Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera

Background: Antibiotic resistance poses an increasing threat to public health. Horizontal gene transfer (HGT) promoted by antibiotics is recognized as a significant pathway to disseminate antibiotic resistance genes (ARGs). However, it is unclear whether non-antibiotic, anti-microbial (NAAM) chemica...

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Main Authors: Ji Lu, Yue Wang, Jie Li, Likai Mao, Son Hoang Nguyen, Tania Duarte, Lachlan Coin, Philip Bond, Zhiguo Yuan, Jianhua Guo
Format: Article
Language:English
Published: Elsevier 2018-12-01
Series:Environment International
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412018317264
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spelling doaj-1acaa68cd65f40c696fdb636205f78bd2020-11-25T01:41:19ZengElsevierEnvironment International0160-41202018-12-0112112171226Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial generaJi Lu0Yue Wang1Jie Li2Likai Mao3Son Hoang Nguyen4Tania Duarte5Lachlan Coin6Philip Bond7Zhiguo Yuan8Jianhua Guo9Advanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaInstitute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, AustraliaInstitute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, AustraliaInstitute for Molecular Bioscience, University of Queensland, St Lucia, Brisbane, Queensland 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, AustraliaAdvanced Water Management Centre (AWMC), The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia; Corresponding author.Background: Antibiotic resistance poses an increasing threat to public health. Horizontal gene transfer (HGT) promoted by antibiotics is recognized as a significant pathway to disseminate antibiotic resistance genes (ARGs). However, it is unclear whether non-antibiotic, anti-microbial (NAAM) chemicals can directly promote HGT of ARGs in the environment. Objectives: We aimed to investigate whether triclosan (TCS), a widely-used NAAM chemical in personal care products, is able to stimulate the conjugative transfer of antibiotic multi-resistance genes carried by plasmid within and across bacterial genera. Methods: We established two model mating systems, to investigate intra-genera transfer and inter-genera transfer. Escherichia coli K-12 LE392 carrying IncP-α plasmid RP4 was used as the donor, and E. coli K-12 MG1655 or Pseudomonas putida KT2440 were the intra- and inter-genera recipients, respectively. The mechanisms of the HGT promoted by TCS were unveiled by detecting oxidative stress and cell membrane permeability, in combination with Nanopore sequencing, genome-wide RNA sequencing and proteomic analyses. Results: Exposure of the bacteria to environmentally relevant concentrations of TCS (from 0.02 μg/L to 20 μg/L) significantly stimulated the conjugative transfer of plasmid-encoded multi-resistance genes within and across genera. The TCS exposure promoted ROS generation and damaged bacterial membrane, and caused increased expression of the SOS response regulatory genes umuC, dinB and dinD in the donor. In addition, higher expression levels of ATP synthesis encoding genes in E. coli and P. putida were found with increased TCS dosage. Conclusions: TCS could enhance the conjugative ARGs transfer between bacteria by triggering ROS overproduction at environmentally relevant concentrations. These findings improve our awareness of the hidden risks of NAAM chemicals on the spread of antibiotic resistance. Keywords: Non-antibiotic antimicrobial (NAAM), Triclosan, Environmental concentration, Antibiotic resistance genes, Horizontal gene transferhttp://www.sciencedirect.com/science/article/pii/S0160412018317264
collection DOAJ
language English
format Article
sources DOAJ
author Ji Lu
Yue Wang
Jie Li
Likai Mao
Son Hoang Nguyen
Tania Duarte
Lachlan Coin
Philip Bond
Zhiguo Yuan
Jianhua Guo
spellingShingle Ji Lu
Yue Wang
Jie Li
Likai Mao
Son Hoang Nguyen
Tania Duarte
Lachlan Coin
Philip Bond
Zhiguo Yuan
Jianhua Guo
Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
Environment International
author_facet Ji Lu
Yue Wang
Jie Li
Likai Mao
Son Hoang Nguyen
Tania Duarte
Lachlan Coin
Philip Bond
Zhiguo Yuan
Jianhua Guo
author_sort Ji Lu
title Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
title_short Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
title_full Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
title_fullStr Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
title_full_unstemmed Triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
title_sort triclosan at environmentally relevant concentrations promotes horizontal transfer of multidrug resistance genes within and across bacterial genera
publisher Elsevier
series Environment International
issn 0160-4120
publishDate 2018-12-01
description Background: Antibiotic resistance poses an increasing threat to public health. Horizontal gene transfer (HGT) promoted by antibiotics is recognized as a significant pathway to disseminate antibiotic resistance genes (ARGs). However, it is unclear whether non-antibiotic, anti-microbial (NAAM) chemicals can directly promote HGT of ARGs in the environment. Objectives: We aimed to investigate whether triclosan (TCS), a widely-used NAAM chemical in personal care products, is able to stimulate the conjugative transfer of antibiotic multi-resistance genes carried by plasmid within and across bacterial genera. Methods: We established two model mating systems, to investigate intra-genera transfer and inter-genera transfer. Escherichia coli K-12 LE392 carrying IncP-α plasmid RP4 was used as the donor, and E. coli K-12 MG1655 or Pseudomonas putida KT2440 were the intra- and inter-genera recipients, respectively. The mechanisms of the HGT promoted by TCS were unveiled by detecting oxidative stress and cell membrane permeability, in combination with Nanopore sequencing, genome-wide RNA sequencing and proteomic analyses. Results: Exposure of the bacteria to environmentally relevant concentrations of TCS (from 0.02 μg/L to 20 μg/L) significantly stimulated the conjugative transfer of plasmid-encoded multi-resistance genes within and across genera. The TCS exposure promoted ROS generation and damaged bacterial membrane, and caused increased expression of the SOS response regulatory genes umuC, dinB and dinD in the donor. In addition, higher expression levels of ATP synthesis encoding genes in E. coli and P. putida were found with increased TCS dosage. Conclusions: TCS could enhance the conjugative ARGs transfer between bacteria by triggering ROS overproduction at environmentally relevant concentrations. These findings improve our awareness of the hidden risks of NAAM chemicals on the spread of antibiotic resistance. Keywords: Non-antibiotic antimicrobial (NAAM), Triclosan, Environmental concentration, Antibiotic resistance genes, Horizontal gene transfer
url http://www.sciencedirect.com/science/article/pii/S0160412018317264
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