Diversity and evolution of oligopeptide permease systems in staphylococcal species

• This work systematically classified Opp systems in staphylococcal species.
• This work revealed the mechanisms involved in Opp generation and dissemination.
• This work revealed the origin of S. aureus encoded ACME-Opp system.

Several oligopeptide permease (Opp) systems have been found in staphylococcal species, including Opp1-4, Opp3′ and the arginine catabolic mobile element (ACME)-encoded Opp system (ACME-Opp). They confer upon bacteria the increasing fitness, but their evolutionary histories remain unclear. In this work, we performed a genome-wide identification of Opp systems in staphylococcal species. Novel Opp systems were identified, including the duplicate of Opp4 in Staphylococcus pseudintermedius and the ACME-Opp-like systems in coagulase-negative staphylococci (CoNS). Phylogenetic analysis revealed that all of the identified Opp systems were derived from Opp3 system by operon duplication during species divergence, while lateral gene transfer might also confer to the dissemination of Opp in staphylococci. In addition, we proposed an improved theory on evolution of ACME: the Opp and arginine-deiminase systems were firstly transferred from Staphylococcus haemolyticus to Staphylococcus epidermidis independently; in S. epidermidis they were assembled together and then transferred to Staphylococcus aureus.