Decoding the metagenome of the precious red coral: discovery of a new spirochete lineage and carotenoid-producing bacteria

Abstract The precious red coral Corallium rubrum is an ecologically and economically iconic Mediterranean octocoral, yet the diversity and functions of its microbiome remain a “blackbox” at the genomic scale. Here, we present a genome-resolved metagenomic analysis of C. rubrum , reconstructing 25 high-quality metagenome-assembled genomes (MAGs), including 16 from wild colonies and 9 additional ones from a laboratory colony, to gain insight into the functional potential of its microbiome. Our phylogenomic analysis of the two dominant Spirochaetota symbionts reveals that one of the two symbionts represents a potential novel, previously undescribed lineage, which appears to be exclusively associated with octocoral species. Functional profiling indicates that these Spirochaetota exhibit different metabolic pathways, and are adapted to the symbiotic life, probably representing mutualistic partners for C. rubrum . Their genomes encode biosynthetic pathways of a wide range of essential amino acids and vitamins, and the capacity to ferment sugars to acetate, potentially supplementing host dietary deficiencies. We also identified an interesting symbiont, affiliated with the Qipengyuania genus, that possesses the genomic potential for the biosynthesis of the carotenoid canthaxanthin, one of the main pigments involved in the red color of C. rubrum . The other MAGs encode a wide range of metabolic pathways, especially those linked to nitrogen and sulfur transformations. Our findings suggest potential metabolic interactions between the red coral host and its microbiome. This study offers detailed taxonomic and functional characterization of newly identified octocoral symbionts, establishing a foundation for future investigations into octocoral symbiotic relationships.