PandemicVibrio parahaemolyticuswave succession by gene loss

Abstract

While the importance of spontaneous mutation and gene acquisition in the emergence and adaptive evolution of microbial pathogens is well recognized, the role of gene loss remains underexplored. Here, by large-scale phylogenomic analysis of 8,684 global isolates, we reconstructed the origin and evolutionary dynamics of the pandemic clone (PC) ofVibrio parahaemolyticus, the leading cause of seafood-associated infections worldwide. As has also been observed for the pandemic lineage ofV. cholerae, there was an ‘explosive’ burst of gene and genomic island acquisition during the emergence of the clone followed by divergence into distinct, successive sublineages mediating waves of infections. InV. parahaemolyticus,a recent global wave succession event has been driven by gene-loss in the putrescine utilization (Puu) pathway, which confers phenotypic advantages related to environmental adaptation (enhanced biofilms) and human transmission (increased cell adhesion and intestinal colonization, reduced virulence in an animal model and milder clinical symptoms in humans), aligning with the trade-off hypothesis of pathogen virulence evolution. We identify similar lineage-specific Puu-gene-loss across multiple bacterial genera, with effects on biofilm and adhesion replicated inV. choleraeandE. coli, suggesting convergent evolution and universal mechanisms across bacteria. Our findings provide a novel paradigm of adaptative evolution by gene loss in a pandemic pathogen.