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Occurrence and dissemination of antibiotic resistance genes in mine soil ecosystems

  • Environmental Biotechnology
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Abstract

Metal(loid) selection contributes to selection pressure on antibiotic resistance, but to our knowledge, evidence of the dissemination of antibiotic resistance genes (ARGs) induced by metal(loid)s in mine soil ecosystems is rare. In the current study, using a high-throughput sequencing (HTS)-based metagenomic approach, 819 ARG subtypes were identified in a mine soil ecosystem, indicating that these environmental habitats are important reservoirs of ARGs. The results showed that metal(loid)-induced coselection has an important role in the distribution of soil ARGs. Furthermore, metal(loid) selection-induced ARGs were mainly associated with resistance-nodulation-division (RND) antibiotic efflux, which is distinct from what is observed in agricultural soil ecosystems. By using independent genome binning, metal(loid)s were shown impose coselection pressure on multiple ARGs residing on mobile genetic elements (MGEs), which promotes the dissemination of the antibiotic resistome. Interestingly, the current results showed that the density of several MGEs conferring ARGs was considerably higher in organisms most closely related to the priority pathogens Pseudomonas aeruginosa and Escherichia coli. Together, the results of this study indicate that mine soil ecosystems are important reservoirs of ARGs and that metal(loid)-induced coselection plays critical roles in the dissemination of ARGs in this type of soil habitat.

Key points

• Mining soil ecosystem is a reservoir of antibiotic resistance genes (ARGs).

• ARGs distribute via bacterial resistance-nodulation-division efflux systems.

• Metal(loid)s coselected ARGs residing on mobile genetic elements in P. aeruginosa and E. coli.

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Funding

This research was funded by the National Natural Science Foundation of China (41830753, 41807127, U1612442) and the Science and Technology Planning Project of Guangzhou (No. 202002020072).

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Authors and Affiliations

  1. Key Laboratory for Water Quality and Conservation of the Pearl River Delta, Ministry of Education, School of Environmental Science and Engineering, Guangzhou University, 230 Waihuanxi Road, Guangzhou, 510006, China

    Enzong Xiao, Yuqi Wang, Jinmei Deng, Wenjun Fan & Tangfu Xiao

  2. National-Regional Joint Engineering Research Center for Soil Pollution Control and Remediation in South China, Guangdong Key Laboratory of Integrated Agro-Environmental Pollution Control and Management, Institute of Eco-Environmental and Soil Sciences, Guangdong Academy of Sciences, Guangzhou, 510650, China

    Weimin Sun

  3. School of Environment, Henan Normal University, Xinxiang, China

    Weimin Sun

  4. Key Laboratory of Yellow River and Huai River Water Environment and Pollution Control, Ministry of Education, Henan Key Laboratory for Environmental Pollution Control, School of Environment, Henan Normal University, Xinxiang, China

    Weimin Sun

  5. State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang, 550081, China

    Zengping Ning

  6. College of Resource and Environment, Anhui Science and Technology University, Chuzhou, 233100, Anhui, China

    Fande Meng

  7. State Key Laboratory of Geohazard Prevention and Geoenvironment Protection, Chengdu University of Technology, Chengdu, 610059, China

    Tangfu Xiao

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  1. Enzong Xiao
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Contributions

EZX and TFX contributed to the study conception and design. Material preparation, data collection, and analysis were performed by EZX, WMS, and ZPN. The first draft of the manuscript was written by EZX; YQW, JMD, WJF, FDM, and TFX commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Tangfu Xiao.

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Xiao, E., Sun, W., Ning, Z. et al. Occurrence and dissemination of antibiotic resistance genes in mine soil ecosystems. Appl Microbiol Biotechnol 106, 6289–6299 (2022). https://doi.org/10.1007/s00253-022-12129-0

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