WGS analysis of ST9-MRSA-XII isolates from live pigs in China provides insights into transmission among porcine, human and bovine hosts

Objectives: To elucidate the phylogenetic relationships among ST9-MRSA-XII isolates from different sources and their genetic features in colonization of different hosts. Methods: We obtained whole-genome sequences of two ST9-MRSA-XII isolates from nasal swabs associated with live pigs in China, and compared them with 135 previously sequenced genomes of 78 human-associated, 39 bovine and 18 porcine Staphylococcus aureus consisting of 11 MRSA of SCCmecXII, 62 MRSA of other SCCmec types and 62 MSSA. The distribution of diverse mobile genetic elements (MGEs), resistance genes and virulence determinants was investigated in relation to isolate phylogeny. Comparisons of SNPs and small insertion/deletions (indels) were conducted to examine genome-level variation between porcine and bovine ST9-MRSA-XII. Results: Phylogenetic analysis revealed that both of our porcine ST9-MRSA-XII isolates clustered with porcine, bovine and human-associated ST9-MRSA-XII. All of these isolates possessed a novel type V pathogenicity island, vSa alpha, carrying the von Willebrand-binding protein gene vwb, the immune evasion complex gene scn, the amino glycoside resistance gene aadE, staphylococcal superantigen-like genes (ssl1-ssl11) and lpl tandem genes. Compared with bovine ST9-MRSA-XII BA01611, our porcine isolates contain non-synonymous nucleotide substitutions in genes encoding adhesins and an indel located in a phosphonate ABC transporter pseudogene. Conclusions: The data suggest transmission of ST9-MRSA-XII among swine, cattle and humans. The extraordinary success of the ST9-MRSA-XII group in colonization of various hosts is likely due to acquisition of many MGEs harbouring functional antimicrobial resistance and virulence genes. Transmission of ST9-MRSA-XII between porcine and bovine hosts was accompanied by changes in binding profile and function in genes involved in metabolism.