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Mechanisms Underlying the Overlooked Chiral Fungicide-Driven Enantioselective Proliferation of Antibiotic Resistance in Earthworm Intestinal Microbiome

文献类型： 外文期刊

作者： Song, Jiajin 1 ; Zheng, Conglai 1 ; Qiu, Mengting 1 ; Zhan, Xiu-ping 4 ; Zhang, Zihan 1 ; Zhang, Houpu 3 ; Shi, Nan 2 ; Zhang, Luqing 1 ; Yu, Yunlong 1 ; Nicolaisen, Mogens 6 ; Xu, Lihui 5 ; Fang, Hua 1 ;

作者机构： 1.Zhejiang Univ, Key Lab Biol Crop Pathogens & Insects Zhejiang Pro, Minist Agr,Inst Pedticide & Environm Toxicol, Key Lab Mol Biol Crop Pathogens & Insect Pests,Col, Hangzhou 310058, Peoples R China

2.Univ Calif Irvine, Dept Dev & Cell Biol, Irvine, CA 92697 USA

3.Anhui Agr Univ, Coll Resources & Environm, Anhui Prov Key Lab Hazardous Factors & Risk Contro, Hefei 230036, Peoples R China

4.Shanghai Agr Technol Extens & Serv Ctr, Shanghai 201103, Peoples R China

5.Inst Ecoenvironm Protect, Shanghai Acad Agr Sci, Shanghai 201403, Peoples R China

6.Aarhus Univ, Fac Tech Sci, Dept Agroecol, Slagelse, Denmark

关键词： chiral fungicide; antibiotic resistance gene; earthworm gut; mobilome; horizontal transfer

期刊名称：ENVIRONMENTAL SCIENCE & TECHNOLOGY （ 影响因子：11.4； 五年影响因子：12.0 ）

ISSN： 0013-936X

年卷期： 2024 年 58 卷 6 期

页码：

收录情况： SCI

摘要： From a "One Health" perspective, the global threat of antibiotic resistance genes (ARGs) is associated with modern agriculture practices including agrochemicals application. Chiral fungicides account for a considerable proportion of wildly used agrochemicals; however, whether and how their enantiomers lead to differential proliferation of antibiotic resistance in agricultural environments remain overlooked. Focused on the soil-earthworm ecosystem, we for the first time deciphered the mechanisms underlying the enantioselective proliferation of antibiotic resistance driven by the enantiomers of a typical chiral fungicide mandipropamid (i.e., R-MDP and S-MDP) utilizing a multiomic approach. Time-series metagenomic analysis revealed that R-MDP led to a significant enhancement of ARGs with potential mobility (particularly the plasmid-borne ARGs) in the earthworm intestinal microbiome. We further demonstrated that R-MDP induced a concentration-dependent facilitation of plasmid-mediated ARG transfer among microbes. In addition, transcriptomic analysis with verification identified the key aspects involved, where R-MDP enhanced cell membrane permeability, transfer ability, biofilm formation and quorum sensing, rebalanced energy production, and decreased cell mobility versus S-MDP. Overall, the findings provide novel insights into the enantioselective disruption of microbiome and resistome in earthworm gut by chiral fungicides and offer significant contributions to the comprehensive risk assessment of chiral agrochemicals in agroecosystems.

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