Quantitative and genomic epidemiology of Staphylococcus aureus in retail foods: insights into foodborne risk and clinically relevant lineages.

Abstract

Staphylococcus aureus is a major pathogen worldwide. This study quantified S. aureus in 3088 retail food samples and identified bulk sushi and salads as potential high-risk food categories, with 1.3% of sushi and 0.9% of salad samples exceeding 103 CFU/g. Classical staphylococcal enterotoxin (SE) genes were concentrated in clonal complex 1 (CC1) and CC5, which were broadly distributed across food categories, whereas CC15 and ST398 were major SE-negative lineages with distinct food tropism. Numerous virulence genes associated with immune evasion, adhesion, biofilm formation, and toxin production were also identified. CC22-ST22-t005 was the only clone harboring both TSST-1 and PVL-encoding genes. It was identified exclusively in salad samples, representing the first report of this emerging hypervirulent clone in Chinese retail foods. Acquired antibiotic resistance genes were identified on transposons, conferring resistance to multiple antibiotic classes, including β-lactams, macrolides, lincosamides, streptogramins, and tetracyclines. Methicillin-resistant S. aureus (MRSA) accounted for 4.3% of food isolates, 83.3% of which were multidrug resistant and harbored plasmid-borne resistance genes and diverse staphylococcal cassette chromosome mec (SCCmec) cassettes. Phylogenetic analysis of ST7-t091, CC22-ST22-t309, and CC22-ST22-t005 revealed co-circulation of food-derived and clinical isolates from diverse geographic regions and sources, with close genetic relatedness and pairwise genetic distances as low as 0.00007 substitutions per site. This comprehensive study provides baseline data for food safety risk monitoring and targeted control strategies, while also highlighting the potential role of food as a reservoir for clinically relevant lineages and antibiotic resistance genes.