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A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli

A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be common in...

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Autores principales: Wang, Han, Xu, Qi, Chen, Kaichao, Chan, Bill Kwan Wai, Ye, Lianwei, Yang, Xuemei, Xie, Miaomiao, Liu, Xiaobo, Ni, Hongyuhang, Chan, Edward Wai Chi, Chen, Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241742/
https://www.ncbi.nlm.nih.gov/pubmed/35604148
http://dx.doi.org/10.1128/spectrum.02528-21
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author Wang, Han
Xu, Qi
Chen, Kaichao
Chan, Bill Kwan Wai
Ye, Lianwei
Yang, Xuemei
Xie, Miaomiao
Liu, Xiaobo
Ni, Hongyuhang
Chan, Edward Wai Chi
Chen, Sheng
author_facet Wang, Han
Xu, Qi
Chen, Kaichao
Chan, Bill Kwan Wai
Ye, Lianwei
Yang, Xuemei
Xie, Miaomiao
Liu, Xiaobo
Ni, Hongyuhang
Chan, Edward Wai Chi
Chen, Sheng
author_sort Wang, Han
collection PubMed
description A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be common in E. coli from various sources. To understand the contribution of this plasmid to the virulence of E. coli, plasmid p1108-IncFIB in strain EC1108 was first cured to generate strain EC1108-PC. The virulence plasmid p15WZ-82_Vir in Klebsiella pneumoniae strain 15WZ-82 was then transmitted to EC1108-PC to produce the transconjugant, EC1108-PC-TC to assess the contribution of this virulence plasmid to the virulence level of E. coli. During the process of conjugation, p15WZ-82_Vir was found to be evolved into p15WZ-82_int, which underwent homologous recombination with a plasmid encoding a carbapenemase gene, bla(NDM-1), p1108-NDM, in EC1108-PC. Comparison between the level of virulence in the EC1108, EC1108-PC-TC, and EC1108-PC through serum and macrophage resistance assay, as well as animal experiments, confirmed that plasmid p1108-IncFIB encoded a high level of virulence in E. coli, yet the fusion plasmid derived from p15WZ-82_Vir did not encode virulence but instead imposed a high fitness cost in the E. coli strain EC1108-PC-TC. These findings indicate that E. coli strains carrying the virulence plasmid p1108-IncFIB in multidrug-resistant (MDR) strains may also impose serious public health threats like that of hypervirulent Klebsiella pneumoniae strains harboring the p15WZ-82_Vir plasmid. IMPORTANCE Acquisition of pLVPK-like virulence plasmid by Klebsiella pneumoniae converts it to hypervirulent K. pneumoniae (HvKP), which has become one of the most important clinical bacterial pathogens. The potential of transmission of this virulence plasmid and its contribution to the virulence of other Enterobacteriaceae, such as E. coli, are not clear yet. In this study, we showed that pLVPK-like virulence plasmid exhibited fitness costs and did not contribute to the virulence in E. coli. However, we identified a novel virulence plasmid, p1108-IncFIB, that encodes similar siderophore genes as those of pLVPK from a foodborne E. coli strain and showed that p1108-IncFIB encoded a high level of virulence in E. coli. BLAST of E. coli genomes from GenBank showed that these siderophore genes were widespread in clinical E. coli strains. Further studies are warranted to understand the impact of this plasmid in the control of clinical infections caused by E. coli.
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spelling pubmed-92417422022-06-30 A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli Wang, Han Xu, Qi Chen, Kaichao Chan, Bill Kwan Wai Ye, Lianwei Yang, Xuemei Xie, Miaomiao Liu, Xiaobo Ni, Hongyuhang Chan, Edward Wai Chi Chen, Sheng Microbiol Spectr Research Article A plasmid that harbored the virulence factors highly like those of the virulence plasmid commonly found in clinical hypervirulent Klebsiella pneumoniae strains was detected in a foodborne Escherichia coli strain EC1108 and designated p1108-IncFIB. This virulent-like plasmid was found to be common in E. coli from various sources. To understand the contribution of this plasmid to the virulence of E. coli, plasmid p1108-IncFIB in strain EC1108 was first cured to generate strain EC1108-PC. The virulence plasmid p15WZ-82_Vir in Klebsiella pneumoniae strain 15WZ-82 was then transmitted to EC1108-PC to produce the transconjugant, EC1108-PC-TC to assess the contribution of this virulence plasmid to the virulence level of E. coli. During the process of conjugation, p15WZ-82_Vir was found to be evolved into p15WZ-82_int, which underwent homologous recombination with a plasmid encoding a carbapenemase gene, bla(NDM-1), p1108-NDM, in EC1108-PC. Comparison between the level of virulence in the EC1108, EC1108-PC-TC, and EC1108-PC through serum and macrophage resistance assay, as well as animal experiments, confirmed that plasmid p1108-IncFIB encoded a high level of virulence in E. coli, yet the fusion plasmid derived from p15WZ-82_Vir did not encode virulence but instead imposed a high fitness cost in the E. coli strain EC1108-PC-TC. These findings indicate that E. coli strains carrying the virulence plasmid p1108-IncFIB in multidrug-resistant (MDR) strains may also impose serious public health threats like that of hypervirulent Klebsiella pneumoniae strains harboring the p15WZ-82_Vir plasmid. IMPORTANCE Acquisition of pLVPK-like virulence plasmid by Klebsiella pneumoniae converts it to hypervirulent K. pneumoniae (HvKP), which has become one of the most important clinical bacterial pathogens. The potential of transmission of this virulence plasmid and its contribution to the virulence of other Enterobacteriaceae, such as E. coli, are not clear yet. In this study, we showed that pLVPK-like virulence plasmid exhibited fitness costs and did not contribute to the virulence in E. coli. However, we identified a novel virulence plasmid, p1108-IncFIB, that encodes similar siderophore genes as those of pLVPK from a foodborne E. coli strain and showed that p1108-IncFIB encoded a high level of virulence in E. coli. BLAST of E. coli genomes from GenBank showed that these siderophore genes were widespread in clinical E. coli strains. Further studies are warranted to understand the impact of this plasmid in the control of clinical infections caused by E. coli. American Society for Microbiology 2022-05-23 /pmc/articles/PMC9241742/ /pubmed/35604148 http://dx.doi.org/10.1128/spectrum.02528-21 Text en Copyright © 2022 Wang 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
Wang, Han
Xu, Qi
Chen, Kaichao
Chan, Bill Kwan Wai
Ye, Lianwei
Yang, Xuemei
Xie, Miaomiao
Liu, Xiaobo
Ni, Hongyuhang
Chan, Edward Wai Chi
Chen, Sheng
A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title_full A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title_fullStr A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title_full_unstemmed A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title_short A Siderophore-Encoding Plasmid Encodes High-Level Virulence in Escherichia coli
title_sort siderophore-encoding plasmid encodes high-level virulence in escherichia coli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241742/
https://www.ncbi.nlm.nih.gov/pubmed/35604148
http://dx.doi.org/10.1128/spectrum.02528-21
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