Background: Staphylococcus aureus causes a wide variety of disease. The population structure of S. aureus comprises clonal complexes (CCs) with <2% nucleotide divergence between members of different CCs. Recently, more divergent S. aureus lineages, provisionally named S. argenteus and S. schweitzeri, have been recovered from humans across the world and monkeys in Africa.
Methods: We analysed whole genome sequence data for 189 isolates from these divergent lineages together with reference genomes from S. aureus and other staphylococcal species, and examined for phenotypic differences between the lineages.
Results: The isolates form two distinct phylogenetic and phenotypic clusters distinct from each other and from conventional S. aureus. On the basis of orthologous SNPs, S. argenteus and S. schweitzeri are sister groups that share <95% identity with each other, and <90% identity with conventional S. aureus. In addition: 1) S. argenteus is non-pigmented; 2) S. schweitzeri cannot be detected by standard nucA PCR; 3) S. schweitzeri has a distinct ecological niche; and 4) S. argenteus has virulence properties distinct from S. aureus. There are ~180 genes present in the core genome of all three lineages but absent from the next closest species, S. simiae, including genes for iron acquisition, efflux pumps, immune invasion, complement inhibition, capsule synthesis and fibrinogen binding. The acquisition of these genes was likely to be key events in the evolution of the pathogenic potential of these populations compared to other staphylococcal species. There is evidence for core genome reduction in S. aureus subsequent to its divergence from S. argenteus and S. schweitzeri. Notably, there continues to be inter-species horizontal gene transfer of accessory genome content including antimicrobial resistance determinants.
Conclusions: This study provides detailed information regarding the evolutionary history of S. aureus and two related, but clearly distinct, populations that should be considered as separate staphylococcal species.