Deciphering a marine bone degrading microbiome reveals a complex community effort

The marine bone biome is a complex assemblage of macro- and microorganisms, however the enzymatic repertoire to access bone-derived nutrients remains unknown. The resilient structure of collagen in bones, its main organic component and its interwoven character with inorganic hydroxyapatite makes it however difficult to be exploited as an organic resource. To study the microbial assemblages harnessing organic bone components as nutrients, we conducted field experiments with the placement of bovine and turkey bones at 69 m depth in a Norwegian fjord (Byfjorden, Bergen). Metagenomic sequence analysis was used to assess the functional potential of microbial assemblages from bone surface and the bone eating worm Osedax mucofloris that is a frequent colonizer of whale falls and known to degrade bone. The bone microbiome displayed a surprising taxonomic diversity and novelty revealed by the examination of 59 high quality metagenome assembled genomes from at least 23 different bacterial families. Over 700 enzymes from twelve relevant enzymatic families pertaining to collagenases, peptidases, glycosidases putatively involved in bone degradation were identified. This study allowed us to decipher the bone degrading microbiome that initiates demineralization of inorganic bone components by a closed sulfur biogeochemical cycle between sulfur-oxidizing and sulfur-reducing bacteria leading to a drop in pH and subsequent processing of organic components. An unusually large collagen utilization gene cluster was retrieved from one genome belonging to the γ-proteobacterial genus Colwellia. The gene cluster displayed a significant degree of novelty in comparison to clusters present in closely related Colwellia strains, none yet described in detail.