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Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate

Bacterial antimicrobial resistance, especially phenotypic resistance to multiple drugs (MDR), has posed a serious threat to public health worldwide. To clarify the mechanism of transmission of multidrug resistance encoding plasmids in Enterobacterales, all seven plasmids of an Escherichia coli (E. c...

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Autores principales: Liu, Xiaobo, Li, Ruichao, Chan, Edward Wai-Chi, Chen, Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10101111/
https://www.ncbi.nlm.nih.gov/pubmed/36943060
http://dx.doi.org/10.1128/spectrum.02820-22
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author Liu, Xiaobo
Li, Ruichao
Chan, Edward Wai-Chi
Chen, Sheng
author_facet Liu, Xiaobo
Li, Ruichao
Chan, Edward Wai-Chi
Chen, Sheng
author_sort Liu, Xiaobo
collection PubMed
description Bacterial antimicrobial resistance, especially phenotypic resistance to multiple drugs (MDR), has posed a serious threat to public health worldwide. To clarify the mechanism of transmission of multidrug resistance encoding plasmids in Enterobacterales, all seven plasmids of an Escherichia coli (E. coli) strain 1108 obtained from a chicken meat sample were extracted and sequenced by Illumina Nextseq 500 and MinION platforms. Plasmids in strain 1108 possessed 16 known antimicrobial resistance genes, with p1108-NDM (~97K) being the most variable plasmid. The multidrug resistance region of p1108-NDM was punctuated by eight IS26 insertion sequences; thus, four MDR regions were found in the backbone of this plasmid. The plasmid p1108-MCR (~65K) was found to lack the ISApl1 element and harbor the bla(CTX-M-64)-ISEcp1 transposition unit. Moreover, the ISEcp1-bla(CMY-2) transposition unit was found in plasmid p1108-CMY2 (~98K), whereas plasmid p1108-emrB (~102K) was associated with resistance to erythromycin (emrB) and streptomycin (aadA22). p1108-IncY (96K) was a phage P1-like plasmid, while p1108-IncFIB (~194K) was found to harbor a virulence region similar to ColV plasmids, and they were found to encode a conserved conjugative transfer protein but harbor no resistance genes. Finally, no mobile element and resistant genes were found in p1108-ColV (~2K). Carriage of mcr-1-encoding elements in carbapenemase-producing Escherichia coli will potentially render all antimicrobial treatment regimens ineffective. Enhanced surveillance and effective intervention strategies are urgently needed to control the transmission of such multidrug resistance plasmids. IMPORTANCE Antimicrobial resistance (AMR) has been increasingly prevalent in agricultural and clinical fields. Understanding the genetic environment involved in AMR genes is important for preventing transmission and developing mitigation strategies. In this study, we investigated the genetic features of an E. coli strain (1108) isolated from food product and harboring 16 AMR genes, including bla(NDM-1) and mcr-1 genes encoding resistance to last line antibiotics, meropenem, and colistin. Moreover, this strain also carried virulence genes such as iroBCDEN, iucABCD, and iutA. Our findings confirmed that multiple conjugative plasmids that were formed through active recombination and translocation events were associated with transmission of AMR determinants. Our data warrant the continuous monitoring of emergence and further transmission of these important MDR pathogens.
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spelling pubmed-101011112023-04-14 Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate Liu, Xiaobo Li, Ruichao Chan, Edward Wai-Chi Chen, Sheng Microbiol Spectr Research Article Bacterial antimicrobial resistance, especially phenotypic resistance to multiple drugs (MDR), has posed a serious threat to public health worldwide. To clarify the mechanism of transmission of multidrug resistance encoding plasmids in Enterobacterales, all seven plasmids of an Escherichia coli (E. coli) strain 1108 obtained from a chicken meat sample were extracted and sequenced by Illumina Nextseq 500 and MinION platforms. Plasmids in strain 1108 possessed 16 known antimicrobial resistance genes, with p1108-NDM (~97K) being the most variable plasmid. The multidrug resistance region of p1108-NDM was punctuated by eight IS26 insertion sequences; thus, four MDR regions were found in the backbone of this plasmid. The plasmid p1108-MCR (~65K) was found to lack the ISApl1 element and harbor the bla(CTX-M-64)-ISEcp1 transposition unit. Moreover, the ISEcp1-bla(CMY-2) transposition unit was found in plasmid p1108-CMY2 (~98K), whereas plasmid p1108-emrB (~102K) was associated with resistance to erythromycin (emrB) and streptomycin (aadA22). p1108-IncY (96K) was a phage P1-like plasmid, while p1108-IncFIB (~194K) was found to harbor a virulence region similar to ColV plasmids, and they were found to encode a conserved conjugative transfer protein but harbor no resistance genes. Finally, no mobile element and resistant genes were found in p1108-ColV (~2K). Carriage of mcr-1-encoding elements in carbapenemase-producing Escherichia coli will potentially render all antimicrobial treatment regimens ineffective. Enhanced surveillance and effective intervention strategies are urgently needed to control the transmission of such multidrug resistance plasmids. IMPORTANCE Antimicrobial resistance (AMR) has been increasingly prevalent in agricultural and clinical fields. Understanding the genetic environment involved in AMR genes is important for preventing transmission and developing mitigation strategies. In this study, we investigated the genetic features of an E. coli strain (1108) isolated from food product and harboring 16 AMR genes, including bla(NDM-1) and mcr-1 genes encoding resistance to last line antibiotics, meropenem, and colistin. Moreover, this strain also carried virulence genes such as iroBCDEN, iucABCD, and iutA. Our findings confirmed that multiple conjugative plasmids that were formed through active recombination and translocation events were associated with transmission of AMR determinants. Our data warrant the continuous monitoring of emergence and further transmission of these important MDR pathogens. American Society for Microbiology 2023-03-21 /pmc/articles/PMC10101111/ /pubmed/36943060 http://dx.doi.org/10.1128/spectrum.02820-22 Text en Copyright © 2023 Liu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Liu, Xiaobo
Li, Ruichao
Chan, Edward Wai-Chi
Chen, Sheng
Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title_full Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title_fullStr Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title_full_unstemmed Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title_short Complete Genetic Analysis of Plasmids Carrying Multiple Resistance, Virulence, and Phage-Like Genes in Foodborne Escherichia coli Isolate
title_sort complete genetic analysis of plasmids carrying multiple resistance, virulence, and phage-like genes in foodborne escherichia coli isolate
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10101111/
https://www.ncbi.nlm.nih.gov/pubmed/36943060
http://dx.doi.org/10.1128/spectrum.02820-22
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