Bacteriophages are the most abundant biological entities in the oceans and play key roles in bacterial activity, diversity and evolution. While extensive research has been conducted on the role of tailed viruses (Class: Caudoviricetes), very little is known about the distribution and functions of the non-tailed viruses (Class: Tectiliviricetes). The recent discovery of the lytic Autolykiviridae family demonstrated the potential importance of this structural lineage, emphasizing the need for further exploration of the role of this group of marine viruses. Here, we report the novel family of temperate phages under the class of Tectiliviricetes, which we propose to name “Asemoviridae” with phage NO16 as a main representative. These phages are widely distributed across geographical regions and isolation sources and found inside the genomes of at least 30 species of Vibrio, in addition to the original V. anguillarum isolation host. Genomic analysis identified dif-like sites, suggesting that NO16 prophages recombine with the bacterial genome based on the XerCD site-specific recombination mechanism. The interactions between the NO16 phage and its V. anguillarum host were linked to cell density and phage–host ratio. High cell density and low phage predation levels were shown to favor the temperate over the lytic lifestyle for NO16 viruses, and their spontaneous induction rate was highly variable between different V. anguillarum lysogenic strains. NO16 prophages coexist with the V. anguillarum host in a mutualistic interaction by rendering fitness properties to the host, such as increased virulence and biofilm formation through lysogenic conversion, likely contributing to their global distribution.

Understanding host-specific phage diversity is essential for deciphering the complex dynamics shaping microbial ecology and evolution. However, the lack of inherent host associations between uncultivated bacteria and their viruses remains a major limitation to understanding the drivers of viral diversity and its role in bacterial ecology, particularly given the intricate specificity of phage-host interactions. The naturally low complexity of the gut microbiota within piscivorous fish, such as Atlantic salmon (Salmo salar), makes it a valuable model for unravelling ecological patterns of viral diversity in the context of a limited bacterial species composition, and to explore the impact of an invading pathogen on the ‘steady-state’ viral community. The intestinal microbiota of the salmon studied here, was in some cases dominated by a salmon-associated Mycoplasma or increasing levels of an opportunistic Aliivibrio, the latter observed in response to a disease outbreak. The two bacteria are distinctively different in their ecological strategies and their overall genomic and functional properties. A pronounced difference was observed in the gut viral communities and diversity, depending on whether it was dominated by a commensal or an invading bacterial species. Samples dominated by Mycoplasma sp. had few to no viruses, whereas samples dominated by Aliivibrio sp. had viral communities comprising up to 22 viral taxonomic operational units. This study provides unique insights into the significance of bacterial ecological trade-offs linked to niche adaptation and how these affect the associated viral communities in a natural host-controlled environment.