Reshaping the battlefield: A decade of clonal wars among Staphylococcus aureus in China

Long-term comprehensive studies on the genomic epidemiology of both methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-susceptible S. aureus (MSSA) isolates are limited in China. Here, we aimed to assess the genomic epidemiological characteristics and population dynamics of S. aureus in China.

We performed whole-genome sequencing and resistance phenotyping on 3848 S. aureus isolates from bloodstream infections across 72 hospitals in 22 provinces, from 2011 to 2020 in China. We explored the dynamic trends in the resistance/virulence genes and mobile genetic element profiles across lineages, and conducted time-scaled phylogenetic investigation for prevalent lineages.

The results revealed 315 different sequence types (STs) among all strains, 205 of which were novel. Significant shifts in MRSA population structure were observed, with ST59 replacing ST239 as the dominant lineage, exhibiting widespread inter-hospital transmission and increasing lineage diversity. In contrast, the composition of predominant MSSA lineages, ST188 (11.21 %), ST7 (9.79 %), ST22 (9.10 %), ST5 (8.56 %) and ST398 (7.91 %), remained relatively stable over time, with the diversity among MSSA strains consistently preserved at the population level. Phylogenetic reconstruction showed that ST59, ST398, ST22 and ST188 MSSA could evolve into corresponding MRSA lineages through the acquisition of staphylococcal cassette chromosome mec (SCCmec) elements. Moreover, the distribution patterns of resistance and virulence genes closely correlated with different lineages, where the proportion of PVL⁺ isolates in MRSA is rising. Concurrently, changes in the MRSA population structure led to an overall decrease in the number of resistance and virulence genes, significantly increased antimicrobial sensitivity.

The shifting genomic landscape of S. aureus in China underscores the need for tailored antimicrobial stewardship and enhances understanding of its epidemiological trends over the past decade.