Characterization of sponge-associatedVerrucomicrobia: microcompartment-based sugar utilization and enhanced toxin-antitoxin modules as features of host-associatedOpitutales

Bacteria of the phylumVerrucomicrobiaare ubiquitous in marine environments and can be found as free-living organisms or as symbionts of eukaryotic hosts. Little is known about host-associatedVerrucomicrobiain the marine environment. Here we reconstructed two genomes of symbioticVerrucomicrobiafrom bacterial metagenomes derived from the Atlanto-Mediterranean spongePetrosia ficiformisand three genomes from strains that we isolated from offshore seawater of the Eastern Mediterranean Sea. Phylogenomic analysis of these five strains indicated that they are all members ofVerrucomicrobiasubdivision 4, orderOpitutales. We compared these novel sponge-associated and seawater-isolated genomes to closely relatedVerrucomicrobia. Genomic analysis revealed thatPlanctomycetes-Verrucomicrobiamicrocompartment gene clusters are enriched in the genomes of symbioticOpitutalesincluding sponge symbionts but not in free-living ones. We hypothesize that in sponge symbionts these microcompartments are used for degradation ofl-fucose andl-rhamnose, which are components of algal and bacterial cell walls and therefore may be found at high concentrations in the sponge tissue. Furthermore, we observed an enrichment of toxin-antitoxin modules in symbioticOpitutales. We suggest that, in sponges, verrucomicrobial symbionts utilize these modules as a defence mechanism against antimicrobial activity deriving from the abundant microbial community co-inhabiting the host.