Regional and global dissemination of methicillin-resistant Staphylococcus pseudintermedius, an opportunistic pathogen of canine origin

Staphylococcus pseudintermedius is a major bacterial colonizer and opportunistic pathogen in dogs. Methicillin-resistant S. pseudintermedius (MRSP) has emerged in the last decade as a serious threat to canine health. We sought to determine the phylogenetic relationships of MRSP and MDR S. pseudintermedius across five states in New England and place them in a global context. We used 126 previously published S. pseudintermedius genomes supplemented with 45 newly sequenced isolates. These were all obtained from disease cases of 166 dogs and five cats. The core genome phylogenetic tree revealed many deep branching lineages consisting of 110 multi-locus sequence types (STs). In silico detection of the mecA gene revealed 41 MRSP and 130 methicillin-susceptible S. pseudintermedius (MSSP) isolates. MRSP were derived from six structural types of SCCmec, the mobile genetic element that carries the mecA gene conferring methicillin resistance. Although many genomes were MSSP, they nevertheless harbored horizontally transferrable genes conferring resistance to many other antibiotic classes, including aminoglycosides, macrolides, tetracyclines and penams. A total of 81 genomes harbored at least three resistance genes and of which 12 had ten or more resistance genes. We compared the New England genomes to 297 previously published genomes sampled from five other states in the United States and 13 other countries. Despite the prevalence of the clonally expanding ST71 found worldwide and in other parts of the United States, we did not detect it in New England. The common MRSP STs in New England (STs 45, 64, 155, 261 and 749) were also found in the United Kingdom, Sri Lanka, Netherlands, Australia and New Zealand. Our results provide important insights to the evolution and spread of high-risk clones that can threaten the health of companion animals.