Deciphering the pangenome of the shellfish pathogen Vibrio europaeus : Evolutionary history and functional impact of core and accessory genes in aquaculture

Abstract Vibrio europaeus is an important pathogen in shellfish aquaculture, yet its genomic diversity and adaptive potential remain poorly understood. Here, we present the first comprehensive analysis of the V. europaeus pangenome, integrating genomic data from all strains available to the date sequenced specifically for this study. Those were isolated from different aquaculture facilities (shellfish hatcheries) associated to mass mollusk’s mortalities from different geographical locations, years and host species. Our findings revealed an open pangenome with the 61% of the genes associated to the accessory genome that contributes to environmental and host adaptations. Phylogenomic analyses of the core-genome (39% of the pangenome size) allowed to evaluate the evolutionary history and intraspecific diversity of V. europaeus and revealed that Spanish strains displayed a much lower genetic variability than French, Chilean or American strains, probably due to a monophyletic radiation event. Functional annotation of core and accessory genes revealed the key virulence factors of the species while it also disclosed that those are located mainly into the core genes. The high number of anti-phage defense systems encoded in the accessory genome explained almost all the variability of the species. The results provide important insights into the evolutionary history and ecological versatility of V. europaeus, with potential implications for diagnostics, epidemiological surveillance, and disease management strategies in aquaculture. Impact statement This study presents the first comprehensive pangenome analysis of Vibrio europaeus, an emergent pathogen responsible for severe economic losses in shellfish aquaculture, the second most important sector of global aquaculture. Here, we characterized for the first time the V. europaeus pangenome, integrating genomic data from all strains isolated to date, sequenced specifically for this study using NGS and/or third-generation (PacBio) technologies. This work achieved the most complete species pangenome to date and is among the first studies on aquaculture-related bacterial pathogens. Beyond a descriptive framework, the pangenome was critically examined to identify key traits, including virulence factors, secondary metabolite biosynthesis, and antimicrobial resistance genes, essential for host infection and adaptation. Moreover, the study of anti-phage defense systems was shown to account for much of the species’ genomic variability. The genomic resources and insights generated here substantially expand our understanding of V. europaeus biology and provide valuable information that can be applied for diagnostics, epidemiological surveillance, and sustainable management of this pathogen in aquaculture industry. Data summary All genome assemblies have been uploaded to the National Center for Biotechnology Information. The GenBank accession numbers for each of the 39 strains used in this study and detailed information can be found in Table S1. All bioinformatics tools used for comparative genomics have been listed in the Methods section including references, associated databases and analysis parameters. Competing Interest Statement The authors have declared no competing interest.