Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198

Research output: Contribution to journalJournal article – Annual report year: 2019Researchpeer-review

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Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. / Hawkey, Jane; Le Hello, Simon; Doublet, Benoît; Granier, Sophie A; Hendriksen, Rene S.; Fricke, W Florian; Ceyssens, Pieter-Jan; Gomart, Camille; Billman-Jacobe, Helen; Holt, Kathryn E; Weill, François-Xavier.

In: Microbial Genomics, Vol. 5, No. 7, 2019.

Research output: Contribution to journalJournal article – Annual report year: 2019Researchpeer-review

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Hawkey, J, Le Hello, S, Doublet, B, Granier, SA, Hendriksen, RS, Fricke, WF, Ceyssens, P-J, Gomart, C, Billman-Jacobe, H, Holt, KE & Weill, F-X 2019, 'Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198', Microbial Genomics, vol. 5, no. 7. https://doi.org/10.1099/mgen.0.000269

APA

CBE

Hawkey J, Le Hello S, Doublet B, Granier SA, Hendriksen RS, Fricke WF, Ceyssens P-J, Gomart C, Billman-Jacobe H, Holt KE, Weill F-X. 2019. Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. Microbial Genomics. 5(7). https://doi.org/10.1099/mgen.0.000269

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Hawkey, Jane ; Le Hello, Simon ; Doublet, Benoît ; Granier, Sophie A ; Hendriksen, Rene S. ; Fricke, W Florian ; Ceyssens, Pieter-Jan ; Gomart, Camille ; Billman-Jacobe, Helen ; Holt, Kathryn E ; Weill, François-Xavier. / Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198. In: Microbial Genomics. 2019 ; Vol. 5, No. 7.

Bibtex

@article{5173b720c3644f4fb653002fff5ad047,
title = "Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198",
abstract = "Salmonella enterica serotype Kentucky can be a common causative agent of salmonellosis, usually associated with consumption of contaminated poultry. Antimicrobial resistance (AMR) to multiple drugs, including ciprofloxacin, is an emerging problem within this serotype. We used whole-genome sequencing (WGS) to investigate the phylogenetic structure and AMR content of 121 S.enterica serotype Kentucky sequence type 198 isolates from five continents. Population structure was inferred using phylogenomic analysis and whole genomes were compared to investigate changes in gene content, with a focus on acquired AMR genes. Our analysis showed that multidrug-resistant (MDR) S.enterica serotype Kentucky isolates belonged to a single lineage, which we estimate emerged circa 1989 following the acquisition of the AMR-associated Salmonella genomic island (SGI) 1 (variant SGI1-K) conferring resistance to ampicillin, streptomycin, gentamicin, sulfamethoxazole and tetracycline. Phylogeographical analysis indicates this clone emerged in Egypt before disseminating into Northern, Southern and Western Africa, then to the Middle East, Asia and the European Union. The MDR clone has since accumulated various substitution mutations in the quinolone-resistance-determining regions (QRDRs) of DNA gyrase (gyrA) and DNA topoisomerase IV (parC), such that most strains carry three QRDR mutations which together confer resistance to ciprofloxacin. The majority of AMR genes in the S. enterica serotype Kentucky genomes were carried either on plasmids or SGI structures. Remarkably, each genome of the MDR clone carried a different SGI1-K derivative structure; this variation could be attributed to IS26-mediated insertions and deletions, which appear to have hampered previous attempts to trace the clone's evolution using sub-WGS resolution approaches. Several different AMR plasmids were also identified, encoding resistance to chloramphenicol, third-generation cephalosporins, carbapenems and/or azithromycin. These results indicate that most MDR S. enterica serotype Kentucky circulating globally result from the clonal expansion of a single lineage that acquired chromosomal AMR genes 30 years ago, and has continued to diversify and accumulate additional resistances to last-line oral antimicrobials. This article contains data hosted by Microreact.",
keywords = "Salmonella, SGI, ST198, Phylogenomics, MDR, Kentucky",
author = "Jane Hawkey and {Le Hello}, Simon and Beno{\^i}t Doublet and Granier, {Sophie A} and Hendriksen, {Rene S.} and Fricke, {W Florian} and Pieter-Jan Ceyssens and Camille Gomart and Helen Billman-Jacobe and Holt, {Kathryn E} and Fran{\cc}ois-Xavier Weill",
year = "2019",
doi = "10.1099/mgen.0.000269",
language = "English",
volume = "5",
journal = "Microbial Genomics",
issn = "2057-5858",
publisher = "Microbiology Society",
number = "7",

}

RIS

TY - JOUR

T1 - Global phylogenomics of multidrug-resistant Salmonella enterica serotype Kentucky ST198

AU - Hawkey, Jane

AU - Le Hello, Simon

AU - Doublet, Benoît

AU - Granier, Sophie A

AU - Hendriksen, Rene S.

