Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort

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 bone matrix is a composite material made up mainly of organic collagen and inorganic hydroxyapatite. We conducted field experim...

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Autores principales:	Erik Borchert, Antonio García-Moyano, Sergio Sanchez-Carrillo, Thomas G. Dahlgren, Beate M. Slaby, Gro Elin Kjæreng Bjerga, Manuel Ferrer, Sören Franzenburg, Ute Hentschel
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Osedax mucofloris bone biome bone degradation metagenomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/45d1d7075e8c4f05b7ed9d5194fe850b
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spelling	oai:doaj.org-article:45d1d7075e8c4f05b7ed9d5194fe850b2021-12-02T19:22:16ZDeciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort10.1128/mSystems.01218-202379-5077https://doaj.org/article/45d1d7075e8c4f05b7ed9d5194fe850b2021-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01218-20https://doaj.org/toc/2379-5077ABSTRACT The marine bone biome is a complex assemblage of macro- and microorganisms; however, the enzymatic repertoire to access bone-derived nutrients remains unknown. The bone matrix is a composite material made up mainly of organic collagen and inorganic hydroxyapatite. We conducted field experiments to study microbial assemblages that can use organic bone components as nutrient source. Bovine and turkey bones were deposited 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, which is a frequent colonizer of whale falls and known to degrade bone. The bone microbiome displayed a surprising taxonomic diversity revealed by the examination of 59 high-quality metagenome-assembled genomes from at least 23 bacterial families. Over 700 genes encoding enzymes from 12 relevant enzymatic families pertaining to collagenases, peptidases, and glycosidases putatively involved in bone degradation were identified. Metagenome-assembled genomes (MAGs) of the class Bacteroidia contained the most diverse gene repertoires. We postulate that demineralization of inorganic bone components is achieved by a timely succession of a closed sulfur biogeochemical cycle between sulfur-oxidizing and sulfur-reducing bacteria, causing a drop in pH and subsequent enzymatic processing of organic components in the bone surface communities. An unusually large and novel collagen utilization gene cluster was retrieved from one genome belonging to the gammaproteobacterial genus Colwellia. IMPORTANCE 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. In this metagenomic study, we decipher the microbial pathways and enzymes that we postulate to be involved in bone degradation in the marine environment. We here demonstrate the interplay between different bacterial community members, each supplying different enzymatic functions with the potential to cover an array of reactions relating to the degradation of bone matrix components. We identify and describe a novel gene cluster for collagen utilization, which is a key function in this unique environment. We propose that the interplay between the different microbial taxa is necessary to achieve the complex task of bone degradation in the marine environment.Erik BorchertAntonio García-MoyanoSergio Sanchez-CarrilloThomas G. DahlgrenBeate M. SlabyGro Elin Kjæreng BjergaManuel FerrerSören FranzenburgUte HentschelAmerican Society for MicrobiologyarticleOsedax mucoflorisbone biomebone degradationmetagenomicsMicrobiologyQR1-502ENmSystems, Vol 6, Iss 1 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Osedax mucofloris bone biome bone degradation metagenomics Microbiology QR1-502
spellingShingle	Osedax mucofloris bone biome bone degradation metagenomics Microbiology QR1-502 Erik Borchert Antonio García-Moyano Sergio Sanchez-Carrillo Thomas G. Dahlgren Beate M. Slaby Gro Elin Kjæreng Bjerga Manuel Ferrer Sören Franzenburg Ute Hentschel Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
description	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 bone matrix is a composite material made up mainly of organic collagen and inorganic hydroxyapatite. We conducted field experiments to study microbial assemblages that can use organic bone components as nutrient source. Bovine and turkey bones were deposited 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, which is a frequent colonizer of whale falls and known to degrade bone. The bone microbiome displayed a surprising taxonomic diversity revealed by the examination of 59 high-quality metagenome-assembled genomes from at least 23 bacterial families. Over 700 genes encoding enzymes from 12 relevant enzymatic families pertaining to collagenases, peptidases, and glycosidases putatively involved in bone degradation were identified. Metagenome-assembled genomes (MAGs) of the class Bacteroidia contained the most diverse gene repertoires. We postulate that demineralization of inorganic bone components is achieved by a timely succession of a closed sulfur biogeochemical cycle between sulfur-oxidizing and sulfur-reducing bacteria, causing a drop in pH and subsequent enzymatic processing of organic components in the bone surface communities. An unusually large and novel collagen utilization gene cluster was retrieved from one genome belonging to the gammaproteobacterial genus Colwellia. IMPORTANCE 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. In this metagenomic study, we decipher the microbial pathways and enzymes that we postulate to be involved in bone degradation in the marine environment. We here demonstrate the interplay between different bacterial community members, each supplying different enzymatic functions with the potential to cover an array of reactions relating to the degradation of bone matrix components. We identify and describe a novel gene cluster for collagen utilization, which is a key function in this unique environment. We propose that the interplay between the different microbial taxa is necessary to achieve the complex task of bone degradation in the marine environment.
format	article
author	Erik Borchert Antonio García-Moyano Sergio Sanchez-Carrillo Thomas G. Dahlgren Beate M. Slaby Gro Elin Kjæreng Bjerga Manuel Ferrer Sören Franzenburg Ute Hentschel
author_facet	Erik Borchert Antonio García-Moyano Sergio Sanchez-Carrillo Thomas G. Dahlgren Beate M. Slaby Gro Elin Kjæreng Bjerga Manuel Ferrer Sören Franzenburg Ute Hentschel
author_sort	Erik Borchert
title	Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
title_short	Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
title_full	Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
title_fullStr	Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
title_full_unstemmed	Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort
title_sort	deciphering a marine bone-degrading microbiome reveals a complex community effort
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/45d1d7075e8c4f05b7ed9d5194fe850b
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Deciphering a Marine Bone-Degrading Microbiome Reveals a Complex Community Effort

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