Environmental Behavior and Control of Antibiotic Resistance Genes in Soil — A Review
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X53

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the National Natural Science Foundation of China, the Key Program of Frontier Sciences, Chinese Academy of Sciences, the Natural Science Foundation of Jiangsu Province

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    Abstract:

    Over the past several decades, the long-term misuse and abuse of antibiotics in human health and livestock production have significantly contributed to the widespread dissemination of antibiotic resistance. Antibiotic resistance has been regarded as the top of the six emerging environmental issues and global challenges humans face in this century. Antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) in natural and agricultural environments such as soil may have a substantial impact on the spread of resistance determinants to the human microbiome. Research on the distribution, source, diffusion and elimination techniques of ARGs in soil has become a hot topic.

    ARGs have been widely identified in diverse environments affected or unaffected by human activities, including soil, water sources, and atmosphere. Soil undoubtedly contains a complex natural resistome and also acts as a key reservoir for ARB and ARGs in the environment. The ARGs in soil primarily originate from internal resistance and external input. The internal resistance in microorganisms mainly indicates the presence of ARGs in the genomes of microbes. However, the antibiotic resistance in microbial can also be ascribed to the random mutation of genes under special conditions. In addition, with the widespread use of antibiotics in clinical care, livestock and agricultural production, more ARB and ARGs are introduced into the soil, resulting in an increased enrichment of ARGs.

    The transfer of ARGs often occurs via environmental media. However, recent studies have shown that they may also be transmitted between parents and offspring or among different species of bacteria by vertical and horizontal gene transfer (HGT), respectively. ARGs in the soil can be transferred to surface/groundwater, atmosphere and the phytosphere. Both natural factors and human activities play vital roles in ARGs transmission in soils. For example, soil physicochemical properties (pH, organic matter, water content, etc.), agronomic regulations (cropping patterns, reclaimed water irrigation, organic fertilization, etc.), and environmental contaminants (heavy metals, nanoparticles, microplastics, etc.) can significantly affect the structural diversity and function of soil microbial communities. They have been identified as important environmental pressures that induce the evolution and spread of antibiotic resistance.

    ARGs are also identified in human clinical pathogens conveyed by soil microbes. When comparing the multidrug-resistant resistome of soil bacteria with those in clinical human pathogens, the functional metagenomic analysis indicated a high nucleotide identity (>99%). This inferred possible HGT among bacteria from various environments. To reduce the threat posed by ARGs, treatment measures (aerobic composting, anaerobic digestion, and wastewater treatment technologies) have been examined to alleviate the selective pressure and reduce the import of ARGs into the soil. Generally, the reduction of ARGs in the environment is mainly related to extracellular DNA and cell transport, death of the host, and attenuation of extracellular ARGs.

    Although the threat of ARB and ARGs to humans is generally recognized, it is difficult to determine threshold values for the maximum admissible levels of ARB and ARGs in diverse environments highly related to human activities. Furthermore, there is insufficient information to quantitatively evaluate the associated human health risks. Considering the urgency of the problem, it is necessary to establish a global systematic and publicly available monitoring network, for consecutively measuring antibiotic usage and the diversity of antibiotic resistance from clinical and agricultural practices. Continuous surveillance of antibiotic resistance can contribute to disease therapy, effective antimicrobial management and policy formulating. Thus, the “One Health” theory was proposed to manage the development and spread of ARGs in an interdisciplinary manner, and holistically reduce human risk to the lowest level. More attention should be paid to ARGs pollution with investment in both fundamental and applied research, to provide a strong scientific basis for formulating effective alleviation actions and a standardized assessment system. This will serve as a baseline for preventing, reducing, and removing these environmental contaminants.

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SHENG Hongjie, WANG Fang, XIANG Leilei, FU Yuhao, WANG Ziquan, XU Min, MEI Zhi, LIU Yu, DOU Qingyuan, JIANG Xin, JAMES M. Tiedje. Environmental Behavior and Control of Antibiotic Resistance Genes in Soil — A Review[J]. Acta Pedologica Sinica,2023,60(1):39-49.

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  • Received:November 10,2021
  • Revised:January 04,2022
  • Adopted:March 16,2022
  • Online: March 17,2022
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