Metagenomic approach reveals the role of bioagents in the environmental dissemination risk of rhizosphere soil antibiotic resistance genes pollution

Qiqi Zhi; Bufan Zheng; Kai Teng; Yansong Xiao; Xiangping Zhou; Qianjun Tang; Juan Li; Huaqun Yin; Delong Meng; Tianbo Liu

doi:10.1016/j.envres.2024.120090

Metagenomic approach reveals the role of bioagents in the environmental dissemination risk of rhizosphere soil antibiotic resistance genes pollution

Environ Res. 2024 Oct 5;263(Pt 2):120090. doi: 10.1016/j.envres.2024.120090. Online ahead of print.

Authors

Qiqi Zhi¹, Bufan Zheng², Kai Teng³, Yansong Xiao⁴, Xiangping Zhou⁵, Qianjun Tang⁶, Juan Li², Huaqun Yin¹, Delong Meng⁷, Tianbo Liu⁸

Affiliations

¹ School of Minerals Processing and Bioengineering, Central South University, Changsha, 410083, China; Key Laboratory of Biometallurgy, Ministry of Education, Changsha, 410083, China.
² College of Agronomy, Hunan Agricultural University, Changsha, 410127, China.
³ Hunan Province Xiangxi Autonomous Prefecture Tobacco Company, Jishou, 416000, China.
⁴ Chenzhou Tobacco Company of Hunan Province, Chenzhou, 423000, China.
⁵ Yongzhou Tobacco Company of Hunan Province, Yongzhou, 425000, China.
⁶ College of Plant Protection, Hunan Agricultural University, Changsha, 410127, China.
⁷ School of Minerals Processing and Bioengineering, Central South University, Changsha, 410083, China; Key Laboratory of Biometallurgy, Ministry of Education, Changsha, 410083, China. Electronic address: delong.meng@csu.edu.cn.
⁸ Tobacco Research Institute of Hunan Province, Changsha, 410004, China. Electronic address: tianboliu@126.com.

PMID: 39374754
DOI: 10.1016/j.envres.2024.120090

Abstract

Antibiotic resistance genes (ARGs) have been identified as emerging contaminants, raising concerns around the world. As environmentally friendly bioagents (BA), plant growth-promoting rhizobacteria (PGPR) have been used in agricultural systems. The introduction of BA will lead to the turnover of the microbial communities structure. Nevertheless, it is still unclear how the colonization of the invaded microorganisms could affects the rhizosphere resistome. Consequently, 190 ARGs and 25 integrative and conjugative elements (ICEs) were annotated using the metagenomic approach in 18 samples from the Solanaceae crop rhizosphere soil under BA and conventional treatment (CK) groups. Our study found that, after 90 days of treatment, ARG abundance was lower in the CK group than in the BA group. The results showed that aminoglycoside antibiotic resistance (OprZ), phenicol antibiotic resistance (OprN), aminoglycoside antibiotic resistance (ceoA/B), aminocoumarin antibiotic resistance (mdtB) and phenicol antibiotic resistance (MexW) syntenic with ICEs. Moreover, in 11 sequences, OprN (phenicol antibiotic resistance) was observed to have synteny with ICEPaeLESB58-1, indicating that the ICEs could contribute to the spread of ARGs. Additionally, the binning result showed that the potential bacterial hosts of the ARGs were beneficial bacteria which could promote the nutrition cycle, such as Haliangium, Nitrospira, Sideroxydans, Burkholderia, etc, suggesting that bacterial hosts have a great influence on ARG profiles. According to the findings, considering the dissemination of ARGs, BA should be applied with caution, especially the use of beneficial bacteria in BA. In a nutshell, this study offers valuable insights into ARGs pollution control from the perspective of the development and application of BA, to make effective strategies for blocking pollution risk migration in the ecological environment.

Keywords: Antibiotic resistance genes (ARGs); Bioagents; Environmental pollution; Integrative and conjugative elements (ICEs); Metagenomics; Rhizosphere soil.