Genomic plasticity and mobilome architecture of Vibrio europaeus reveal key mechanisms of evolutionary adaptation

<i>Vibrio europaeus</i> has emerged as a significant pathogen in shellfish aquaculture, causing mass mortality outbreaks in key bivalve species and leading to severe economic losses for the industry. Studies on the structure and characteristics of the accessory genome in aquaculture pathogens remain scarce, despite its crucial role in evolutionary and ecological adaptation. The accessory genome provides indeed genetic variability that enables rapid responses to environmental challenges, host adaptation and selective pressures such as antibiotics or phage predation. Here, we present the first comprehensive comparative genomic analysis of the <i>V. europaeus</i> pangenome to investigate the structural organization and functional content of its accessory genome. The soft mobilome of <i>V. europaeus</i> comprises 73% of accessory genes and 44% of the total pangenome, including non-chromosomic (plasmids) and chromosomic genetic elements such as prophages, integrative and conjugative/mobilizable elements, phage satellites and other mobile genetic elements (MGEs) designated as unclassified chromosomic regions of genomic plasticity (unclassified chromosomic RGPs). Among accessory elements, unclassified chromosomic RGPs were the primary drivers of evolutionary dynamics in <i>V. europaeus</i>, acting as the main genetic reservoir of anti-phage defence systems and antimicrobial resistance genes. Notably, the identification of abundant insertion hotspots in chromosomic genetic elements facilitates the rapid acquisition of anti-phage defence systems, thereby enabling rapid turnover of these systems and enhancing host fitness. In addition, novel pVE1-like plasmids (>300 kb) - only found in this species and its closest relative <i>Vibrio tubiashii</i> - emerged as the largest and most ubiquitous MGEs in <i>V. europaeus</i>. These plasmids encode the highest number of virulence genes and secondary metabolite biosynthetic genes, as well as a remarkable diversity of anti-phage defence systems among closely related strains. Although the genome dataset analysed here is limited to strains isolated from moribund/dead animals in aquaculture environments, this study provides new insights into the role of accessory genetic elements in the evolution, adaptation and diversification of the shellfish pathogen <i>V. europaeus</i>. The findings reveal the complexity and plasticity of its pangenome and highlight the importance of RGPs and plasmids in bacterial fitness.