Abstract
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.
Highlights
IntroductionIt is well known that early acquisition of the staphylococcal chromosome cassette (SCC) mec in 1961 led to methicillin-resistant S. aureus (MRSA) [1, 2]
Staphylococcus aureus poses significant public health challenges worldwide
The present study, combining molecular characterization of the mobile genetic elements and phylogenetic analysis based on multiple-locus variable-number tandem repeat analysis (MLVA), further elucidated these differences, as follows: (i) genetic relatedness within the Clonal complex 59 (CC59)/SCCmec IV methicillin-resistant S. aureus (MRSA) strains was diverse, with the non-subtype-g SCCmec IV MRSA phylogenetically closer to CC59/SCCmec V (5C2&5) MRSA than to CC59/SCCmec IVg MRSA; and (ii) CC59 methicillin-susceptible S. aureus (MSSA) strains were phylogenetically clustered within the SCCmec IVg MRSA or SCCmec V (5C2&5) MRSA, sharing both of their features
Summary
It is well known that early acquisition of the staphylococcal chromosome cassette (SCC) mec in 1961 led to methicillin-resistant S. aureus (MRSA) [1, 2]. MRSA has imposed a heavy burden in healthcare environments, where it is known as healthcare-associated MRSA (HA-MRSA) [1, 2]. In the late 1990s, another genetically distinct MRSA, designated community-associated MRSA (CA-MRSA), emerged in the community, causing skin and soft tissue infections (SSTIs) and severe clinical disease, such as necrotizing pneumonia, in children and young adults without antecedent healthcare exposure [2,3,4,5]. Accumulation of increased drug resistance and increasing incidence in healthcare facilities has been noted in some CA-MRSA strains, such as the USA300 clone, which emerged in the United States [8]
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