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Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids

The occurrence of carbapenemase-producing Enterobacteriaceae (CPE) poses a considerable risk for public health. The gene for Klebsiella pneumoniae carbapenemase-2 (KPC-2) has been reported in many countries worldwide, and KPC-2-producing strains are mainly of human origin. In this study, we identifi...

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Autores principales: Zhang, Wanjiang, Zhu, Yao, Wang, Changzhen, Liu, Wenyu, Li, Ruichao, Chen, Fuguang, Luan, Tian, Zhang, Yanhe, Schwarz, Stefan, Liu, Siguo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739495/
https://www.ncbi.nlm.nih.gov/pubmed/31511369
http://dx.doi.org/10.1128/mSphere.00590-19
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author Zhang, Wanjiang
Zhu, Yao
Wang, Changzhen
Liu, Wenyu
Li, Ruichao
Chen, Fuguang
Luan, Tian
Zhang, Yanhe
Schwarz, Stefan
Liu, Siguo
author_facet Zhang, Wanjiang
Zhu, Yao
Wang, Changzhen
Liu, Wenyu
Li, Ruichao
Chen, Fuguang
Luan, Tian
Zhang, Yanhe
Schwarz, Stefan
Liu, Siguo
author_sort Zhang, Wanjiang
collection PubMed
description The occurrence of carbapenemase-producing Enterobacteriaceae (CPE) poses a considerable risk for public health. The gene for Klebsiella pneumoniae carbapenemase-2 (KPC-2) has been reported in many countries worldwide, and KPC-2-producing strains are mainly of human origin. In this study, we identified two novel hybrid plasmids that carry either bla(KPC-2) or the fosfomycin resistance gene fosA3 in the multiresistant K. pneumoniae isolate K15 of swine origin in China. The bla(KPC-2)-bearing plasmid pK15-KPC was a fusion derivative of an IncF33:A−:B− incompatibility group (Inc) plasmid and chromosomal sequences of K. pneumoniae (CSKP). A 5-bp direct target sequence duplication (GACTA) was identified at the boundaries of the CSKP, suggesting that the integration might have been due to a transposition event. The bla(KPC-2) gene on pK15-KPC was in a derivative of ΔTn6296-1. The multireplicon fosA3-carrying IncN-IncR plasmid pK15-FOS also showed a mosaic structure, possibly originating from a recombination between an epidemic fosA3-carrying pHN7A8-like plasmid and a pKPC-LK30-like IncR plasmid. Stability tests demonstrated that both novel hybrid plasmids were stably maintained in the original host without antibiotic selection but were lost from the transformants after approximately 200 generations. This is apparently the first description of a porcine sequence type 11 (ST11) K. pneumoniae isolate coproducing KPC-2 and FosA3 via pK15-KPC and pK15-FOS, respectively. The multidrug resistance (MDR) phenotype of this high-risk K. pneumoniae isolate may contribute to its spread and its persistence. IMPORTANCE The global dissemination of carbapenem resistance genes is of great concern. Animals are usually considered a reservoir of resistance genes and an important source of human infection. Although carbapenemase-producing Enterobacteriaceae strains of animal origin have been reported increasingly, bla(KPC-2)-positive strains from food-producing animals are still rare. In this study, we first describe the isolation and characterization of a carbapenem-resistant Klebsiella pneumoniae ST11 isolate, strain K15, which is of pig origin and coproduces KPC-2 and FosA3 via two novel hybrid plasmids. Furthermore, our findings highlight that this ST11 Klebsiella pneumoniae strain K15 is most likely of human origin and could be easily transmitted back to humans via direct contact or food intake. In light of our findings, significant attention must be paid to monitoring the prevalence and further evolution of bla(KPC-2)-carrying plasmids among the Enterobacteriaceae strains of animal origin.
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spelling pubmed-67394952019-09-13 Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids Zhang, Wanjiang Zhu, Yao Wang, Changzhen Liu, Wenyu Li, Ruichao Chen, Fuguang Luan, Tian Zhang, Yanhe Schwarz, Stefan Liu, Siguo mSphere Research Article The occurrence of carbapenemase-producing Enterobacteriaceae (CPE) poses a considerable risk for public health. The gene for Klebsiella pneumoniae carbapenemase-2 (KPC-2) has been reported in many countries worldwide, and KPC-2-producing strains are mainly of human origin. In this study, we identified two novel hybrid plasmids that carry either bla(KPC-2) or the fosfomycin resistance gene fosA3 in the multiresistant K. pneumoniae isolate K15 of swine origin in China. The bla(KPC-2)-bearing plasmid pK15-KPC was a fusion derivative of an IncF33:A−:B− incompatibility group (Inc) plasmid and chromosomal sequences of K. pneumoniae (CSKP). A 5-bp direct target sequence duplication (GACTA) was identified at the boundaries of the CSKP, suggesting that the integration might have been due to a transposition event. The bla(KPC-2) gene on pK15-KPC was in a derivative of ΔTn6296-1. The multireplicon fosA3-carrying IncN-IncR plasmid pK15-FOS also showed a mosaic structure, possibly originating from a recombination between an epidemic fosA3-carrying pHN7A8-like plasmid and a pKPC-LK30-like IncR plasmid. Stability tests demonstrated that both novel hybrid plasmids were stably maintained in the original host without antibiotic selection but were lost from the transformants after approximately 200 generations. This is apparently the first description of a porcine sequence type 11 (ST11) K. pneumoniae isolate coproducing KPC-2 and FosA3 via pK15-KPC and pK15-FOS, respectively. The multidrug resistance (MDR) phenotype of this high-risk K. pneumoniae isolate may contribute to its spread and its persistence. IMPORTANCE The global dissemination of carbapenem resistance genes is of great concern. Animals are usually considered a reservoir of resistance genes and an important source of human infection. Although carbapenemase-producing Enterobacteriaceae strains of animal origin have been reported increasingly, bla(KPC-2)-positive strains from food-producing animals are still rare. In this study, we first describe the isolation and characterization of a carbapenem-resistant Klebsiella pneumoniae ST11 isolate, strain K15, which is of pig origin and coproduces KPC-2 and FosA3 via two novel hybrid plasmids. Furthermore, our findings highlight that this ST11 Klebsiella pneumoniae strain K15 is most likely of human origin and could be easily transmitted back to humans via direct contact or food intake. In light of our findings, significant attention must be paid to monitoring the prevalence and further evolution of bla(KPC-2)-carrying plasmids among the Enterobacteriaceae strains of animal origin. American Society for Microbiology 2019-09-11 /pmc/articles/PMC6739495/ /pubmed/31511369 http://dx.doi.org/10.1128/mSphere.00590-19 Text en Copyright © 2019 Zhang 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
Zhang, Wanjiang
Zhu, Yao
Wang, Changzhen
Liu, Wenyu
Li, Ruichao
Chen, Fuguang
Luan, Tian
Zhang, Yanhe
Schwarz, Stefan
Liu, Siguo
Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title_full Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title_fullStr Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title_full_unstemmed Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title_short Characterization of a Multidrug-Resistant Porcine Klebsiella pneumoniae Sequence Type 11 Strain Coharboring bla(KPC-2) and fosA3 on Two Novel Hybrid Plasmids
title_sort characterization of a multidrug-resistant porcine klebsiella pneumoniae sequence type 11 strain coharboring bla(kpc-2) and fosa3 on two novel hybrid plasmids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739495/
https://www.ncbi.nlm.nih.gov/pubmed/31511369
http://dx.doi.org/10.1128/mSphere.00590-19
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