Sponges are increasingly recognised as valuable models 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 present a detailed characterisation of the simplest sponge holobiont discovered so far, consisting only of the host, two cellular symbionts and a phage.
Through long-read DNA sequencing, we generated complete genomes for a novel heterotrophic bacterial symbiont, a novel autotrophic ammonia-oxidising archaeal symbiont, and a novel viral lineage. Through transcriptomic analysis, metabolic modelling, and metabolite quantification, we show how ammonia-driven primary production by the archaeon supports the growth of the bacterial symbiont via vitamin and organic carbon provision. This interaction is also mediated by the action of the lytic archaeal virus that changes metabolic fluxes and community dynamics in the holobiont. We also show how host-derived nitrogen and carbon sources support symbiont metabolism and how this in turn may benefit the sponge. Finally, we reveal how metabolic exchanges and viral actions can interact to underpin holobiont stability.
Our analysis of this extremely simple holobiont reveal that the exchange of vitamin B12 and dicarboxylate may be evolutionarily conserved features of symbiosis in more complex metazoan-microbe symbioses, as they can also be found in interactions between free-living marine bacteria, and between microbes and plants or diatoms.