AbstractSponges thrive in the deep, dark and nutrient-depleted ocean and may rely on microbial symbionts for carbon acquisition and energy generation. However, these symbiotic relationships remain largely unexplored. In this study, we analyze the microbiome of deep-sea sponges and show that ammonia-oxidizing archaea (AOA) of the family Nitrosopumilaceae make up at least 75% of the microbial communities of the sponges Aphrocallistes sp., Farrea sp. and Paratimea sp.. Given the known autotrophic metabolism of AOAs, this implies that these sponge holobionts can have the capacity for primary production in the deep-sea. We also show that specific AOA lineages are highly specific towards their hosts, hinting towards an unprecedent vertical transmission of these symbionts in deep-sea sponges. Our results show that the ecology and evolution of symbiotic relationships in deep-sea sponge is distinct from that of their shallow-water counterparts.