Unveiling the emergence of community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) in Chinese hospitals with remarkable genetic diversity: a multicenter molecular epidemiological investigation.

To understand the prevalence and phylogeny of methicillin-resistant Staphylococcus aureus (MRSA) in Chinese hospitals and identify the dominant MRSA lineages causing hospital infections, we collected 101 S. aureus isolates from multiple centers across China, tested their antibiotic sensitivity, and performed whole-genome sequencing. Using our group's database, a core genome-based phylogenetic analysis of 204 S. aureus isolates was conducted. The results revealed an interspersed distribution of MRSA and MSSA without distinct clade separation. CC59-ST59-t437-SCCmec IV was identified as the predominant community-associated MRSA (CA-MRSA) clone widely distributed across cities, while hospital-associated MRSA (HA-MRSA) was mainly composed of CC5-ST5-SCCmec II and CC8-ST239-SCCmec III, forming significant phylogenetic clusters. In contrast, MSSA strains were more diverse, with no clear clustering patterns. No regional clustering was observed, suggesting a widespread dissemination of major clones nationwide. Notably, some sequence types (e.g., ST45 and ST59) were shared by both MRSA and MSSA, and closely related strains with and without SCCmec elements suggested that smaller SCCmec types may be more readily gained or lost during evolution. Our findings indicate that CA-MRSA has a significant presence in hospitals with diverse subtypes, highlighting the need for increased attention to CA-MRSA in S. aureus control and prevention. IMPORTANCE The aim of this study was to identify the molecular epidemiological characteristics of S. aureus in Chinese hospitals, especially the dominant typing changes of MRSA during transmission. This study found that CA-MRSA appeared in the hospital environment with high diversity, suggesting that clinical attention should be paid to CA-MRSA in the prevention and diagnosis of S. aureus infection.