Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

Author:

Liao Hanpeng1,Li Xi1,Yang Qiue1,Bai Yudan1,Cui Peng1,Wen Chang1,Liu Chen1,Chen Zhi1,Tang Jiahuan1,Che Jiangang1,Yu Zhen2,Geisen Stefan3,Zhou Shungui1,Friman Ville-Petri4ORCID,Zhu Yong-Guan5

Affiliation:

1. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China

2. Guangdong Key Laboratory of Integrated Agro-environmental Pollution Control and Management, Guangdong Institute of Eco-environmental Science & Technology, Guangzhou 510650, China

3. Laboratory of Nematology, Wageningen University, Wageningen 6700AA, Netherlands

4. Department of Biology, University of York, Wentworth Way, York YO10 5DD, United Kingdom

5. Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China

Abstract

Abstract 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.

Funder

National Natural Science Foundation of China

National Key Technologies R&D Program of China

Fujian Agriculture and Forestry University Program for Distinguished Young Scholar

Natural Science Foundation of Fujian

Royal Society

UKRI, Defra, and the Scottish Government

Strategic Priorities Fund Plant Bacterial Diseases programme

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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