Whole-genome sequencing reveals the genomic epidemiology of Yersinia enterocolitica in South African meat and global populations

Abstract Background Yersinia enterocolitica is a globally distributed foodborne pathogen increasingly recognised within the meat production continuum; however, its genomic epidemiology in South Africa remains poorly characterised. Methods This study employed whole-genome sequencing (WGS) to investigate the population structure, antimicrobial resistance (AMR), and virulence determinants of Y. enterocolitica isolated from retail meat and meat products, and to contextualise these findings within a global genomic framework. A total of 23 isolates from beef and pork samples were sequenced, of which 18 high-quality genomes were retained and analysed alongside 356 publicly available food-associated genomes. Results Phylogenomic analysis based on core genome multilocus sequence typing (cgMLST) revealed clustering into four major lineages,with South African isolates predominantly belonging to the globally distributed HC1490_10 clade. Multilocus sequence typing identified 11 sequence types among local isolates, including potentially uncommon lineages (ST661, ST329, ST173, andST352), whereas ST3, ST18, and ST178 represented widely distributed, globally prevalent lineage. Pan-genome analysis demonstrated substantial genomic plasticity, with an open pan-genome structure characterised by a high proportion of accessory and cloud genes, particularly in the global dataset. AMR profiling revealed a conserved intrinsic resistome dominated by β-lactamase genes ( blaA and ampC ) and efflux-associated determinants, while acquired resistance genes were detected at low frequencies and were confined to HC1490_10 isolates. Virulence profiling indicated that South African isolates lacked plasmid-associated pathogenicity determinants, including Type III secretion system-associated genes,and were classified as non-pathogenic biotype 1 A. In contrast, the pathogenic lineage (HC1490_2), harboured both chromosomal and plasmidencoded virulence factors. Mobile genetic element analysis identified diverse plasmids and prophages, highlighting their role in genome plasticity and horizontal gene transfer, although no plasmid-associated AMR genes were detected. Conclusions While the dominance of non-pathogenic lineages suggests a currently low virulence risk, the presence of globally distributed lineages underscores the potential for emergence of pathogenic variants. These findings support the integration of genomic surveillance intofood safety and One Health frameworks.