2016},
month = {Fri Mar 04 00:00:00 EST 2016}
}
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