Simple Porifera holobiont reveals complex interactions between the host, an archaeon, a bacterium, and a phage

The basal metazoan phylum Porifera (sponges) is increasingly used as a model to investigate ecological and evolutionary features of microbe-animal symbioses. However, sponges often host complex microbiomes, which has hampered our understanding of their interactions with their microbial symbionts. Here, we describe the discovery and characterization of the simplest sponge holobiont reported to date, consisting of the deep-sea glass sponge Aphrocallistes beatrix and two newly-described microbial symbionts: an autotrophic ammonia-oxidizing archaeon and a bacterial heterotroph. Omics analyses and metabolic modeling revealed the dependency of the ammonia-oxidizing archaea on sponge-derived ammonia to drive primary production, which in turn supports the bacterium's growth by providing the dicarboxylate fumarate. Furthermore, virus-mediated archaeal lysis appears crucial to overcome the bacterium's vitamin B₁₂ auxotrophy. These findings reveal that the exchanges of vitamin B₁₂ and dicarboxylate may be evolutionarily conserved features of symbiosis as they can also be found in interactions between free-living marine bacteria, and between microbes and plants or diatoms.