Fourteen-year genomic surveillance of pediatric invasive Streptococcus pneumoniae: genomic and pan-genomic characterization

Invasive pneumococcal disease (IPD) poses a severe threat to children, with molecular epidemiological shifts driven by vaccination and antimicrobial pressure. Long-term genomic surveillance of pediatric IPD isolates is critical for optimizing prevention strategies. A total of 119 invasive Streptococcus pneumoniae (S. pneumoniae) strains were collected from children (2011–2024) at a tertiary children’s hospital. Whole-genome sequencing (WGS) was used for serotyping, Global Pneumococcal Sequencing Cluster (GPSC)/ Sequence type (ST) typing, phylogenetic analysis, antimicrobial resistance (AMR) and virulence gene profiling, and pan-genome analysis. The top predominant serotypes were 19 F (26.1%), 14 (15.1%), 19 A (11.8%), and 6 F (10.9%). GPSC1 (37.0%) and GPSC4 (12.6%) were the major lineages, with ST271 (24.4%), ST876 (11.8%), and ST320 (10.9%) as the leading STs. Phylogenetic analysis clustered strains into two clades, with serotypes/GPSCs/STs showing distinct clustering. Pan-genome analysis revealed 3921 genes (36.2% core, 49.9% accessory, 13.9% unique) with an open structure. Clusters of Orthologous Groups (COG) annotations showed core genes enriched in metabolism (39.1%) and information storage/processing (31.3%), while accessory/unique genes focused on information storage/processing. Kyoto Encyclopedia of Genes and Genomes (KEGG) annotations indicated metabolism as the dominant pathway (63.5%–70.5%) across gene categories, with unique genes enriched in human disease-related pathways (11.6%). This 14-year genomic study reveals the dominant lineages and genetic characteristics of pediatric IPD strains. Pan-genome COG/KEGG annotations clarify functional genetic diversity, providing region-specific molecular epidemiological evidence for optimizing vaccine selection and clinical precision management of pediatric IPD in Zhejiang Province.