The novel, wide-spread sponge-associated phylum Spongivicinota shows metabolic complementarity to its sister-phylum Latescibacterota

Abstract Sponges host phylogenetically highly diverse yet stable microbial symbiont communities that underpin the ecological success of the holobiont through functions such as nutrient cycling and secondary metabolite production. Here we describe 17 MAGs recovered from deep-sea sponges that belong to an uncultivated and previously uncharacterised, globally distributed microbial clade historically assigned a variety of placeholder names (AncK6, SAUL, PAUC34f and JAAXHH01). Using comprehensive phylogenetic analyses, we propose the phylum name Spongivicinota for this clade. While members of this group were detected across a range of marine and aquatic environments, their preferred lifestyle appear to be as symbionts of sponges and corals, where they consistently co-occur with members of their sister phylum Latescibacterota. Genome-based metabolic reconstruction supported by transcriptomic evidence reveals a specialisation of the Spongivicinota on the degradation of complex peptides and an enhanced capacity for vitamin B12 and iron uptake, with likely cross-phylum acquisition of vitamins B1, B2, B5 and B7. Several evolutionary divergences between Spongivicinota and Latescibacterota highlight the breadth of possible niches and adaptations these symbionts may exploit in the host environment.