Molecular epidemiological analysis of Staphylococcus aureus from hospital and food in Huai’an, Jiangsu, China, based on whole genome sequencing

Staphylococcus aureus (S. aureus) is a major pathogen causing severe infections and foodborne illnesses worldwide. Molecular epidemiological characteristics of S. aureus exhibit substantial temporal and regional differences. This study aims to investigate the genomic epidemiology of clinical (81 isolates) and food-derived (17 isolates) S. aureus strains from Huai’an, Jiangsu, China, during 2020 to 2021. Whole-genome sequencing revealed dominant multi-locus sequence typing (MLST) types, including ST398 (18.4%), ST1 (15.3%), and ST59 (11.2%). Hospital isolates showed higher methicillin-resistant S. aureus (MRSA) prevalence (58.0% vs. 41.2% in food), although the carriage rates of antimicrobial resistance (AMR) and virulence factor (VF) genes were similar between the two sources. Staphylococcal Chromosomal Cassette mec (SCCmec) type IVa(2B) (48.1%) predominated, suggesting community-associated MRSA infiltration into healthcare settings. Biofilm-associated gene profiles varied between MRSA and methicillin-susceptible S. aureus (MSSA), with ST1-t127 strains harboring comprehensive biofilm genes. Mobile genetic elements (MGEs), particularly plasmids (38.5%) and insertion sequences (32.3%), facilitated the dissemination of AMR and VF genes. Pan-genomic analysis demonstrated an open genome structure, with core genes enriched in metabolic functions (clusters of orthologous groups [COG] categories C, E, H, and P). Phylogenetic reconstruction revealed cross-regional transmission of ST1 and ST398, including international clades, while ST59 isolates exhibited clade diversification. This study elucidates the genetic diversity of S. aureus in Huai’an, Jiangsu, China, indicating its potential for cross-transmission between food and human sources and for regional dissemination, underscoring the need for One Health surveillance to curb the spread of high-risk clones.