Identification, classification, and functional characterization of novel sponge-associated acidimicrobiial species

Sponges are known to harbour an exceptional diversity of uncultured microorganisms, including members of the phylum Actinobacteriota. While members of the actinobacteriotal class Actinomycetia have been studied intensively due to their potential for secondary metabolite production, the sister class of Acidimicrobiia is often more abundant in sponges. However, the taxonomy, functions, and ecological roles of sponge-associated Acidimicrobiia are largely unknown. Here, we reconstructed and characterized 22 metagenome-assembled genomes (MAGs) of Acidimicrobiia from three sponge species. These MAGs represented six novel species, belonging to five genera, four families, and two orders, which are all uncharacterized (except the order Acidimicrobiales) and for which we propose nomenclature. These six uncultured species have either only been found in sponges and/or corals and have varying degrees of specificity to their host species. Functional gene profiling indicated that these six species shared a similar potential to non-symbiotic Acidimicrobiia with respect to amino acid biosynthesis and utilization of sulfur compounds. However, sponge-associated Acidimicrobiia differed from their non-symbiotic counterparts by relying predominantly on organic rather than inorganic sources of energy, and their predicted capacity to synthesise bioactive compounds or their precursors implicated in host defence. Additionally, the species possess the genetic capacity to degrade aromatic compounds that are frequently found in sponges. The novel Acidimicrobiia may also potentially mediate host development by modulating Hedgehog signalling and by the production of serotonin, which can affect host body contractions and digestion. These results highlight unique genomic and metabolic features of six new acidimicrobiial species that potentially support a sponge-associated lifestyle.