Deciphering a marine bone degrading microbiome reveals a complex community effort

Borchert, Erik, García-Moyano, Antonio, Sanchez-Carrillo, Sergio, Dahlgren, Thomas G., Slaby, Beate M., Bjerga, Gro Elin Kjæreng, Ferrer, Manuel, Franzenburg, Sören and Hentschel, Ute (Submitted) Deciphering a marine bone degrading microbiome reveals a complex community effort bioRxiv . DOI 10.1101/2020.05.13.093005.

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Abstract

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.

Importance In this metagenomic study we decipher the interactions, pathways and enzymes that are necessary to access and utilize the organic bone matrix in the marine microbial space. Bones are an underexploited, yet potentially profitable feedstock for biotechnological advances and value chains, due to the sheer amounts of residues produced by the modern meat and poultry processing industry. We herein demonstrate the interplay between core community members from specialist to generalist and present a toolbox of enzymes with the potential to cover an array of reactions relating to the bone matrix components. We identify and describe a novel gene cluster for collagen utilization. The bone microbiome is a perfect example of an extraordinarily complex microbial assemblage, that is only able to function and survive due to the interplay between the different community members across taxonomic borders.

Document Type: Article
Research affiliation: OceanRep > GEOMAR > FB3 Marine Ecology > FB3-MS Marine Symbioses
Kiel University
Refereed: No
DOI etc.: 10.1101/2020.05.13.093005
Date Deposited: 04 Aug 2020 11:59
Last Modified: 04 Aug 2020 11:59
URI: http://eprints.uni-kiel.de/id/eprint/50270

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