Comparative genomics of Staphylococcus aureus isolates from wild birds and pig farms elucidates levels of mobilomes, antibiotic pressure and host adaptation

The molecular characterization of Staphylococcus aureus isolates from different ecological niches could elucidate their pattern of host adaptation, transmission and drivers of antimicrobial resistance. Here, the genomic content and phylogenetic relatedness of 52 S. aureus isolates previously obtained from the nasal cavity of healthy nestling storks, pigs, and pig farmers in Spain were characterized. Illumina technology was used to obtain high-quality draft genomes to characterize their resistome, virulome, and mobile genetic elements. The relatedness of isolates was assessed by core-genome single nucleotide polymorphisms (SNPs). Bivariate logistic analysis showed that the frequencies of multidrug-resistance phenotype and transposons were significantly lower in isolates from nestling storks than in those from pigs (p=0.0002) and pig farmers (p=0.0004). However, the presence of human immune evasion cluster genes in S. aureus isolates from nestling storks was significantly higher than in those from pigs (p=0.0001) and pig farmers (p=0.0023). Interestingly, the frequencies of plasmids and phages were not significantly associated with the host (p>0.05). The phylogenetic analysis identified a cluster of all the MSSA-CC398 isolates carrying φSa3 and ermT on rep13 separately from the two MRSA-CC398 isolates (carrying ermT on repUS18). Also, highly related MRSA-CC398 isolates were detected in some pigs and related farmers (<10 SNPs). This study confirms high-level antibiotic selection in S. aureus in pigs and pig farmers in comparison to nestling storks. Furthermore, our findings highlight the continuous transmission of MRSA-CC398 in the pig-to-human interface and human-adapted MSSA-CC398 in nestling storks. Molecular surveillance of S. aureus using the One Health model to direct appropriate control strategies is required.