Evolutionary origins, ecological drivers, and environmental implications of antibiotic resistance genes proliferation and dissemination: a 'One Health' perspective

Abstract

The dissemination of antibiotic resistance genes (ARGs) poses a severe and global threat to public health, and a core objective of the 'One Health' framework is to clarify how antibiotic resistomes evolve in natural environments. This review, grounded in the 'One Health' perspective, comprehensively explores the evolutionary origins, the ecological drivers underlying the proliferation and dissemination of ARGs, and their far-reaching environmental implications. Drawing on relevant studies, most ARGs have evolved beyond mere antibiotic resistance functions; instead, their evolutions are closely linked to their intrinsic physiological roles (such as the substrate transport function of efflux pumps), phylogenetic signatures (e.g., associations with bacterial community taxonomy), and ecological divisions (like resistome differences across distinct habitats). Ecologically, genomic incompatibility (e.g., disparities in nucleotide composition) acts as a constraint, limiting the spread of ARGs in natural environments. In contrast, anthropogenic disturbances, including the overuse of antibiotics and habitat modification, enhance habitat connectivity (e.g., gene flow among soil, human, and livestock systems), thereby promoting cross-compartment transmission of ARGs to pathogenic bacteria. Finally, this review highlights critical issues such as the blurred boundaries between human and environmental health, the urgent need for ecosystem-centric mitigation strategies, and key research gaps. These gaps include the long-term impacts of ARGs on microbial resilience and ecosystem multifunctionality, as well as the necessity of interdisciplinary efforts to safeguard both human health and ecological systems.