Genomic Characterization of Staphylococcus aureus in Wildlife

SIMPLE SUMMARY: Staphylococcus aureus is both a commensal and opportunistic pathogen that colonizes human and animal skin and mucosal membranes. It is widely acknowledged that livestock can act as a reservoir for human strains and genetic traits, but less is known about the epidemiological significance of wild animals. In the present work, the S. aureus isolated from wild animals, hunters, and hunting auxiliary animals of Eastern Spain are described and characterized. The genomic structure of the population of the sequenced isolates showed a significant degree of diversity, raising the question of these strains’ origin and evolution. In addition, genomic characterization revealed the presence of relevant genes in the isolates belonging to wild animals, including resistance genes, as well as superantigens implicated in the pathogenicity of certain human S. aureus infections. These findings highlight the role of wild animals as a reservoir for some clinically relevant S. aureus strains and the importance of wildlife surveillance because the environment-animals-humans interaction impacts the transmission and evolution dynamics of S. aureus. ABSTRACT: Staphylococcus aureus is an opportunistic multi-host pathogen that threatens both human and animal health. Animals can act as a reservoir of S. aureus for humans, but very little is known about wild animals’ epidemiological role. Therefore, in this study, we performed a genomic characterization of S. aureus isolates from wildlife, hunters, and their auxiliary hunting animals of Eastern Spain. Of 20 different species, 242 wild animals were examined, of which 28.1% were S. aureus carriers. The common genet, the Iberian ibex, and the European hedgehog were the species with the highest S. aureus carriage. We identified 30 different sequence types (STs), including lineages associated with wild animals such as ST49 and ST581, multispecies lineages such as ST130, ST398, and ST425, and lineages commonly isolated from humans, including ST1 and ST5. The hunters and the single positive ferret shared ST5, ST398, or ST425 with wild animals. In wildlife isolates, the highest resistance levels were found for penicillin (32.8%). For virulence factors, 26.2% of them carried superantigens, while 14.8% harbored the immune evasion cluster (IEC), which indicates probable human origin. Our findings suggest that wild animals are a reservoir of clinically relevant genes and lineages that could have the potential to be transmitted to humans. These data support the notion that wildlife surveillance is necessary to better understand the epidemiology of S. aureus as a pathogen that circulates among humans, animals, and the environment.