Abstract:Methicillin-resistant Staphylococcus aureus (MRSA) was classified as a high-group bacterial pathogen by the World Health Organization (WHO) and has been widely found in livestock products, with transmission occurring along the food processing chain. A novel multidrug-resistant ST9-SCCmecXII MRSA strain, HP, was isolated from a diseased pig's spleen. The objective is to gain insight into the resistance and genetic evolutionary characteristics of this novel MRSA. The resistance phenotype, antibiotic resistance genes (ARGs), mobile genetic elements (MGEs) and genetic evolutionary features were comprehensively analyzed by K-B disc diffusion method, PCR, whole genome sequencing, and comparative genomics. The results showed that HP exhibited resistance to 11 antibiotics belonging to 8 distinct classes, such as β-lactams, fluoroquinolones, etc. Conversely, it demonstrated susceptibility to vancomycin, ticlopidine, and linezolid. A total of nine ARGs were identified through PCR, while whole genome sequencing and database comparison led to the detection of 42 ARGs, predominantly comprising β-lactams, aminoglycosides, and MLSs. Of these, nine ARGs were located on the gene island HPGI1 and one ARG was located on the plasmid2. Evolutionary analysis showed that HP was closely related to milk-derived and porcine ST9-SCCmecXII type MRSA isolates and carried similar MGEs with them, including SCCmecXII, transposons, and gene islands. This study demonstrates that the novel strain HP has a complex resistance profile and multiple ARGs with multiple MGEs, which suggests the potential risks for transmission between different hosts and along food processing chains. This paper provides scientific information and a genetic basis for early warning and effective control of ST9-SCCmecXII novel MRSA transmission in the food processing chain.