Nanomaterials and environmental antimicrobial resistance: Propagation and inhibition of antibiotic resistance gene flow in the soil-plant system

Abstract

<p indent="0mm">The propagation of antibiotic resistance genes (ARGs), one of the emerging contaminants threatening global sanitation and health, has called for the necessity to overcome the spread of antimicrobial resistance (AMR). ARGs derived from manure is the main source of AMR in agricultural soil that can be propagated rapidly in soil-plant system and finally into food chain via horizontal gene transfer (HGT), which mainly includes three pathways mediated by mobile genetic elements (MGEs), namely, plasmid-mediated conjugation, extracellular DNA-mediated transformation, and phage- mediated transduction. The massive production and wide application of engineered nanomaterials (ENMs) and micro(nano) plastics have resulted in increasing concentrations of ENMs and micro(nano) plastics in the environment, which will eventually enter the soil and lead to migration and propagation of ARGs in soil-plant system. Bacterial pure culture studies reported that ENMs can exacerbate the dissemination of ARGs via changing intracellular reactive oxygen species (ROS), cell membrane permeability, and expression of genes related to conjugation. Moreover, ENMs and micro(nano) plastics in soil can change the soil antibiotic resistome and plant root morphology, structure and root exudates, which may affect the migration of ARB and ARGs from the rhizosphere to plants. The interactions between ENMs/micro(nano) plastics and ARGs might drive the development of multidrug resistance in soil-plant system. Although research targeting the effects of ENMs/micro(nano) plastics on the fate of ARGs is growing, an overview of biological impact and related mechanism is somehow lacking. In this review article, we systematically reviewed the interaction between ENMs/micro(nano) plastics and ARGs, especially in soil-plant system and attempted to explore the possibilities of nanotechnology to inhibit the transfer of antibiotic resistance gene flow. This review mainly covers: (1) Molecular mechanisms of ENMs and micro(nano) plastics regulating ARGs propagation. ENMs (i.e., Ag ENMs, CuO ENMs, TiO₂/Ag/GO ENMs and nano-graphene oxide) can promote ARGs propagation by accumulating intracellular reactive oxygen species (ROS), increasing cell membrane permeability and up-regulating of conjugation-related gene expression. However, CeO₂ ENMs and Fe₂O₃@MoS₂ ENMs have the potential to inhibit the propagation of ARGs via ROS elimination and down-regulating expression of HGT-related genes. (2) Influence of ENMs/micro(nano) plastics on ARGs in soil-plant system. ENMs/micro(nano) plastics can alter soil bacterial community and affect plant growth which will likely reduce the horizontal transfer of ARGs in soil by inhibiting the growth of soil microorganisms, reducing the abundance and diversity of ARB in soil, or changing the amount and composition of root exudates. (3) Application of nanotechnology on inhibiting antibiotic resistance gene flow. The regulatory mechanisms of nanotechnology on ARGs can be classified as: Inhibition of HGT, change of bacterial community composition, adsorption/degradation on ARGs and antimicrobial performance. Nanotechnology is promising for eliminating ARGs with high accuracy while its high cost and instability remain to be solved. For future study, more attention should be paid on the management of antibiotics, ARB and ARGs and the establishment of AMR risk assessment system to comprehensively assess the potential risk of AMR propagation via soil-plant-human pathways. Besides, the propagation of ARGs regulated by ENMs might be a challenge to distinguish and balance the advantages and disadvantages of ENMs in soil-plant system. Thus, it is urgent to comprehensively and systematically assess the environmental behavior and ecological risks of ENMs and micro(nano) plastics, contributing to the safe and efficient nano-based reduction of AMR.