Genomic diversity and evolution of antibiotic resistance in Yersinia enterocolitica across multiple hosts in eastern China: A 19-year surveillance study.

Yersinia enterocolitica is a pathogenic Yersinia species whose public health significance in China is frequently underestimated. Y. enterocolitica poses significant health risks through gastrointestinal infection and extra-intestinal complications. This study conducted systematic, whole-genome sequencing (WGS)-based surveillance of Y. enterocolitica in Jiangsu Province, China (2005-2023), to elucidate epidemiological trends, genomics and antimicrobial resistance (AMR) characteristics, and zoonotic transmission dynamics. Among 30,398 samples (from humans, animals and food), 545 Y. enterocolitica isolates were detected (1.80 %). Pigs exhibited the highest detection rate (7.29 %), followed by dogs (2.59 %) and humans (1.44 %). Serotype O:3 (78.81 % pig-derived) and sequence type (ST) 429 (25.73 % of isolates) dominated. The predominance of the highly MDR ST429-O:3 clone in pigs raises concerns about its enhanced fitness and potential virulence. Multidrug resistance (MDR) was observed in 70.07 % of isolates, with pigs exhibiting the highest rate (79.37 %). Host-specific AMR profiles revealed an escalating MDR trend in human isolates, while strains of animal origin exhibited higher resistance rates than those of human origin, particularly from pigs, dogs, and chickens. Plasmid analysis identified IncC and IncFII(Y) as the predominant replicon types, with IncC plasmids harboring 15 AMR genes (including qnrVC4 and tet(A)). WGS analysis confirmed interprovincial transmission of ST656 strains, with ≤4 core-genome single-nucleotide polymorphism (SNP) differences between isolates from Ningxia (2019) and Jiangsu (2008-2023). Notably, dogs were identified as critical zoonotic reservoirs, sharing 24 STs with humans, highlighting a possible transmission pathway for pathogenic strains to humans. Y. enterocolitica in Jiangsu is characterized by the clonal expansion of MDR ST429-O:3 in pigs, significant zoonotic transmission through dogs and poultry, and plasmid-driven AMR dissemination. Enhanced "One Health" surveillance targeting pigs, dogs, and poultry is critical for mitigating outbreaks driven by these successful MDR and potentially virulent clones.