Ca. Nemesobacterales, a sponge-specific clade of Desulfobacterota adapted to symbiotic lifestyle
Members of the candidate phylum Dadabacteria, recently reassigned to the phylum Candidatus Desulfobacterota, are cosmopolitan in the marine environment, and are found both free-living and associated with hosts that are mainly marine sponges. Yet, these microorganisms are poorly characterised, showing an ambiguous phylogeny and having no cultured representatives. Here, we performed genome-centric metagenomics to elucidate the phylogeny and predict the metabolism of the sponge-associated members of this lineage. Rank-based phylogenomics revealed several new species and a novel family (Candidatus Spongomicrobiaceae) within a sponge-specific order, named here Candidatus Nemesobacterales (GTDB order RKRQ01). Metabolic reconstruction suggests that Ca. Nemesobacterales are aerobic heterotrophs, capable of synthesizing most amino acids, vitamins and cofactors and degrading complex carbohydrates. We also report functional divergence between sponge- and seawater-associated metagenome-assembled genomes (MAGs). Niche-specific adaptations to the sponge holobiont were evident from significantly enriched genes involved in defense mechanisms against foreign DNA and environmental stressors, host-symbiont interactions and secondary metabolite production. Fluorescencet in situ hybridization (FISH) gave a first glimpse of the morphology and lifestyle of a member of Ca. Desulfobacterota. The Candidatus Nemesobacterales spp. rappii wereas found inside bacteriocytes in the tissue mesohyl of the sponge Geodia barretti. Altogether, this is the first study that sheds light on the enigmatic group Ca. Nemesobacterales and their functional characteristics which reflect a symbiotic lifestyle.