Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts

ABSTRACT Akkermansia muciniphila has evolved to specialize in the degradation and utilization of host mucus, which it may use as the sole source of carbon and nitrogen. Mucus degradation and fermentation by A. muciniphila are known to result in the liberation of oligosaccharides and subsequent produ...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Clara Belzer, Loo Wee Chia, Steven Aalvink, Bhawani Chamlagain, Vieno Piironen, Jan Knol, Willem M. de Vos
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Akkermansia muciniphila anaerobes butyrate cross-feeding intestine microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b09000039f574b05ae08069150e2e76c
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:b09000039f574b05ae08069150e2e76c
record_format	dspace
spelling	oai:doaj.org-article:b09000039f574b05ae08069150e2e76c2021-11-15T15:51:51ZMicrobial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts10.1128/mBio.00770-172150-7511https://doaj.org/article/b09000039f574b05ae08069150e2e76c2017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00770-17https://doaj.org/toc/2150-7511ABSTRACT Akkermansia muciniphila has evolved to specialize in the degradation and utilization of host mucus, which it may use as the sole source of carbon and nitrogen. Mucus degradation and fermentation by A. muciniphila are known to result in the liberation of oligosaccharides and subsequent production of acetate, which becomes directly available to microorganisms in the vicinity of the intestinal mucosa. Coculturing experiments of A. muciniphila with non-mucus-degrading butyrate-producing bacteria Anaerostipes caccae, Eubacterium hallii, and Faecalibacterium prausnitzii resulted in syntrophic growth and production of butyrate. In addition, we demonstrate that the production of pseudovitamin B12 by E. hallii results in production of propionate by A. muciniphila, which suggests that this syntrophy is indeed bidirectional. These data are proof of concept for syntrophic and other symbiotic microbe-microbe interactions at the intestinal mucosal interface. The observed metabolic interactions between A. muciniphila and butyrogenic bacterial taxa support the existence of colonic vitamin and butyrate production pathways that are dependent on host glycan production and independent of dietary carbohydrates. We infer that the intestinal symbiont A. muciniphila can indirectly stimulate intestinal butyrate levels in the vicinity of the intestinal epithelial cells with potential health benefits to the host. IMPORTANCE The intestinal microbiota is said to be a stable ecosystem where many networks between microorganisms are formed. Here we present a proof of principle study of microbial interaction at the intestinal mucus layer. We show that indigestible oligosaccharide chains within mucus become available for a broad range of intestinal microbes after degradation and liberation of sugars by the species Akkermansia muciniphila. This leads to the microbial synthesis of vitamin B12, 1,2-propanediol, propionate, and butyrate, which are beneficial to the microbial ecosystem and host epithelial cells.Clara BelzerLoo Wee ChiaSteven AalvinkBhawani ChamlagainVieno PiironenJan KnolWillem M. de VosAmerican Society for MicrobiologyarticleAkkermansia muciniphilaanaerobesbutyratecross-feedingintestinemicrobiomeMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Akkermansia muciniphila anaerobes butyrate cross-feeding intestine microbiome Microbiology QR1-502
spellingShingle	Akkermansia muciniphila anaerobes butyrate cross-feeding intestine microbiome Microbiology QR1-502 Clara Belzer Loo Wee Chia Steven Aalvink Bhawani Chamlagain Vieno Piironen Jan Knol Willem M. de Vos Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
description	ABSTRACT Akkermansia muciniphila has evolved to specialize in the degradation and utilization of host mucus, which it may use as the sole source of carbon and nitrogen. Mucus degradation and fermentation by A. muciniphila are known to result in the liberation of oligosaccharides and subsequent production of acetate, which becomes directly available to microorganisms in the vicinity of the intestinal mucosa. Coculturing experiments of A. muciniphila with non-mucus-degrading butyrate-producing bacteria Anaerostipes caccae, Eubacterium hallii, and Faecalibacterium prausnitzii resulted in syntrophic growth and production of butyrate. In addition, we demonstrate that the production of pseudovitamin B12 by E. hallii results in production of propionate by A. muciniphila, which suggests that this syntrophy is indeed bidirectional. These data are proof of concept for syntrophic and other symbiotic microbe-microbe interactions at the intestinal mucosal interface. The observed metabolic interactions between A. muciniphila and butyrogenic bacterial taxa support the existence of colonic vitamin and butyrate production pathways that are dependent on host glycan production and independent of dietary carbohydrates. We infer that the intestinal symbiont A. muciniphila can indirectly stimulate intestinal butyrate levels in the vicinity of the intestinal epithelial cells with potential health benefits to the host. IMPORTANCE The intestinal microbiota is said to be a stable ecosystem where many networks between microorganisms are formed. Here we present a proof of principle study of microbial interaction at the intestinal mucus layer. We show that indigestible oligosaccharide chains within mucus become available for a broad range of intestinal microbes after degradation and liberation of sugars by the species Akkermansia muciniphila. This leads to the microbial synthesis of vitamin B12, 1,2-propanediol, propionate, and butyrate, which are beneficial to the microbial ecosystem and host epithelial cells.
format	article
author	Clara Belzer Loo Wee Chia Steven Aalvink Bhawani Chamlagain Vieno Piironen Jan Knol Willem M. de Vos
author_facet	Clara Belzer Loo Wee Chia Steven Aalvink Bhawani Chamlagain Vieno Piironen Jan Knol Willem M. de Vos
author_sort	Clara Belzer
title	Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
title_short	Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
title_full	Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
title_fullStr	Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
title_full_unstemmed	Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts
title_sort	microbial metabolic networks at the mucus layer lead to diet-independent butyrate and vitamin b<sub>12</sub> production by intestinal symbionts
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/b09000039f574b05ae08069150e2e76c
work_keys_str_mv	AT clarabelzer microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT looweechia microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT stevenaalvink microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT bhawanichamlagain microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT vienopiironen microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT janknol microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts AT willemmdevos microbialmetabolicnetworksatthemucuslayerleadtodietindependentbutyrateandvitaminbsub12subproductionbyintestinalsymbionts
_version_	1718427360909328384

Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B<sub>12</sub> Production by Intestinal Symbionts

Ejemplares similares