Inducible prophages modulate symbiotic phenotypes in Sargassum-associated bacteria

Abstract Background Symbioses between primary producers and bacteria are crucial for host growth and niche adaptation. Here, we investigate the role of viruses on the genomic and functional adaptations of bacteria associated with the pelagic algae Sargassum, which has undergone a dramatic range expansion in the Atlantic in the past decade. Results We reconstructed 73 bacterial and 3,963 viral metagenome-assembled genomes (bMAGs and vMAGs, respectively) from coastal Sargassum and surrounding seawater. Sargassum bMAGs were enriched in prophages compared to seawater (28% and 0.02%, respectively), which was not explained by bMAG completion. Roseobacter and Synechococcus bMAGs, abundant members of the Sargassum microbiome, were shared between the algae and seawater but were associated with distinct phages in each environment. Genes related to biofilm formation and quorum sensing were enriched in Sargassum phages, indicating their potential to influence the switch from free-living to algal association in their bacterial host. In-vitro assays with a Sargassum-derived bacterial community depleted of free viruses demonstrated that Sargassum-associated prophages are inducible and that their induction led to a significant decrease in biofilm formation by the bacteria growing on Sargassum media. Conclusions Our data shows that prophages contribute to the flexible genomes in Sargassum-associated bacteria. These prophages encode genes with symbiotic functions, and their induction decreases biofilm formation, an essential capacity for the symbiosis between bacteria and the algae. These results indicate that prophage acquisition and induction contribute to genomic and functional diversification that mediates Sargassum-bacteria symbioses, with potential implications for algae growth.