Uncovering the prevalence and drivers of antibiotic resistance genes in soils across different land-use types

Jie Wu; Shumin Guo; Haiyan Lin; Kejie Li; Zhutao Li; Jinyang Wang; William H Gaze; Jianwen Zou

doi:10.1016/j.jenvman.2023.118920

Uncovering the prevalence and drivers of antibiotic resistance genes in soils across different land-use types

J Environ Manage. 2023 Oct 15:344:118920. doi: 10.1016/j.jenvman.2023.118920. Epub 2023 Sep 1.

Authors

Jie Wu¹, Shumin Guo¹, Haiyan Lin¹, Kejie Li¹, Zhutao Li¹, Jinyang Wang², William H Gaze³, Jianwen Zou⁴

Affiliations

¹ Key Laboratory of Green and Low-carbon Agriculture in Southeastern China, Ministry of Agriculture and Rural Affairs, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China.
² Key Laboratory of Green and Low-carbon Agriculture in Southeastern China, Ministry of Agriculture and Rural Affairs, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China; Jiangsu Key Laboratory of Low Carbon Agriculture and GHGs Mitigation, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing, 210095, China. Electronic address: jywang@njau.edu.cn.
³ European Centre for Environment and Human Health, University of Exeter Medical School, Environment & Sustainability Institute, Penryn Campus, TR10 9FE, United Kingdom.
⁴ Key Laboratory of Green and Low-carbon Agriculture in Southeastern China, Ministry of Agriculture and Rural Affairs, College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China; Jiangsu Key Laboratory of Low Carbon Agriculture and GHGs Mitigation, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing, 210095, China.

PMID: 37660639
DOI: 10.1016/j.jenvman.2023.118920

Abstract

The emergence and spread of antibiotic resistance genes (ARGs) in soil due to animal excreta and organic waste is a major threat to human health and ecosystems, and global efforts are required to tackle the issue. However, there is limited knowledge of the variation in ARG prevalence and diversity resulting from different land-use patterns and underlying driving factors in soils. This study aimed to comprehensively characterize the profile of ARGs and mobile genetic elements and their drivers in soil samples collected from 11 provinces across China, representing three different land-use types, using high-throughput quantitative polymerase chain reaction and 16S rRNA amplicon sequencing. Our results showed that agricultural soil had the highest abundance and diversity of ARGs, followed by tea plantation and forest land. A total of 124 unique ARGs were detected in all samples, with shared subtypes among different land-use patterns indicating a common origin or high transmission frequency. Moreover, significant differences in ARG distribution were observed among different geographical regions, with the greatest enrichment of ARGs found in southern China. Biotic and abiotic factors, including soil properties, climatic factors, and bacterial diversity, were identified as the primary drivers associated with ARG abundance, explaining 71.8% of total ARG variation. The findings of our study demonstrate that different land-use patterns are associated with variations in ARG abundance in soil, with agricultural practices posing the greatest risk to human health and ecosystems regarding ARGs. Our identification of biotic and abiotic drivers of ARG abundance provides valuable insights into strategies for mitigating the spread of these genes. This study emphasizes the need for coordinated and integrated approaches to address the global antimicrobial resistance crisis.

Keywords: Antibiotic resistance genes; Environmental factors; Land-use patterns; Large-scale field survey; Shared ARGs.

MeSH terms

Animals
Anti-Bacterial Agents
Drug Resistance, Microbial / genetics
Ecosystem*
Humans
Prevalence
RNA, Ribosomal, 16S
Soil*

Substances

Soil
RNA, Ribosomal, 16S
Anti-Bacterial Agents