Abstract
INTRODUCTION: Foodborne antibiotic-resistant enterococci pose significant risks to One Health and clinical antimicrobial efficacy through food chain transmission. Following the taxonomic reclassification of Enterococcus faecium (E. faecium), comprehensive long-term surveillance data on antibiotic resistance (ABR) patterns and genomic characteristics of E. faecium and Enterococcus lactis (E. lactis) across food animals, environmental sources, and human populations remain limited. METHODS: A total of 2,233 samples were collected from multiple nodes along the food chain across 5 Chinese provincial-level administrative divisions (PLADs) during 2015-2019 and 2023-2024. E. faecium (87 isolates) and E. lactis (153 isolates) were identified through whole-genome sequencing and average nucleotide identity analysis. Antimicrobial susceptibility testing, comprehensive genomic content analysis, and pan-genome-wide association studies were performed. RESULTS: E. faecium demonstrated significantly higher resistance rates to 12 antimicrobials compared with E. lactis (P<0.05). Conversely, E. lactis exhibited a higher resistance rate to erythromycin than E. faecium (P<0.01). The multidrug-resistant (MDR) rate of E. faecium (43/87, 49.4%) substantially exceeded that of E. lactis (16/153, 10.5%) (P<0.001). Genomic analysis revealed that E. faecium harbors significantly more antibiotic resistance genes, mobile genetic elements, and plasmid replicons than E. lactis. No significant interspecies differences were observed in virulence gene profiles associated with adhesion, immune modulation, biofilm formation, and exotoxin production. CONCLUSIONS: E. faecium presents substantially greater ABR risks than E. lactis within the Chinese food chain, necessitating enhanced species-specific surveillance programs. Future interventions should prioritize targeted control strategies tailored to each species to effectively mitigate One Health threats.