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Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts

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...

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Autores principales: Belzer, Clara, Chia, Loo Wee, Aalvink, Steven, Chamlagain, Bhawani, Piironen, Vieno, Knol, Jan, de Vos, Willem M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5605934/
https://www.ncbi.nlm.nih.gov/pubmed/28928206
http://dx.doi.org/10.1128/mBio.00770-17
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author Belzer, Clara
Chia, Loo Wee
Aalvink, Steven
Chamlagain, Bhawani
Piironen, Vieno
Knol, Jan
de Vos, Willem M.
author_facet Belzer, Clara
Chia, Loo Wee
Aalvink, Steven
Chamlagain, Bhawani
Piironen, Vieno
Knol, Jan
de Vos, Willem M.
author_sort Belzer, Clara
collection PubMed
description 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 B(12) 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.
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spelling pubmed-56059342017-09-28 Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts Belzer, Clara Chia, Loo Wee Aalvink, Steven Chamlagain, Bhawani Piironen, Vieno Knol, Jan de Vos, Willem M. mBio Research Article 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 B(12) 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. American Society for Microbiology 2017-09-19 /pmc/articles/PMC5605934/ /pubmed/28928206 http://dx.doi.org/10.1128/mBio.00770-17 Text en Copyright © 2017 Belzer et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Belzer, Clara
Chia, Loo Wee
Aalvink, Steven
Chamlagain, Bhawani
Piironen, Vieno
Knol, Jan
de Vos, Willem M.
Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title_full Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title_fullStr Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title_full_unstemmed Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title_short Microbial Metabolic Networks at the Mucus Layer Lead to Diet-Independent Butyrate and Vitamin B(12) Production by Intestinal Symbionts
title_sort microbial metabolic networks at the mucus layer lead to diet-independent butyrate and vitamin b(12) production by intestinal symbionts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5605934/
https://www.ncbi.nlm.nih.gov/pubmed/28928206
http://dx.doi.org/10.1128/mBio.00770-17
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