Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania

ABSTRACT Increased knowledge about the role of horizontal gene transfer is key to improve our understanding of the spread of antimicrobial resistance (AMR) in human populations. We therefore studied the dissemination of the blaCTX-M-15 extended-spectrum-β-lactamase (ESBL) gene in Klebsiella pneumoni...

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Autores principales:	Torunn Pedersen, Marit Gjerde Tellevik, Øyvind Kommedal, Paul Christoffer Lindemann, Sabrina John Moyo, Jessin Janice, Bjørn Blomberg, Ørjan Samuelsen, Nina Langeland
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	CTX-M-15 HGT IncFIIK5 plasmid Klebsiella pneumoniae whole-genome sequencing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/6adaca3fcee242ea87a73b606e9cf28e
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spelling	oai:doaj.org-article:6adaca3fcee242ea87a73b606e9cf28e2021-11-15T15:30:50ZHorizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania10.1128/mSphere.00428-202379-5042https://doaj.org/article/6adaca3fcee242ea87a73b606e9cf28e2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00428-20https://doaj.org/toc/2379-5042ABSTRACT Increased knowledge about the role of horizontal gene transfer is key to improve our understanding of the spread of antimicrobial resistance (AMR) in human populations. We therefore studied the dissemination of the blaCTX-M-15 extended-spectrum-β-lactamase (ESBL) gene in Klebsiella pneumoniae isolates obtained from stool samples from hospitalized children and healthy controls below 2 years of age in Dar es Salaam, Tanzania, from August 2010 to July 2011. We performed Illumina whole-genome sequencing (WGS) to characterize resistance genes, multilocus sequence type (MLST), plasmid incompatibility group (Inc), and plasmid MLST of 128 isolates of K. pneumoniae with blaCTX-M-15 recovered from both healthy and hospitalized children. We assessed the phylogenetic relationship using single nucleotide polymorphism (SNP)-based analysis and resolved the sequences of five reference plasmids by Oxford Nanopore technology to investigate plasmid dissemination. The WGS analyses revealed the presence of a blaCTX-M-15-positive IncFIIK5/IncR plasmid with a highly conserved backbone in 70% (90/128) of the isolates. This plasmid, harboring genes encoding resistance to most β-lactams, aminoglycosides, trimethoprim-sulfamethoxazole, and chloramphenicol, was present in phylogenetically very diverse K. pneumoniae strains (48 different MLSTs) carried by both hospitalized and healthy children. Our data strongly suggest widespread horizontal transfer of this ESBL-carrying plasmid both in hospitals and in the general population. IMPORTANCE Horizontal spread of plasmids carrying multiple resistance genes is considered an important mechanism behind the global health problem caused by multidrug-resistant bacteria. Nevertheless, knowledge about spread of plasmids in a community is limited. Our detailed molecular analyses of K. pneumoniae isolated from hospitalized and healthy children in Tanzania disclosed an epidemic spread of a resistance plasmid. In this study population, we revealed horizontal plasmid transfer among K. pneumoniae as the key factor for dissemination of ESBLs. Traditional outbreak investigation and surveillance focus on the spread of bacterial clones, and short-read sequencing can result in erroneous plasmid composition. Our approach using long-read sequencing reveals horizontal gene transfer of antimicrobial resistance, and therefore has a potential impact on outbreak investigations and approaches to limit spread of AMR.Torunn PedersenMarit Gjerde TellevikØyvind KommedalPaul Christoffer LindemannSabrina John MoyoJessin JaniceBjørn BlombergØrjan SamuelsenNina LangelandAmerican Society for MicrobiologyarticleCTX-M-15HGTIncFIIK5 plasmidKlebsiella pneumoniaewhole-genome sequencingMicrobiologyQR1-502ENmSphere, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	CTX-M-15 HGT IncFIIK5 plasmid Klebsiella pneumoniae whole-genome sequencing Microbiology QR1-502
spellingShingle	CTX-M-15 HGT IncFIIK5 plasmid Klebsiella pneumoniae whole-genome sequencing Microbiology QR1-502 Torunn Pedersen Marit Gjerde Tellevik Øyvind Kommedal Paul Christoffer Lindemann Sabrina John Moyo Jessin Janice Bjørn Blomberg Ørjan Samuelsen Nina Langeland Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
description	ABSTRACT Increased knowledge about the role of horizontal gene transfer is key to improve our understanding of the spread of antimicrobial resistance (AMR) in human populations. We therefore studied the dissemination of the blaCTX-M-15 extended-spectrum-β-lactamase (ESBL) gene in Klebsiella pneumoniae isolates obtained from stool samples from hospitalized children and healthy controls below 2 years of age in Dar es Salaam, Tanzania, from August 2010 to July 2011. We performed Illumina whole-genome sequencing (WGS) to characterize resistance genes, multilocus sequence type (MLST), plasmid incompatibility group (Inc), and plasmid MLST of 128 isolates of K. pneumoniae with blaCTX-M-15 recovered from both healthy and hospitalized children. We assessed the phylogenetic relationship using single nucleotide polymorphism (SNP)-based analysis and resolved the sequences of five reference plasmids by Oxford Nanopore technology to investigate plasmid dissemination. The WGS analyses revealed the presence of a blaCTX-M-15-positive IncFIIK5/IncR plasmid with a highly conserved backbone in 70% (90/128) of the isolates. This plasmid, harboring genes encoding resistance to most β-lactams, aminoglycosides, trimethoprim-sulfamethoxazole, and chloramphenicol, was present in phylogenetically very diverse K. pneumoniae strains (48 different MLSTs) carried by both hospitalized and healthy children. Our data strongly suggest widespread horizontal transfer of this ESBL-carrying plasmid both in hospitals and in the general population. IMPORTANCE Horizontal spread of plasmids carrying multiple resistance genes is considered an important mechanism behind the global health problem caused by multidrug-resistant bacteria. Nevertheless, knowledge about spread of plasmids in a community is limited. Our detailed molecular analyses of K. pneumoniae isolated from hospitalized and healthy children in Tanzania disclosed an epidemic spread of a resistance plasmid. In this study population, we revealed horizontal plasmid transfer among K. pneumoniae as the key factor for dissemination of ESBLs. Traditional outbreak investigation and surveillance focus on the spread of bacterial clones, and short-read sequencing can result in erroneous plasmid composition. Our approach using long-read sequencing reveals horizontal gene transfer of antimicrobial resistance, and therefore has a potential impact on outbreak investigations and approaches to limit spread of AMR.
format	article
author	Torunn Pedersen Marit Gjerde Tellevik Øyvind Kommedal Paul Christoffer Lindemann Sabrina John Moyo Jessin Janice Bjørn Blomberg Ørjan Samuelsen Nina Langeland
author_facet	Torunn Pedersen Marit Gjerde Tellevik Øyvind Kommedal Paul Christoffer Lindemann Sabrina John Moyo Jessin Janice Bjørn Blomberg Ørjan Samuelsen Nina Langeland
author_sort	Torunn Pedersen
title	Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
title_short	Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
title_full	Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
title_fullStr	Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
title_full_unstemmed	Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania
title_sort	horizontal plasmid transfer among <named-content content-type="genus-species">klebsiella pneumoniae</named-content> isolates is the key factor for dissemination of extended-spectrum β-lactamases among children in tanzania
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/6adaca3fcee242ea87a73b606e9cf28e
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Horizontal Plasmid Transfer among <named-content content-type="genus-species">Klebsiella pneumoniae</named-content> Isolates Is the Key Factor for Dissemination of Extended-Spectrum β-Lactamases among Children in Tanzania

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