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Summary  Deep‐sea hydrothermal vents harbour diverse and abundant animals and their symbiotic microorganisms, which together comprise holobionts. The interplay between bacterial members of holobionts and their viruses (phages) is important for maintaining these symbiotic systems; however, phage–bacterium interactions in deep‐sea vent holobionts are not well understood. Marine sponges serve as good models for such studies and are used to unveil phage–bacterium interplay via metagenomic analysis. In three demosponges from deep‐sea hydrothermal vent fields in the southern Okinawa Trough, the genomes of a diverse array of symbiotic bacteria, including 10 bacterial phyla, were found to lack intact prophages. Genes related to diverse anti‐viral defence systems, for example, the restriction–modification and toxin–antitoxin systems, were abundant in the bacterial communities. We also detected phage genes that could complement or compensate host bacterial metabolism, indicating beneficial roles of phage infection. Our findings provide insight into phage–bacterium interplay in sponges from deep‐sea hydrothermal vents.

Unique phage–bacterium interplay in sponge holobionts from the southern Okinawa Trough hydrothermal vent