Reforestation substantially changed the soil antibiotic resistome and its relationships with metal resistance genes, mobile genetic elements, and pathogens

Song Zhang; Ting Li; Jinming Hu; Kexin Li; Dong Liu; Haixia Li; Fang Wang; Danhong Chen; Zejin Zhang; Qiuping Fan; Xiaoyong Cui; Rongxiao Che

doi:10.1016/j.jenvman.2023.118037

Reforestation substantially changed the soil antibiotic resistome and its relationships with metal resistance genes, mobile genetic elements, and pathogens

J Environ Manage. 2023 Sep 15:342:118037. doi: 10.1016/j.jenvman.2023.118037. Epub 2023 May 11.

Authors

Song Zhang¹, Ting Li², Jinming Hu³, Kexin Li⁴, Dong Liu⁵, Haixia Li⁶, Fang Wang⁷, Danhong Chen³, Zejin Zhang⁷, Qiuping Fan³, Xiaoyong Cui⁷, Rongxiao Che⁸

Affiliations

¹ Institute of International Rivers and Eco-security, Yunnan Key Laboratory of International Rivers and Transboundary Eco-Security, Yunnan University, Kunming, 650500, China; State Key Laboratory of Pollution Control & Resource Reuse, School of the Environment, Nanjing University, Nanjing, 210023, China.
² Institute of International Rivers and Eco-security, Yunnan Key Laboratory of International Rivers and Transboundary Eco-Security, Yunnan University, Kunming, 650500, China; College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China.
³ Institute of International Rivers and Eco-security, Yunnan Key Laboratory of International Rivers and Transboundary Eco-Security, Yunnan University, Kunming, 650500, China.
⁴ Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, 130102, China.
⁵ School of Life Sciences, Yunnan University, Kunming, 650091, China.
⁶ Faculty of Land Resource Engineering, Kunming University of Science and Technology, Kunming, 650093, China.
⁷ College of Life Sciences, University of Chinese Academy of Sciences, Beijing, 100049, China.
⁸ Institute of International Rivers and Eco-security, Yunnan Key Laboratory of International Rivers and Transboundary Eco-Security, Yunnan University, Kunming, 650500, China. Electronic address: cherongxiao@ynu.edu.cn.

PMID: 37178462
DOI: 10.1016/j.jenvman.2023.118037

Abstract

Revealing the effects of reforestation on soil antibiotic resistome is essential for assessing ecosystem health, yet related studies remain scarce. Here, to determine the responses of the soil antibiotic resistome to reforestation, 30 pairs of cropland and forest soil samples were collected from southwestern China, a region with high environmental heterogeneity. All the forests had been derived from croplands more than one decade ago. The diversity and abundance of soil antibiotic resistance genes (ARGs), metal resistance genes (MRGs), mobile genetic elements (MGEs), and pathogens were determined by metagenomic sequencing and real-time PCR. The results showed that reforestation significantly increased soil microbial abundance and the contents of Cu, total carbon, total nitrogen, total organic carbon, and ammonium nitrogen. Nevertheless, it decreased the contents of soil Zn, Ba, nitrate nitrogen, and available phosphorus. The main soil ARGs identified in this region were vancomycin, multidrug, and bacitracin resistance genes. Reforestation significantly increased the soil ARG abundance by 62.58%, while it decreased the ARG richness by 16.50%. Reforestation exerted no significant effects on the abundance of heavy metal resistance genes and pathogens, but it doubled the abundance of MGEs. Additionally, reforestation substantially decreased the co-occurrence frequencies of ARGs with MRGs and pathogens. In contrast, the correlation between ARGs and MGEs was greatly enhanced by reforestation. Similarly, the correlations between soil ARG abundance and environmental factors were also strengthened by reforestation. These findings suggest that reforestation can substantially affect the soil antibiotic resistome and exerts overall positive effects on soil health by decreasing ARG richness, providing critical information for assessing the effects of "grain for green" project on soil health.

Keywords: Antibiotic resistome; Farmlands; Forests; Land use changes; Metagenomics; Soil microbiome.

MeSH terms

Anti-Bacterial Agents / pharmacology
Ecosystem
Genes, Bacterial*
Interspersed Repetitive Sequences
Soil Microbiology
Soil*

Substances

Soil
Anti-Bacterial Agents