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Background  Deep-sea animals in hydrothermal vents often form endosymbioses with chemosynthetic bacteria. Endosymbionts serve essential biochemical and ecological functions, but the prokaryotic viruses (phages) that determine their fate are unknown.    Results  We conducted metagenomic analysis of a deep-sea vent snail. We assembled four genome bins for  Caudovirales  phages that had developed dual endosymbiosis with sulphur-oxidising bacteria (SOB) and methane-oxidising bacteria (MOB). Clustered regularly interspaced short palindromic repeat (CRISPR) spacer mapping, genome comparison, and transcriptomic profiling revealed that phages Bin1, Bin2, and Bin4 infected SOB and MOB. The observation of prophages in the snail endosymbionts and expression of the phage integrase gene suggested the presence of lysogenic infection, and the expression of phage structural protein and lysozyme genes indicated active lytic infection. Furthermore, SOB and MOB appear to employ adaptive CRISPR–Cas systems to target phage DNA. Additional expressed defence systems, such as innate restriction–modification systems and dormancy-inducing toxin–antitoxin systems, may co-function and form multiple lines for anti-viral defence. To counter host defence, phages Bin1, Bin2, and Bin3 appear to have evolved anti-restriction mechanisms and expressed methyltransferase genes that potentially counterbalance host restriction activity. In addition, the high-level expression of the auxiliary metabolic genes  narGH , which encode nitrate reductase subunits, may promote ATP production, thereby benefiting phage DNA packaging for replication.    Conclusions  This study provides new insights into phage–bacteria interplay in intracellular environments of a deep-sea vent snail.Video AbstractSupplementary Information  The online version contains supplementary material available at 10.1186/s40168-021-01099-6.

Arms race in a cell: genomic, transcriptomic, and proteomic insights into intracellular phage–bacteria interplay in deep-sea snail holobionts