Ammonia oxidation and recalcitrant carbon degradation fuel mixotrophic growth in the symbiont community of a deep-sea sponge.

Sponges are important members of shallow-water, benthic ecosystems, where they often rely on their microbial symbionts to acquire organic or inorganic carbon. Sponges are also found in the deep sea, however, how they metabolically interact there with their symbionts remains underexplored. Here, we combined metagenomic, metatranscriptomic and stable-isotope labelling approaches to investigate the metabolic activities of the microbial community of the deep-sea sponge Calyx sp. Approximately 84% of the total estimated microbial abundance was composed of nine heterotrophic phyla, whilst the remaining 16% consisted of two autotrophic ammonia-oxidising archaea. Metatranscriptomic analysis revealed the high expression of genes involved in the degradation of recalcitrant polysaccharides of algal origin, suggesting that an undegraded fraction of marine snow plays a role in the nutrition of this deep-sea holobiont. Additionally, we detected active ammonia oxidation and carbon fixation pathways in the autotrophic community members and, through ex situ incubations with labelled carbonate show a potential to fix 13.67 mg CO2 per g dry weight in a year. This study highlights the mixotrophic lifestyle of a deep-sea sponge microbiome, expanding our knowledge of the sponge-microbe symbiosis in the oligotrophic environment of the deep ocean. Video Abstract.