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Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification

The human gut can be viewed as a flow-through system with a short residence time, a high turnover rate and a spatial gradient of physiological conditions. As a consequence, the gut microbiota is exposed to highly fluctuating environmental determinants presented by the host and diet. Here, we assesse...

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Autores principales: De Paepe, Kim, Verspreet, Joran, Courtin, Christophe M., Van de Wiele, Tom
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976558/
https://www.ncbi.nlm.nih.gov/pubmed/31712738
http://dx.doi.org/10.1038/s41396-019-0550-5
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author De Paepe, Kim
Verspreet, Joran
Courtin, Christophe M.
Van de Wiele, Tom
author_facet De Paepe, Kim
Verspreet, Joran
Courtin, Christophe M.
Van de Wiele, Tom
author_sort De Paepe, Kim
collection PubMed
description The human gut can be viewed as a flow-through system with a short residence time, a high turnover rate and a spatial gradient of physiological conditions. As a consequence, the gut microbiota is exposed to highly fluctuating environmental determinants presented by the host and diet. Here, we assessed the fermentation and colonisation of insoluble wheat bran by faecal microbiota of three individuals at an unprecedented sampling intensity. Time-resolved 16S rRNA gene amplicon sequencing, revealed a dynamic microbial community, characterised by abrupt shifts in composition, delimiting states with a more constant community, giving rise to a succession of bacterial taxa alternately dominating the community over a 72 h timespan. Early stages were dominated by Enterobacteriaceae and Fusobacterium species, growing on the carbohydrate-low, protein rich medium to which wheat bran was supplemented. The onset of wheat bran fermentation, marked by a spike in short chain fatty acid production with an increasing butyrate proportion and an increased endo-1,4-β-xylanase activity, corresponded to donor-dependent proportional increases of Bacteroides ovatus/stercoris, Prevotella copri and Firmicutes species, which were strongly enriched in the bran-attached community. Literature and database searches provided novel insights into the metabolic and growth characteristics underlying the observed succession and colonisation, illustrating the potency of a time-resolved analysis to increase our understanding of gut microbiota dynamics upon dietary modulations.
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spelling pubmed-69765582020-01-29 Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification De Paepe, Kim Verspreet, Joran Courtin, Christophe M. Van de Wiele, Tom ISME J Article The human gut can be viewed as a flow-through system with a short residence time, a high turnover rate and a spatial gradient of physiological conditions. As a consequence, the gut microbiota is exposed to highly fluctuating environmental determinants presented by the host and diet. Here, we assessed the fermentation and colonisation of insoluble wheat bran by faecal microbiota of three individuals at an unprecedented sampling intensity. Time-resolved 16S rRNA gene amplicon sequencing, revealed a dynamic microbial community, characterised by abrupt shifts in composition, delimiting states with a more constant community, giving rise to a succession of bacterial taxa alternately dominating the community over a 72 h timespan. Early stages were dominated by Enterobacteriaceae and Fusobacterium species, growing on the carbohydrate-low, protein rich medium to which wheat bran was supplemented. The onset of wheat bran fermentation, marked by a spike in short chain fatty acid production with an increasing butyrate proportion and an increased endo-1,4-β-xylanase activity, corresponded to donor-dependent proportional increases of Bacteroides ovatus/stercoris, Prevotella copri and Firmicutes species, which were strongly enriched in the bran-attached community. Literature and database searches provided novel insights into the metabolic and growth characteristics underlying the observed succession and colonisation, illustrating the potency of a time-resolved analysis to increase our understanding of gut microbiota dynamics upon dietary modulations. Nature Publishing Group UK 2019-11-11 2020-02 /pmc/articles/PMC6976558/ /pubmed/31712738 http://dx.doi.org/10.1038/s41396-019-0550-5 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
De Paepe, Kim
Verspreet, Joran
Courtin, Christophe M.
Van de Wiele, Tom
Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title_full Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title_fullStr Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title_full_unstemmed Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title_short Microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
title_sort microbial succession during wheat bran fermentation and colonisation by human faecal microbiota as a result of niche diversification
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976558/
https://www.ncbi.nlm.nih.gov/pubmed/31712738
http://dx.doi.org/10.1038/s41396-019-0550-5
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