Chlorothalonil drives the antibiotic resistome in earthworm guts

• Published in: Journal of hazardous materials 2024-02, Vol.463, p.132831, Article 132831
• Main Authors: Qiu, Mengting, Wu, Zishan, Song, Jiajin, Zheng, Conglai, Zhan, Xiuping, Shan, Mei, Cui, Minrong, Chen, Liezhong, Zhang, Luqing, Yu, Yunlong, Fang, Hua
• Format: Article
• Language: English
• Subjects: Antibiotic resistance genes; Earthworm; Fungicide; Gut microbiome; Soil
• ISSN: 0304-3894; 1873-3336; 1873-3336
• DOI: 10.1016/j.jhazmat.2023.132831

Earthworms are recognized as carriers of pollutants; however, how fungicide residues affect microbiota and antibiotic resistance genes (ARGs) in earthworm guts has remained unclear. In this work, changes in the earthworm gut microbiome and resistome were investigated after chlorothalonil (CTL) application. Earthworm activity accelerated the dissipation of CTL in soil, while metagenomic analysis revealed that CTL altered the ARG profile, leading to an increased abundance of ARGs in earthworm guts, particularly with respect to ARG subtypes CRP and OXA-427. CTL also reduced bacterial diversity and elevated the relative abundance of the phylum Proteobacteria, including a potential ARG host, Aeromonas, which is a known pathogen. Various bacterial genera from the Actinobacteria and Proteobacteria phyla were identified as broad-spectrum hosts for ARGs in earthworm guts. CTL could increase the abundance of multidrug efflux pump genes and enhance the abundance of mobile genetic elements, especially plasmids. Various co-occurrence patterns between plasmids and ARGs were also found after CTL treatments. It is concluded that CTL may act as a selective stress for ARGs and lead to an increase in their abundance by facilitating the proliferation of potential ARG hosts and enhancing plasmid-mediated horizontal transfer frequency of ARGs in earthworm guts. Fungicides appear to exert selective stress on ARGs in a manner that affects the dissemination of ARGs in agricultural environments. Soil fauna form an important part of soil ecosystems, with the guts of soil fauna acting as a commonly neglected reservoir of ARGs. Previous studies have rarely assessed the influence of pesticide residues on ARGs in soil faunal guts; hence, the current study investigated the profile of the earthworm gut resistome after CTL applications and revealed the driving mechanisms. [Display omitted] •Chlorothalonil enhanced the antibiotic resistome in earthworm gut microbiota.•The diversity of potential ARG hosts was explored in earthworm gut microbiota.•Abundance of multidrug efflux pump genes increased under chlorothalonil exposure.•Several co-occurrence patterns between MGEs and ARGs were found in chlorothalonil treatments.•Chlorothalonil exposure facilitated the plasmid-mediated ARGs transfer.