Staphylococcus aureus
sequence type (ST) 88, encompassing both methicillin-resistant
S. aureus
(MRSA) and methicillin-sensitive
S. aureus
(MSSA) phenotypes, is globally prevalent and commonly associated with skin and soft tissue infections. Despite its widespread occurrence, comprehensive genomic studies on this clone remain scarce. In this study, we performed detailed genomic analyses on 130 ST88 isolates derived from severe bloodstream infections alongside 275 publicly available ST88 sequences. Our phylogenetic analysis identified four distinct clades, with evidence suggesting independent evolution and significant clonal expansion of ST88 in China, particularly within clade I, which appeared to have emerged circa 1964. We documented notable interregional, international, and even intercontinental transmission of ST88 isolates. Variability in the distribution of SCC
mec
and
spa
types was observed across clades. Our
in silico
analyses indicated distinct patterns in the distribution of resistance genes, virulence genes, and mobile genetic elements among the clades, with clade I notably harboring the highest prevalence of the intact
sraP
gene and an independently acquired novel prophage, φST88-1. Conversely, clade IV exhibited deletions within the
sasC
gene, with certain sub-clades lacking the
sdrDE
and
fnbB
genes, underscoring the superior adhesive capabilities of clade I.
In vitro
experiments confirmed enhanced biofilm formation in clade I isolates, although the levels of hemolysis and cytotoxicity were similar across clades. Pan-genome-wide association study revealed that core SNPs, rather than the accessory genome, are the primary contributors to the diversification of the ST88 clades. These findings enrich our understanding of the genetic foundations underpinning the transmission dynamics and phenotypic diversity of ST88 clones globally.
IMPORTANCE
Understanding the evolution and transmission of
Staphylococcus aureus
ST88 clones is critically important due to their spread within food, hospital, and community environments, leading to significant health issues. Despite its prevalence, detailed genomic insights into ST88, particularly regarding its diversity and evolutionary dynamics, have been lacking. Our comprehensive genomic analysis of 130 ST88 isolates from severe bloodstream infections, alongside 275 sequences from public databases, significantly advances our understanding of this pathogen. We identified four distinct evolutionary clades, demonstrating the independent evolution and substantial clonal expansion of ST88 in China, as well as its ability to spread across regions and continents. The diversity among the isolates was evident in their unique profiles of
SCCmec
elements, antibiotic resistance genes, virulence genes, and mobile genetic elements. Our findings underscore the critical role of core genomic variations over accessory elements in driving the diversification of ST88. This enhanced understanding provides new insights that could inform more effective control strategies, crucial for developing interventions to combat the global spread of this formidable pathogen.
