Prevalence, diversity, and parasitism of tailed prophages in <i>Vibrio harveyi</i>

<i>Vibrio harveyi</i>, a pathogenic bacterium, contains prophages that significantly influence its pathogenesis and evolutionary traits. Investigating the prevalence, evolution, and ecological roles of these prophages is of great importance as <i>V. harveyi</i> is responsible for luminous bacteriosis in aquatic organisms. In this study, 13 tailed prophages were identified from 55 globally sourced <i>V. harveyi</i> genomes, with prophage-bacterium junctions precisely annotated. These prophages exhibited distinct parasitic mechanisms, including Mu-type transposition, site-specific recombination, and a plasmid-like non-integrated state, reflecting their adaptive plasticity. Proteome-based phylogenetic analysis classified these prophages into eight subfamilies and nine genera, with half representing novel taxonomic singletons. Network analysis of <i>V. harveyi</i> prophages and a large set of prophages across <i>Vibrio</i> species revealed distinct prophage distribution patterns, including broad cross-species dissemination and clade-specific or strain-specific colonization. Further genomic analysis identified homologs of experimentally validated virulence factors associated with motility and biofilm formation, suggesting a potential role of these prophages in enhancing bacterial pathogenicity and adaptive fitness. CRISPR spacer matching provided the intra-species lytic history for 7 out of 13 identified prophages, underscoring their involvement in horizontal transfer of virulence traits. In summary, this study established a comprehensive genomic database of <i>V. harveyi</i> prophages, shedding light on their diversity, prevalence, and parasitic strategies.IMPORTANCEUnderstanding how prophages parasitize <i>Vibrio harveyi</i> holds significant commercial implications, given the pathogen's notoriety for inducing vibriosis across diverse aquatic species and causing substantial economic losses in the global aquaculture industry. We report here 13 well-curated prophage genomes identified from 55 globally collected <i>V. harveyi</i> genomes. Notably, these prophages exhibited previously unrecognized genomic diversity, along with distinct parasitic strategies and hierarchical distribution patterns. In-depth analysis of their genetic profiles identified multiple homologs of experimentally validated virulence determinants involved in regulating bacterial motility and biofilm formation. Lytic history was detected for over half of these prophages, suggesting their role in driving the dissemination of virulence traits within the species.