Microbial exchange and potential pathogen transmission between diverse habitats within urban park ecosystems

Urban parks serve as essential ecological networks that support both human and environmental health. However, the interconnection of microbial communities across their multi-habitat interfaces, along with their associated potential biosafety risks, remains insufficiently explored. To address the described knowledge gap, the study conducted a comprehensive microbiome analysis across the air, plant, soil, fauna, and water continuum of a representative urban park using 16S rRNA amplicon sequencing and whole-genome sequencing (WGS). The analysis identified 189 potential zoonotic pathogens shared among all examined habitats. Furthermore, microbial source tracking analysis indicated that the phyllosphere demonstrated strong connectivity with adjacent environments, serving as a central node for microbial exchange within the urban park ecosystem. WGS analyses revealed that the cross-habitat culturable strains (Bacillus altitudinis 41KF2b and Priestia aryabhattai B8W22) possessed a wide spectrum of antibiotic resistance genes (ARGs) and virulence factor genes (VFGs), including rank I high-risk ARGs, such as bacA. The phyllosphere of Ophiopogon bodinieri demonstrated extensive microbial exchange with the air, contributing 61.39 % to the airborne microbial community, while its cultural microorganisms harbored elevated cellular copy numbers of ARGs and VFGs. Concurrently, two cross-habitat strains isolated from air displayed the co-localization of ARGs with mobile genetic elements (MGEs), indicating that the phyllosphere-air interface may represent both a potential microbial safety risk and a pathway for ARG dissemination. The current study emphasized the migration-driven dispersal of microbes, pathogens, and ARGs/VFGs in urban parks, offering novel insights into urban ecosystem risk dynamics and providing a scientific basis for incorporating the "One Health" approach into landscape and urban planning.