Gradual loss of mobile genetic elements in Staphylococcus aureus USA300 in a closed hospital niche

Our French National Reference Centre for Staphylococci was requested to determine the epidemiological link between 19 methicillin-susceptible/resistant Staphylococcus aureus (MSSA/MRSA) isolates obtained from patients and a healthcare worker in a long-term care hospital, following the death of a nurse from pneumonia presumed to be associated with the drainage of a patient with an active skin infection. Whole genome sequencing was performed on all isolates to characterize their virulome, resistome, and phylogenetic relationships. Phylogenetic analysis revealed that 12 isolates belonged to the North American USA300 lineage, which is the predominant MRSA in North America but is less prevalent in Europe. USA300 strains are typically described as belonging to the clonal complex 8 (CC8) and possessing several mobile genetic elements (MGEs): the pathogenicity island SaPI5, the PVL-encoding bacteriophage ϕSa2USA, the staphylococcal chromosomal cassette mecIVa (SCCmecIVa), and the arginine catabolic mobile element (ACME). All 12 isolates lacked SaPI5, and four possessed the other typical MGEs of the USA300 lineage. However, one isolate did not carry SCCmecIVa, six did not have ACME, and two did not carry ϕSa2USA. The topology of the phylogenetic tree and the phylodynamic analysis suggested the loss of SaPI5 before entry in the long-term hospital, which may have occurred 3-4 years before the current outbreak. As long-term hospital may represent a relatively closed and stable ecosystem, we concluded that this loss of MGEs is a phenomenon of genetic diversification driven by niche specialization, in this case, originally constituted by a healthcare institution.