Genomic Analysis of the Unusual Staphylococcus aureus ST630 Isolates Harboring WTA Glycosyltransferase Genes tarM and tagN

Staphylococcus aureus (S. aureus) can cause a broad spectrum of diseases ranging from skin infections to life-threatening diseases in both community and hospital settings. The surface-exposed wall teichoic acid (WTA) has a strong impact on host interaction, pathogenicity, horizontal gene transfer, and biofilm formation in S. aureus. The unusual S. aureus ST630 strains containing both ribitol-phosphate (RboP) WTA glycosyltransferase gene tarM and glycerol-phosphate (GroP) WTA glycosyltransferase gene tagN have been found recently. Native PAGE analysis showed that the WTA of tagN, tarM-encoding ST630 strains migrated slower than that of non-tagN-encoding ST630 strains, indicating the differences in WTA structure. Some mobile genetic elements (MGEs) such as the unique GroP-WTA biosynthetic gene cluster (SaGroWI), SCCmec element, and prophages that probably originated from the CoNS were identified in tagN, tarM-encoding ST630 strains. The SaGroWI element was first defined in S. aureus ST395 strain, which was refractory to exchange MGEs with typical RboP-WTA expressing S. aureus but could undergo horizontal gene transfer events with other species and genera via the specific bacteriophage Φ187. Overall, our data indicated that this rare ST630 was prone to acquire DNA from CoNS and might serve as a novel hub for the exchange of MGEs between CoNS and S. aureus. IMPORTANCE The structure of wall-anchored glycopolymers wall teichoic acid (WTA) produced by most Gram-positive bacteria is highly variable. While most dominant Staphylococcus aureus lineages produce poly-ribitol-phosphate (RboP) WTA, the tagN, tarM-encoding ST630 lineage probably has a poly-glycerol-phosphate (GroP) WTA backbone like coagulase-negative staphylococci (CoNS). There is growing evidence that staphylococcal horizontal gene transfer depends largely on transducing helper phages via WTA as the receptor. The structural difference of WTA greatly affects the transfer of mobile genetic elements among various bacteria. With the growing advances in sequencing and analysis technologies, genetic analysis has revolutionized research activities in the field of the important pathogen S. aureus. Here, we analyzed the molecular characteristics of ST630 and found an evolutionary link between ST630 and CoNS. Elucidating the genetic information of ST630 lineage will contribute to understanding the emergence and diversification of new pathogenic strains in S. aureus.