Genomic characteristics and evolutionary analysis of Bordetella pertussis in Guizhou Province, China

Abstract Background Pertussis is an acute infectious respiratory disease caused by Bordetella pertussis (Bp). Despite high vaccination coverage, the genome of B. pertussis is prone to variations. These variations can lead to vaccine immune escape, recurrence of outbreaks, and increased difficulty in prevention and control. Therefore, close monitoring of B. pertussis genotype characteristics and evolution is crucial for the precise prevention and control of pertussis. Methods In this study, whole-genome sequencing (WGS) was performed on 36 B. pertussis strains collected in Guizhou Province from 2017 to 2024. A systematic analysis was conducted regarding their antigen genotypes, Multiple-locus variable-number tandem repeat analysis (MLVA) molecular types, antimicrobial susceptibility, resistance genes and mutation sites, evolutionary dynamics, and pan-genome characteristics. Results From 2017 to 2018, the proportion of the Bordetella pertussis vaccine antigen sequence typing (BPagST) genotype BPagST4 ( ptxP 3/ ptxA 1/ ptxB 1/ ptxC 4/ ptxD 1/ ptxE 4/ fhaB -2400_5550-1/ fim 2-1/ fim 3-1) in Guizhou Province was 43.75%, while from 2023 to 2024, its proportion increased to 100%, becoming the dominant genotype. The proportion of prn 150 increased markedly from 0.00% (0/16) in 2017–2018 to 95.00% (19/20) in 2023–2024, becoming the dominant prn allele. MLVA analysis revealed a total of nine MLVA types among B. pertussis isolates in Guizhou, predominantly MT28 and MT195, of which MT28 accounted for 66.67% of the macrolide-resistant isolates. Among the 36 B. pertussis isolates, the resistance rate to macrolide antibiotics was 83.33%. All resistant isolates carried the 23S rRNA A2047G mutation and exhibited cross-resistance to macrolide antibiotics. Considerable divergence between the circulating isolates in Guizhou and the vaccine strains CS and Tohama I was revealed by phylogenetic analysis. Together with domestic and international strains, these isolates were clustered into three main clades. The Guizhou strains clustered closely with domestic and international strains in Clade 1 and Clade 2. All isolates in Clade 1 were assigned to BPagST4 and were mainly concentrated in the MT28/ ptxP 3/ prn 150 subclade. The 23S rRNA A2047G mutation was carried by all of them. Whole-genome analysis showed that the average nucleotide identity between the genomes of the Guizhou B. pertussis isolates and the reference vaccine strains (CS and Tohama I) exceeded 99.88%. Conclusion Between 2017 and 2024, the circulating B. pertussis isolates in Guizhou Province have exhibited clear trends of antigenic evolution and resistance evolution, forming a dominant macrolide‑resistant lineage of MT28/ ptxP 3/ prn 150, which is highly synchronized with the global epidemic trend of B. pertussis strains. This study provides an important molecular epidemiological basis for the precise prevention and control of pertussis, vaccine optimization, and rational clinical drug use in Guizhou Province.