Comparative Genomics and Drug Resistance of a Geographic Variant of ST239 Methicillin-Resistant Staphylococcus aureus Emerged in Russia

Two distinct classes of methicillin-resistant Staphylococcus aureus (MRSA) are spreading in hospitals (as hospital-acquired MRSA, HA-MRSA) and in the community (as community-acquired MRSA, CA-MRSA). Multilocus sequence type (ST) 239 MRSA, one of the most worldwide-disseminated lineages, has been noted as a representative HA-MRSA. Here, we isolated ST239 MRSA (spa type 3 [t037] and staphylococcal cassette chromosome mec [SCCmec] type III.1.1.1) and its novel variant with ST239/spa351 (t030)/SCCmecIII.1.1.4 (SCCmecIII(R)) not only from hospitals but also from patients with urethritis in the community in Russia. The Russian variant (strain 16K) possessed a hybrid genome consisting of CC8 and CC30, similar to the ST239/spa3/SCCmecIII.1.1.1 HA-MRSA (TW20) genome, but with marked diversity. The 16K′ CC30 section had SCCmecIII(R) carrying the dcs-carrying unit (which corresponded to the SCCmecIVc J3 joining region of ST30 CA-MRSA), lacked SCCmercury, and possessed a novel mobile element structure (MES16K) carrying the ccrC-carrying unit (with the recombinase gene ccrC1 allele 3) and drug resistance tranposons. The Russian variant included strains with a high ability to transfer its multiple drug resistance by conjugation; e.g., for strain 16K, the transfer frequency of a chloramphenicol resistance plasmid (p16K-1 with 2.9 kb in size) reached 1.4×10(−2), followed by Tn554 conjugative transfer at 3.6×l0(−4). The Russian variant, which has been increasing recently, included divergent strains with different plasmid patterns and pulsed field gel electrophoresis profiles. The data demonstrate the alternative nature of ST239 MRSA as CA-MRSA and also as a drug resistance disseminator, and its micro but dynamic evolution in Russia.