Molecular Evolutionary Pathways toward Two Successful Community-Associated but Multidrug-Resistant ST59 Methicillin-Resistant Staphylococcus aureus Lineages in Taiwan: Dynamic Modes of Mobile Genetic Element Salvages.
Clonal complex 59 (CC59) Staphylococcus aureus in Taiwan includes both methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA). As the most prominent community-associated MRSA (CA-MRSA) in Taiwan, CC59 has two major clones characterized as PVL-negative SCCmec IV (carrying the staphylococcal cassette chromosome mec IV but Panton-Valentine leukocidin-negative) and PVL-positive SCCmec V (5C2&5). We investigated the drug resistance, phylogeny and the distribution and sequence variation of SCCmec, staphylococcal bacteriophage φSA3, genomic island νSaβ and MES (an enterococcal mobile genetic element conferring multidrug resistance) in 195 CC59 S. aureus. Sequencing and PCR mapping revealed that all of the CC59/SCCmec V (5C2&5) MRSA strains had acquired MESPM1 or its segregants, and obtained a φSA3-related fragment in νSaβ. In contrast, MES6272-2 and MES4578, which showed gentamicin resistance that was not encoded by MESPM1, were dominant in SCCmec IVg MRSA. Translocation of a whole φSA3 into νSaβ instead of only a φSA3-related fragment was common in SCCmec IVg MRSA. However, the non-subtype-g SCCmec IV MRSA (SCCmec IVa is the major) still carried MES and νSaβ structures similar to those in SCCmec V (5C2&5) MRSA. A minimum spanning tree constructed by multiple-locus variable-number tandem repeat analysis revealed that SCCmec IVg MRSA and SCCmec V (5C2&5) MRSA grouped respectively in two major clades. The CC59 MSSA was equally distributed among the two clades, while the non-subtype-g SCCmec IV MRSA mostly clustered with SCCmec V (5C2&5) MRSA. Our findings strongly suggest that CC59 MSSA acquired divergent mobile genetic elements and evolved to SCCmec IVg MRSA and SCCmec V (5C2&5) MRSA/non-subtype-g SCCmec IV MRSA independently. The evolutionary history of CC59 S. aureus explains how mobile genetic elements increase the antimicrobial resistance and virulence and contribute to the success of CA-MRSA in Taiwan.
Department of Microbiology and Immunology, Kaohsiung Medical University, Kaohsiung, Taiwan.
Wei-Chun
WC
Hung
Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taipei, Taiwan.
Tsai-Wen
TW
Wan
Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taipei, Taiwan.
Yu-Chia
YC
Kuo
Department of Epidemiology, Genomics, and Evolution, International Medical Education and Research Center, Niigata, Japan.
Tatsuo
T
Yamamoto
Institute of Medical Device and Imaging, National Taiwan University College of Medicine, Taipei, Taiwan.|Division of Neurosurgery, Department of Surgery, National Taiwan University Hospital, Taipei, Taiwan.
Jui-Chang
JC
Tsai
Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taipei, Taiwan.
Yu-Tzu
YT
Lin
Department of Laboratory Medicine, National Taiwan University Hospital, Taipei, Taiwan.
Po-Ren
PR
Hsueh
Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taipei, Taiwan.|Department of Laboratory Medicine, National Taiwan University Hospital, Taipei, Taiwan.
Lee-Jene
LJ
Teng
D002876:Chromosomes, Bacterial / Q000235:genetics; D002999:Clone Cells; D016000:Cluster Analysis; D017714:Community-Acquired Infections / Q000382:microbiology*; D004251:DNA Transposable Elements / Q000235:genetics; D004352:Drug Resistance, Microbial / Q000235:genetics; D024901:Drug Resistance, Multiple, Bacterial / Q000235:genetics*; D019143:Evolution, Molecular; D014644:Genetic Variation; D023281:Genomics; D055624:Methicillin-Resistant Staphylococcus aureus / Q000187:drug effects / Q000235:genetics* / Q000472:pathogenicity; D008826:Microbial Sensitivity Tests; D010802:Phylogeny; D013624:Taiwan; D014774:Virulence / Q000235:genetics
D004251:DNA Transposable Elements