Emergence of distinct Streptococcus pyogenes emm1 and emm12 lineages in China.

Cases of scarlet fever have increased since 2011 across China. However, genomic epidemiological knowledge of Streptococcus pyogenes, the causative agent, is limited. Here we present a longitudinal analysis of S. pyogenes isolates (n = 1,029) across emm1 and emm12 genotypes collected from eight provinces across China between 1993 and 2024. Genomic data integrated with national scarlet fever incidence data confirmed emm12 and emm1 as dominant genotypes underlying five incidence peaks and disease resurgence in 2024. Phylogenetic analysis showed independent evolution of these genotypes in China compared to global epidemic lineages. Four emm12 clades were present in China before 2011 but were replaced by a single clade, Clade II, by 2020. A dominant emm1 clade, M1china, distinct from global lineages and the M1UK lineage, represents >98% of emm1 cases in China. Sub-clade expansion coincides with carriage of integrative conjugative elements containing macrolide and tetracycline resistance genes and virulence gene-encoding prophage. Ongoing maintenance of these elements in emm1 and emm12 populations likely underlies the resurgence of scarlet fever in China.