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Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli

Horizontal gene transfer plays an important role in the spread of antibiotic resistance, in which plasmid-mediated conjugation transfer is the most important mechanism. While sub-minimal inhibitory concentrations (sub-MIC) of antibiotics could promote conjugation frequency, the mechanism by which su...

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Autores principales: Ding, Manlin, Ye, Zi, Liu, Lu, Wang, Wei, Chen, Qiao, Zhang, Feiyang, Wang, Ying, Sjöling, Åsa, Martín-Rodríguez, Alberto J., Hu, Renjing, Chen, Wenbi, Zhou, Yingshun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9678054/
https://www.ncbi.nlm.nih.gov/pubmed/36419429
http://dx.doi.org/10.3389/fmicb.2022.1017092
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author Ding, Manlin
Ye, Zi
Liu, Lu
Wang, Wei
Chen, Qiao
Zhang, Feiyang
Wang, Ying
Sjöling, Åsa
Martín-Rodríguez, Alberto J.
Hu, Renjing
Chen, Wenbi
Zhou, Yingshun
author_facet Ding, Manlin
Ye, Zi
Liu, Lu
Wang, Wei
Chen, Qiao
Zhang, Feiyang
Wang, Ying
Sjöling, Åsa
Martín-Rodríguez, Alberto J.
Hu, Renjing
Chen, Wenbi
Zhou, Yingshun
author_sort Ding, Manlin
collection PubMed
description Horizontal gene transfer plays an important role in the spread of antibiotic resistance, in which plasmid-mediated conjugation transfer is the most important mechanism. While sub-minimal inhibitory concentrations (sub-MIC) of antibiotics could promote conjugation frequency, the mechanism by which sub-MIC levels of antibiotics affect conjugation frequency is not clear. Here, we used Klebsiella pneumoniae SW1780 carrying the multi-drug resistance plasmid pSW1780-KPC as the donor strain, to investigate the effects of sub-MICs of meropenem (MEM), ciprofloxacin (CIP), cefotaxime (CTX), and amikacin (AK) on conjugational transfer of pSW1780-KPC from SW1780 to Escherichia coli J53. Our results showed that the transfer frequencies increased significantly by treating SW1780 strain with sub-MIC levels of MEM, CIP, CTX and AK. Transfer frequencies at sub-MIC conditions in a Galleria mellonella were significantly higher than in vitro. To investigate gene expression and metabolic effects, RT-qPCR and LC–MS-based metabolome sequencing were performed. Transcript levels of T4SS genes virB1, virB2, virB4, virB8, and conjugation-related genes traB, traK, traE, and traL were significantly upregulated by exposure to sub-MICs of MEM, CIP, CTX, and AK. Metabolome sequencing revealed nine differentially regulated metabolites. Our findings are an early warning for a wide assessment of the roles of sub-MIC levels of antibiotics in the spread of antibiotic resistance.
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spelling pubmed-96780542022-11-22 Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli Ding, Manlin Ye, Zi Liu, Lu Wang, Wei Chen, Qiao Zhang, Feiyang Wang, Ying Sjöling, Åsa Martín-Rodríguez, Alberto J. Hu, Renjing Chen, Wenbi Zhou, Yingshun Front Microbiol Microbiology Horizontal gene transfer plays an important role in the spread of antibiotic resistance, in which plasmid-mediated conjugation transfer is the most important mechanism. While sub-minimal inhibitory concentrations (sub-MIC) of antibiotics could promote conjugation frequency, the mechanism by which sub-MIC levels of antibiotics affect conjugation frequency is not clear. Here, we used Klebsiella pneumoniae SW1780 carrying the multi-drug resistance plasmid pSW1780-KPC as the donor strain, to investigate the effects of sub-MICs of meropenem (MEM), ciprofloxacin (CIP), cefotaxime (CTX), and amikacin (AK) on conjugational transfer of pSW1780-KPC from SW1780 to Escherichia coli J53. Our results showed that the transfer frequencies increased significantly by treating SW1780 strain with sub-MIC levels of MEM, CIP, CTX and AK. Transfer frequencies at sub-MIC conditions in a Galleria mellonella were significantly higher than in vitro. To investigate gene expression and metabolic effects, RT-qPCR and LC–MS-based metabolome sequencing were performed. Transcript levels of T4SS genes virB1, virB2, virB4, virB8, and conjugation-related genes traB, traK, traE, and traL were significantly upregulated by exposure to sub-MICs of MEM, CIP, CTX, and AK. Metabolome sequencing revealed nine differentially regulated metabolites. Our findings are an early warning for a wide assessment of the roles of sub-MIC levels of antibiotics in the spread of antibiotic resistance. Frontiers Media S.A. 2022-11-07 /pmc/articles/PMC9678054/ /pubmed/36419429 http://dx.doi.org/10.3389/fmicb.2022.1017092 Text en Copyright © 2022 Ding, Ye, Liu, Wang, Chen, Zhang, Wang, Sjöling, Martín-Rodríguez, Hu, Chen and Zhou. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ding, Manlin
Ye, Zi
Liu, Lu
Wang, Wei
Chen, Qiao
Zhang, Feiyang
Wang, Ying
Sjöling, Åsa
Martín-Rodríguez, Alberto J.
Hu, Renjing
Chen, Wenbi
Zhou, Yingshun
Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title_full Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title_fullStr Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title_full_unstemmed Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title_short Subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from Klebsiellae pneumoniae to Escherichia coli
title_sort subinhibitory antibiotic concentrations promote the horizontal transfer of plasmid-borne resistance genes from klebsiellae pneumoniae to escherichia coli
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9678054/
https://www.ncbi.nlm.nih.gov/pubmed/36419429
http://dx.doi.org/10.3389/fmicb.2022.1017092
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