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Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli
BACKGROUND: The epidemiology of extended-spectrum β-lactamases (ESBLs) has undergone dramatic changes, with CTX-M-type enzymes prevailing over other types. bla(CTX-M) genes, encoding CTX-M-type ESBLs, are usually found on plasmids, but chromosomal location is becoming common. Given that bla(CTX-M)-h...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8111917/ https://www.ncbi.nlm.nih.gov/pubmed/33971966 http://dx.doi.org/10.1186/s13756-021-00941-8 |
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author | Shawa, Misheck Furuta, Yoshikazu Mulenga, Gillan Mubanga, Maron Mulenga, Evans Zorigt, Tuvshinzaya Kaile, Christone Simbotwe, Manyando Paudel, Atmika Hang’ombe, Bernard Higashi, Hideaki |
author_facet | Shawa, Misheck Furuta, Yoshikazu Mulenga, Gillan Mubanga, Maron Mulenga, Evans Zorigt, Tuvshinzaya Kaile, Christone Simbotwe, Manyando Paudel, Atmika Hang’ombe, Bernard Higashi, Hideaki |
author_sort | Shawa, Misheck |
collection | PubMed |
description | BACKGROUND: The epidemiology of extended-spectrum β-lactamases (ESBLs) has undergone dramatic changes, with CTX-M-type enzymes prevailing over other types. bla(CTX-M) genes, encoding CTX-M-type ESBLs, are usually found on plasmids, but chromosomal location is becoming common. Given that bla(CTX-M)-harboring strains often exhibit multidrug resistance (MDR), it is important to investigate the association between chromosomally integrated bla(CTX-M) and the presence of additional antimicrobial resistance (AMR) genes, and to identify other relevant genetic elements. METHODS: A total of 46 clinical isolates of cefotaxime-resistant Enterobacteriaceae (1 Enterobacter cloacae, 9 Klebsiella pneumoniae, and 36 Escherichia coli) from Zambia were subjected to whole-genome sequencing (WGS) using MiSeq and MinION. By reconstructing nearly complete genomes, bla(CTX-M) genes were categorized as either chromosomal or plasmid-borne. RESULTS: WGS-based genotyping identified 58 AMR genes, including four bla(CTX-M) alleles (i.e., bla(CTX-M-14), bla(CTX-M-15), bla(CTX-M-27), and bla(CTX-M-55)). Hierarchical clustering using selected phenotypic and genotypic characteristics suggested clonal dissemination of bla(CTX-M) genes. Out of 45 bla(CTX-M) gene-carrying strains, 7 harbored the gene in their chromosome. In one E. cloacae and three E. coli strains, chromosomal bla(CTX-M-15) was located on insertions longer than 10 kb. These insertions were bounded by ISEcp1 at one end, exhibited a high degree of nucleotide sequence homology with previously reported plasmids, and carried multiple AMR genes that corresponded with phenotypic AMR profiles. CONCLUSION: Our study revealed the co-occurrence of ISEcp1-bla(CTX-M-15) and multiple AMR genes on chromosomal insertions in E. cloacae and E. coli, suggesting that ISEcp1 may be responsible for the transposition of diverse AMR genes from plasmids to chromosomes. Stable retention of such insertions in chromosomes may facilitate the successful propagation of MDR clones among these Enterobacteriaceae species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13756-021-00941-8. |
format | Online Article Text |
id | pubmed-8111917 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-81119172021-05-11 Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli Shawa, Misheck Furuta, Yoshikazu Mulenga, Gillan Mubanga, Maron Mulenga, Evans Zorigt, Tuvshinzaya Kaile, Christone Simbotwe, Manyando Paudel, Atmika Hang’ombe, Bernard Higashi, Hideaki Antimicrob Resist Infect Control Research BACKGROUND: The epidemiology of extended-spectrum β-lactamases (ESBLs) has undergone dramatic changes, with CTX-M-type enzymes prevailing over other types. bla(CTX-M) genes, encoding CTX-M-type ESBLs, are usually found on plasmids, but chromosomal location is becoming common. Given that bla(CTX-M)-harboring strains often exhibit multidrug resistance (MDR), it is important to investigate the association between chromosomally integrated bla(CTX-M) and the presence of additional antimicrobial resistance (AMR) genes, and to identify other relevant genetic elements. METHODS: A total of 46 clinical isolates of cefotaxime-resistant Enterobacteriaceae (1 Enterobacter cloacae, 9 Klebsiella pneumoniae, and 36 Escherichia coli) from Zambia were subjected to whole-genome sequencing (WGS) using MiSeq and MinION. By reconstructing nearly complete genomes, bla(CTX-M) genes were categorized as either chromosomal or plasmid-borne. RESULTS: WGS-based genotyping identified 58 AMR genes, including four bla(CTX-M) alleles (i.e., bla(CTX-M-14), bla(CTX-M-15), bla(CTX-M-27), and bla(CTX-M-55)). Hierarchical clustering using selected phenotypic and genotypic characteristics suggested clonal dissemination of bla(CTX-M) genes. Out of 45 bla(CTX-M) gene-carrying strains, 7 harbored the gene in their chromosome. In one E. cloacae and three E. coli strains, chromosomal bla(CTX-M-15) was located on insertions longer than 10 kb. These insertions were bounded by ISEcp1 at one end, exhibited a high degree of nucleotide sequence homology with previously reported plasmids, and carried multiple AMR genes that corresponded with phenotypic AMR profiles. CONCLUSION: Our study revealed the co-occurrence of ISEcp1-bla(CTX-M-15) and multiple AMR genes on chromosomal insertions in E. cloacae and E. coli, suggesting that ISEcp1 may be responsible for the transposition of diverse AMR genes from plasmids to chromosomes. Stable retention of such insertions in chromosomes may facilitate the successful propagation of MDR clones among these Enterobacteriaceae species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13756-021-00941-8. BioMed Central 2021-05-10 /pmc/articles/PMC8111917/ /pubmed/33971966 http://dx.doi.org/10.1186/s13756-021-00941-8 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Shawa, Misheck Furuta, Yoshikazu Mulenga, Gillan Mubanga, Maron Mulenga, Evans Zorigt, Tuvshinzaya Kaile, Christone Simbotwe, Manyando Paudel, Atmika Hang’ombe, Bernard Higashi, Hideaki Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title | Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title_full | Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title_fullStr | Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title_full_unstemmed | Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title_short | Novel chromosomal insertions of ISEcp1-bla(CTX-M-15) and diverse antimicrobial resistance genes in Zambian clinical isolates of Enterobacter cloacae and Escherichia coli |
title_sort | novel chromosomal insertions of isecp1-bla(ctx-m-15) and diverse antimicrobial resistance genes in zambian clinical isolates of enterobacter cloacae and escherichia coli |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8111917/ https://www.ncbi.nlm.nih.gov/pubmed/33971966 http://dx.doi.org/10.1186/s13756-021-00941-8 |
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