Genomic epidemiology of dominant lineages of Streptococcus pyogenes emm types between 1993-2020, in China

Streptococcus pyogenes infections such as scarlet fever have increased in China since 2011. The genomic drivers of this increase are not known. The temporal clonal shifts within dominant emm12 and emm1 populations are unknown due to limited sampling. Based on a large longitudinal strain collection, we aimed to describe the molecular epidemiological characteristics and population structure of dominant S. pyogenesemm types circulating in China between 1993–2020.Here, we analyzed genomes of 945 China emm12 and emm1 isolates encompassing 1993–2020. The genomic data was integrated with national data on notifications of scarlet fever in the same period. The bacterial population structure and genomic features were analyzed to characterize the dynamics of circulating lineages during this period. We found there are five incidence peaks during 1993–2020 with S. pyogenes emm12 and emm1 being the dominant genotypes. The two genotypes driving scarlet fever in China have evolved independently of the global epidemic lineages. Four emm12 clades were evident prior to 2011, with a single clade replacing other emm12 populations by 2020. One dominant emm1 clade (termed M1 _china ) represents > 98% of clinical cases in China since the 1980s, and diverged into three subclades that can be clearly distinguished from global epidemic lineages. Compared to clinical strains from the 1990s, selection and expansion of emm12 and emm1 sub-clades coincides with high carriage of drug resistance genes for macrolides and virulence-encoding prophage. The ongoing selection of multi-drug resistant mobile elements and prophage in both emm1 and emm12 populations underlie the resurgence of scarlet fever since 2011 in China. The first detection in China of a genotype M1 _UK isolate in 2018 warrants additional enhanced surveillance.