AU - Fricke, W Florian

AU - Ceyssens, Pieter-Jan

AU - Gomart, Camille

AU - Billman-Jacobe, Helen

AU - Holt, Kathryn E

AU - Weill, François-Xavier

PY - 2019

Y1 - 2019

N2 - Salmonella enterica serotype Kentucky can be a common causative agent of salmonellosis, usually associated with consumption of contaminated poultry. Antimicrobial resistance (AMR) to multiple drugs, including ciprofloxacin, is an emerging problem within this serotype. We used whole-genome sequencing (WGS) to investigate the phylogenetic structure and AMR content of 121 S.enterica serotype Kentucky sequence type 198 isolates from five continents. Population structure was inferred using phylogenomic analysis and whole genomes were compared to investigate changes in gene content, with a focus on acquired AMR genes. Our analysis showed that multidrug-resistant (MDR) S.enterica serotype Kentucky isolates belonged to a single lineage, which we estimate emerged circa 1989 following the acquisition of the AMR-associated Salmonella genomic island (SGI) 1 (variant SGI1-K) conferring resistance to ampicillin, streptomycin, gentamicin, sulfamethoxazole and tetracycline. Phylogeographical analysis indicates this clone emerged in Egypt before disseminating into Northern, Southern and Western Africa, then to the Middle East, Asia and the European Union. The MDR clone has since accumulated various substitution mutations in the quinolone-resistance-determining regions (QRDRs) of DNA gyrase (gyrA) and DNA topoisomerase IV (parC), such that most strains carry three QRDR mutations which together confer resistance to ciprofloxacin. The majority of AMR genes in the S. enterica serotype Kentucky genomes were carried either on plasmids or SGI structures. Remarkably, each genome of the MDR clone carried a different SGI1-K derivative structure; this variation could be attributed to IS26-mediated insertions and deletions, which appear to have hampered previous attempts to trace the clone's evolution using sub-WGS resolution approaches. Several different AMR plasmids were also identified, encoding resistance to chloramphenicol, third-generation cephalosporins, carbapenems and/or azithromycin. These results indicate that most MDR S. enterica serotype Kentucky circulating globally result from the clonal expansion of a single lineage that acquired chromosomal AMR genes 30 years ago, and has continued to diversify and accumulate additional resistances to last-line oral antimicrobials. This article contains data hosted by Microreact.

AB - Salmonella enterica serotype Kentucky can be a common causative agent of salmonellosis, usually associated with consumption of contaminated poultry. Antimicrobial resistance (AMR) to multiple drugs, including ciprofloxacin, is an emerging problem within this serotype. We used whole-genome sequencing (WGS) to investigate the phylogenetic structure and AMR content of 121 S.enterica serotype Kentucky sequence type 198 isolates from five continents. Population structure was inferred using phylogenomic analysis and whole genomes were compared to investigate changes in gene content, with a focus on acquired AMR genes. Our analysis showed that multidrug-resistant (MDR) S.enterica serotype Kentucky isolates belonged to a single lineage, which we estimate emerged circa 1989 following the acquisition of the AMR-associated Salmonella genomic island (SGI) 1 (variant SGI1-K) conferring resistance to ampicillin, streptomycin, gentamicin, sulfamethoxazole and tetracycline. Phylogeographical analysis indicates this clone emerged in Egypt before disseminating into Northern, Southern and Western Africa, then to the Middle East, Asia and the European Union. The MDR clone has since accumulated various substitution mutations in the quinolone-resistance-determining regions (QRDRs) of DNA gyrase (gyrA) and DNA topoisomerase IV (parC), such that most strains carry three QRDR mutations which together confer resistance to ciprofloxacin. The majority of AMR genes in the S. enterica serotype Kentucky genomes were carried either on plasmids or SGI structures. Remarkably, each genome of the MDR clone carried a different SGI1-K derivative structure; this variation could be attributed to IS26-mediated insertions and deletions, which appear to have hampered previous attempts to trace the clone's evolution using sub-WGS resolution approaches. Several different AMR plasmids were also identified, encoding resistance to chloramphenicol, third-generation cephalosporins, carbapenems and/or azithromycin. These results indicate that most MDR S. enterica serotype Kentucky circulating globally result from the clonal expansion of a single lineage that acquired chromosomal AMR genes 30 years ago, and has continued to diversify and accumulate additional resistances to last-line oral antimicrobials. This article contains data hosted by Microreact.

KW - Salmonella

KW - SGI

KW - ST198

KW - Phylogenomics

KW - MDR

KW - Kentucky

U2 - 10.1099/mgen.0.000269

DO - 10.1099/mgen.0.000269

M3 - Journal article

VL - 5

JO - Microbial Genomics

JF - Microbial Genomics

SN - 2057-5858

IS - 7

ER -