Biodegradation of soil agrochemical contamination mitigates the direct horizontal transfer risk of antibiotic resistance genes to crops

Sci Total Environ. 2023 Nov 25:901:166454. doi: 10.1016/j.scitotenv.2023.166454. Epub 2023 Aug 20.

Abstract

Microorganisms can drive a substrate-specific biodegradation process to mitigate soil contamination resulting from extensive agrochemical usage. However, microorganisms with high metabolic efficiency are capable of adapting to the co-occurrence of non-substrate contaminants in the soil (particularly antibiotics). Therefore, the utilization of active microorganisms for biodegradation raises concerns regarding the potential risk of antibiotic resistance development. Here, the horizontal transfer risk of antibiotic-resistance genes (ARGs) in the soil-plant biota was assessed during biodegradation by the newly isolated Proteus terrae ZQ02 (which shortened the half-life of fungicide chlorothalonil from 9.24 d to 2.35 d when exposed to tetracycline). Based on metagenomic analyses, the distribution of ARGs and mobile genetic elements (MGEs) was profiled. The ARGs shared with ∼118 core genes and mostly accumulated in the rhizosphere and maize roots. After ZQ02 was inoculated, the core genes of ARGs reduced significantly in roots. In addition, the Pseudomonas and Proteus genera were identified as the dominant microbial hosts of ARGs and MGEs after ZQ02 adoption. The richness of major ARG hosts increased in soil but barely changed in the roots, which contributed to the mitigation of hosts-mediated ARGs transfer from soil to maize. Finally, the risk of ARGs has been assessed. Compared with the regular planting system, the number of risky ARGs declined from 220 (occupied 4.77 % of the total ARGs) to 143 (occupied 2.67 %) after biodegradation. Among these, 23 out of 25 high-risk genes were aggregated in the soil whereas only 2 genes were identified in roots, which further verified the low antibiotic resistance risk for crop after biodegradation. In a nutshell, this work highlights the critical advantage of ZQ02-based biodegradation that alleviating the ARGs transfer risks from soil to crop, which offers deeper insights into the versatility and feasibility of bioremediation techniques in sustainable agriculture.

Keywords: Antibiotic resistance genes; Biodegradation; Gene transfer risk; Metagenomics; Soil.