Genomic epidemiology and molecular characterization of <i>Streptococcus pyogenes</i> isolates from pediatric infections in Beijing, China

ABSTRACT Streptococcus pyogenes (Group A Streptococcus , GAS) remains a formidable global public health challenge. In this study, we conducted a high-resolution genomic epidemiology study on 176 non-invasive throat GAS isolates collected from pediatric patients in Beijing, China, between June 2024 and March 2025. Whole-genome sequencing was employed to characterize population structure, phylogenetic relationships, virulence genes, and antimicrobial resistance (AMR) determinants. The results showed that the population of GAS isolates in this study was dominated by emm12/ST36 (77.8%) and emm1 (22.2%) types. The emm1 isolates primarily belonged to ST1274 and ST28, with ST1274 being a single-locus variant of ST28. Crucially, the global M1 UK lineage was not detected. Phylogenomic analysis revealed that the emm12 population is structured into a dominant, conserved monophyletic clone (Clade A) co-circulating with diverse ancestral lineages. Pan-genome analysis further demonstrated an open genomic architecture characterized by a vast reservoir of accessory genes, indicating high evolutionary plasticity. While emm1 and emm12 exhibited distinct virulence signatures, a core virulence genome, including the the capsule-encoding hasABC operon, was universally conserved. Notably, we identified one emm12 isolate that acquired the emm1-associated superantigen speA gene via the ΦMGAS5005.1-like prophage. Furthermore, resistance to macrolides (97.7%) and tetracyclines (96.6%) was pervasive across both lineages, underscoring the severity of antimicrobial resistance in circulating GAS isolates. In conclusion, this study illuminates a distinct GAS epidemiological landscape in Beijing characterized by the local expansion of multidrug-resistant emm12 and emm1 clones. These findings emphasize the urgent need for continuous genomic surveillance to monitor the emergence of novel, hypervirulent recombinant variants within this distinct epidemiological context. IMPORTANCE Group A Streptococcus poses a persistent global health challenge, capable of causing life-threatening invasive infections; thus, monitoring its evolving epidemiology is critical. Global surveillance activities have recently identified an upsurge of the hypervirulent M1 UK lineage, and our study of pediatric infections in Beijing identifies a distinct local trajectory dominated by multidrug-resistant emm12 and emm1 lineages. Notably, we documented a horizontal gene transfer event where a multidrug-resistant emm12 isolate acquired the speA superantigen gene—a virulence factor typically associated with the emm1 lineage. This finding illustrates that endemic clones possess the genomic plasticity to combine high virulence potential with existing antimicrobial resistance. Our work highlights that beyond monitoring global high-risk clones like M1 UK , observing local evolutionary dynamics is essential to anticipate emerging regional threats.