Characteristics and genomics study of Salmonella isolates in retail chicken in Shaanxi, China: Focus on comparative genomics analysis of S. Kentucky and S. enteritidis isolates from Shaanxi with those from elsewhere in China.

Abstract

Salmonella is a major foodborne pathogen, frequently linked to poultry and posing serious food safety and public health risks. To investigate its epidemiology in retail chicken in Shaanxi Province, China, we conducted a comprehensive study integrating whole-genome sequencing (WGS), Clusters of Orthologous Groups (COG) analysis, and machine learning (ML). Genomic data of 331&#xa0;S. Kentucky and 614&#xa0;S. enteritidis isolates from the NCBI database were also analyzed to assess genetic relatedness between local strains and those from other sources across China. From 280 chicken samples collected in seven cities, 92 (32.86&#xa0;%) were Salmonella-positive, yielding 132 isolates representing 29 serotypes. S. Kentucky predominated in wet markets, whereas S. enteritidis dominated supermarkets. All isolates were resistant to at least one antibiotic, with 87.88&#xa0;% showing multidrug resistance (MDR) and 38.64&#xa0;% exhibiting extensive drug-resistance (XDR). WGS of 78 representative isolates identified 61 antimicrobial resistance genes (ARGs) and seven quinolone resistance-determining region (QRDR) mutations, with ParC (Thr57Ser) being most frequent. It is worth noting that the high prevalence (100.00&#xa0;%) of Yersinia high-pathogenicity island (HPI) genes detected in S. infantis in this study has hardly been reported previously. Phylogenetic analysis revealed S. Kentucky and S. enteritidis, which are the predominant serotypes detected in the investigation, showing close genetic relationship (SNP&#xa0;<&#xa0;10) with those from chicken, pork, aquatic products, and humans in other provinces and host sources. Pan-genomic analysis showed that the number of accessory genes in S. Kentucky was higher than that in S. enteritidis, and supermarket- and human-origin Salmonella isolates possessed a higher proportion of accessory genes. This indicates that the genomes of these isolates are more open and have greater potential for acquiring exogenous elements. Functional enrichment analysis on the core and auxiliary genomes of S. Kentucky and S. enteritidis based on COG clustering indicated that significant differences could be found in the functions of the accessory genomes between the two serotypes. ML-based screening identified intS3, which is implicated in genomic stability and DNA damage repair, as a key feature gene in wet market isolates. Key feature genes identified in S. Kentucky and S. enteritidis from chicken were torI and rfaF, respectively, both associated with environmental adaptability. In human-derived isolates, ccmA and oadB1 were identified as feature genes, contributing to bacterial proliferation and host adaptation. This study provides comprehensive genomic and epidemiological insights into Salmonella in Shaanxi retail chicken, emphasizing the widespread MDR/XDR burden and cross-regional dissemination, and underscoring the need for strengthened genomic surveillance to protect food safety and public health.