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Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to nontarget organisms, the effects of herbicides on the composition and functioning of soil microbial communities remain unclear. Here we show that application of three widely used herbicides—gly...

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Autores principales: Liao, Hanpeng, Li, Xi, Yang, Qiue, Bai, Yudan, Cui, Peng, Wen, Chang, Liu, Chen, Chen, Zhi, Tang, Jiahuan, Che, Jiangang, Yu, Zhen, Geisen, Stefan, Zhou, Shungui, Friman, Ville-Petri, Zhu, Yong-Guan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136491/
https://www.ncbi.nlm.nih.gov/pubmed/33592098
http://dx.doi.org/10.1093/molbev/msab029
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author Liao, Hanpeng
Li, Xi
Yang, Qiue
Bai, Yudan
Cui, Peng
Wen, Chang
Liu, Chen
Chen, Zhi
Tang, Jiahuan
Che, Jiangang
Yu, Zhen
Geisen, Stefan
Zhou, Shungui
Friman, Ville-Petri
Zhu, Yong-Guan
author_facet Liao, Hanpeng
Li, Xi
Yang, Qiue
Bai, Yudan
Cui, Peng
Wen, Chang
Liu, Chen
Chen, Zhi
Tang, Jiahuan
Che, Jiangang
Yu, Zhen
Geisen, Stefan
Zhou, Shungui
Friman, Ville-Petri
Zhu, Yong-Guan
author_sort Liao, Hanpeng
collection PubMed
description Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to nontarget organisms, the effects of herbicides on the composition and functioning of soil microbial communities remain unclear. Here we show that application of three widely used herbicides—glyphosate, glufosinate, and dicamba—increase the prevalence of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil microbiomes without clear changes in the abundance, diversity and composition of bacterial communities. Mechanistically, these results could be explained by a positive selection for more tolerant genotypes that acquired several mutations in previously well-characterized herbicide and ARGs. Moreover, herbicide exposure increased cell membrane permeability and conjugation frequency of multidrug resistance plasmids, promoting ARG movement between bacteria. A similar pattern was found in agricultural soils across 11 provinces in China, where herbicide application, and the levels of glyphosate residues in soils, were associated with increased ARG and MGE abundances relative to herbicide-free control sites. Together, our results show that herbicide application can enrich ARGs and MGEs by changing the genetic composition of soil microbiomes, potentially contributing to the global antimicrobial resistance problem in agricultural environments.
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spelling pubmed-81364912021-05-25 Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes Liao, Hanpeng Li, Xi Yang, Qiue Bai, Yudan Cui, Peng Wen, Chang Liu, Chen Chen, Zhi Tang, Jiahuan Che, Jiangang Yu, Zhen Geisen, Stefan Zhou, Shungui Friman, Ville-Petri Zhu, Yong-Guan Mol Biol Evol Discoveries Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to nontarget organisms, the effects of herbicides on the composition and functioning of soil microbial communities remain unclear. Here we show that application of three widely used herbicides—glyphosate, glufosinate, and dicamba—increase the prevalence of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil microbiomes without clear changes in the abundance, diversity and composition of bacterial communities. Mechanistically, these results could be explained by a positive selection for more tolerant genotypes that acquired several mutations in previously well-characterized herbicide and ARGs. Moreover, herbicide exposure increased cell membrane permeability and conjugation frequency of multidrug resistance plasmids, promoting ARG movement between bacteria. A similar pattern was found in agricultural soils across 11 provinces in China, where herbicide application, and the levels of glyphosate residues in soils, were associated with increased ARG and MGE abundances relative to herbicide-free control sites. Together, our results show that herbicide application can enrich ARGs and MGEs by changing the genetic composition of soil microbiomes, potentially contributing to the global antimicrobial resistance problem in agricultural environments. Oxford University Press 2021-02-16 /pmc/articles/PMC8136491/ /pubmed/33592098 http://dx.doi.org/10.1093/molbev/msab029 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
Liao, Hanpeng
Li, Xi
Yang, Qiue
Bai, Yudan
Cui, Peng
Wen, Chang
Liu, Chen
Chen, Zhi
Tang, Jiahuan
Che, Jiangang
Yu, Zhen
Geisen, Stefan
Zhou, Shungui
Friman, Ville-Petri
Zhu, Yong-Guan
Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title_full Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title_fullStr Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title_full_unstemmed Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title_short Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes
title_sort herbicide selection promotes antibiotic resistance in soil microbiomes
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8136491/
https://www.ncbi.nlm.nih.gov/pubmed/33592098
http://dx.doi.org/10.1093/molbev/msab029
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