Abstract
INTRODUCTION: The Qinghai-Tibet Plateau, an extreme high-altitude ecosystem, presents a unique model for studying host-microbe-environment coevolution under environmental stress. However, the role of resident wildlife, particularly non-migratory passerines, as reservoirs and vectors for cross-boundary antibiotic resistance gene (ARG) dissemination remains poorly understood. METHODS: Here, through metagenomic analysis of two endemic passerines (Pseudopodoces humilis and Pyrgilauda ruficollis) and their habitats. RESULTS: We reveal convergent adaptations in their gut microbiomes, dominated by Actinomycetota, Pseudomonadota and Bacillota. Functional enrichment in carbohydrate metabolism and genetic information processing underpins host energy optimization in extreme high-altitude environments. Critically, these birds constitute a major reservoir of ARGs, harboring 153 antibiotic resistance ontologies (AROs) with nearly universal resistance to clinical antibiotic classes. The core resistome-comprising glycopeptide (van clusters), fluoroquinolone, and tetracycline resistance genes-reflects anthropogenic contamination amplified by environmental persistence. Environmental transmission pathways were unequivocally demonstrated via 47 AROs shared between avian hosts and proximal matrices (soil/grass), coupled with livestock-derived antibiotic influx through excreta, establishing the plateau as a hotspot for resistance gene flux. Strikingly, "low-abundance-high-resistance" taxa (Pseudomonadota, Actinomycetota, and Bacillota; ≤30% abundance but >80% ARG contribution) drive resistome plasticity, potentially facilitated by horizontal gene transfer. DISCUSSION: Our findings redefine resident passerines as sentinels of ecosystem health and bridges for cross-boundary antimicrobial resistance (AMR) spread. Mitigating global AMR thus necessitates interdisciplinary strategies targeting environmental reservoirs (e.g., regulating livestock antibiotic use) and monitoring avian-mediated gene flow.