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Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate

BACKGROUND: Variability in the health effects of dietary fiber might arise from inter-individual differences in the gut microbiota’s ability to ferment these substrates into beneficial metabolites. Our understanding of what drives this individuality is vastly incomplete and will require an ecologica...

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Autores principales: Nguyen, Nguyen K., Deehan, Edward C., Zhang, Zhengxiao, Jin, Mingliang, Baskota, Nami, Perez-Muñoz, Maria Elisa, Cole, Janis, Tuncil, Yunus E., Seethaler, Benjamin, Wang, Ting, Laville, Martine, Delzenne, Nathalie M., Bischoff, Stephan C., Hamaker, Bruce R., Martínez, Inés, Knights, Dan, Bakal, Jeffrey A., Prado, Carla M., Walter, Jens
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439537/
https://www.ncbi.nlm.nih.gov/pubmed/32814582
http://dx.doi.org/10.1186/s40168-020-00887-w
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author Nguyen, Nguyen K.
Deehan, Edward C.
Zhang, Zhengxiao
Jin, Mingliang
Baskota, Nami
Perez-Muñoz, Maria Elisa
Cole, Janis
Tuncil, Yunus E.
Seethaler, Benjamin
Wang, Ting
Laville, Martine
Delzenne, Nathalie M.
Bischoff, Stephan C.
Hamaker, Bruce R.
Martínez, Inés
Knights, Dan
Bakal, Jeffrey A.
Prado, Carla M.
Walter, Jens
author_facet Nguyen, Nguyen K.
Deehan, Edward C.
Zhang, Zhengxiao
Jin, Mingliang
Baskota, Nami
Perez-Muñoz, Maria Elisa
Cole, Janis
Tuncil, Yunus E.
Seethaler, Benjamin
Wang, Ting
Laville, Martine
Delzenne, Nathalie M.
Bischoff, Stephan C.
Hamaker, Bruce R.
Martínez, Inés
Knights, Dan
Bakal, Jeffrey A.
Prado, Carla M.
Walter, Jens
author_sort Nguyen, Nguyen K.
collection PubMed
description BACKGROUND: Variability in the health effects of dietary fiber might arise from inter-individual differences in the gut microbiota’s ability to ferment these substrates into beneficial metabolites. Our understanding of what drives this individuality is vastly incomplete and will require an ecological perspective as microbiomes function as complex inter-connected communities. Here, we performed a parallel two-arm, exploratory randomized controlled trial in 31 adults with overweight and class-I obesity to characterize the effects of long-chain, complex arabinoxylan (n = 15) at high supplementation doses (female: 25 g/day; male: 35 g/day) on gut microbiota composition and short-chain fatty acid production as compared to microcrystalline cellulose (n = 16, non-fermentable control), and integrated the findings using an ecological framework. RESULTS: Arabinoxylan resulted in a global shift in fecal bacterial community composition, reduced α-diversity, and the promotion of specific taxa, including operational taxonomic units related to Bifidobacterium longum, Blautia obeum, and Prevotella copri. Arabinoxylan further increased fecal propionate concentrations (p = 0.012, Friedman’s test), an effect that showed two distinct groupings of temporal responses in participants. The two groups showed differences in compositional shifts of the microbiota (p ≤ 0.025, PERMANOVA), and multiple linear regression (MLR) analyses revealed that the propionate response was predictable through shifts and, to a lesser degree, baseline composition of the microbiota. Principal components (PCs) derived from community data were better predictors in MLR models as compared to single taxa, indicating that arabinoxylan fermentation is the result of multi-species interactions within microbiomes. CONCLUSION: This study showed that long-chain arabinoxylan modulates both microbiota composition and the output of health-relevant SCFAs, providing information for a more targeted application of this fiber. Variation in propionate production was linked to both compositional shifts and baseline composition, with PCs derived from shifts of the global microbial community showing the strongest associations. These findings constitute a proof-of-concept for the merit of an ecological framework that considers features of the wider gut microbial community for the prediction of metabolic outcomes of dietary fiber fermentation. This provides a basis to personalize the use of dietary fiber in nutritional application and to stratify human populations by relevant gut microbiota features to account for the inconsistent health effects in human intervention studies. TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015.
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spelling pubmed-74395372020-08-24 Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate Nguyen, Nguyen K. Deehan, Edward C. Zhang, Zhengxiao Jin, Mingliang Baskota, Nami Perez-Muñoz, Maria Elisa Cole, Janis Tuncil, Yunus E. Seethaler, Benjamin Wang, Ting Laville, Martine Delzenne, Nathalie M. Bischoff, Stephan C. Hamaker, Bruce R. Martínez, Inés Knights, Dan Bakal, Jeffrey A. Prado, Carla M. Walter, Jens Microbiome Research BACKGROUND: Variability in the health effects of dietary fiber might arise from inter-individual differences in the gut microbiota’s ability to ferment these substrates into beneficial metabolites. Our understanding of what drives this individuality is vastly incomplete and will require an ecological perspective as microbiomes function as complex inter-connected communities. Here, we performed a parallel two-arm, exploratory randomized controlled trial in 31 adults with overweight and class-I obesity to characterize the effects of long-chain, complex arabinoxylan (n = 15) at high supplementation doses (female: 25 g/day; male: 35 g/day) on gut microbiota composition and short-chain fatty acid production as compared to microcrystalline cellulose (n = 16, non-fermentable control), and integrated the findings using an ecological framework. RESULTS: Arabinoxylan resulted in a global shift in fecal bacterial community composition, reduced α-diversity, and the promotion of specific taxa, including operational taxonomic units related to Bifidobacterium longum, Blautia obeum, and Prevotella copri. Arabinoxylan further increased fecal propionate concentrations (p = 0.012, Friedman’s test), an effect that showed two distinct groupings of temporal responses in participants. The two groups showed differences in compositional shifts of the microbiota (p ≤ 0.025, PERMANOVA), and multiple linear regression (MLR) analyses revealed that the propionate response was predictable through shifts and, to a lesser degree, baseline composition of the microbiota. Principal components (PCs) derived from community data were better predictors in MLR models as compared to single taxa, indicating that arabinoxylan fermentation is the result of multi-species interactions within microbiomes. CONCLUSION: This study showed that long-chain arabinoxylan modulates both microbiota composition and the output of health-relevant SCFAs, providing information for a more targeted application of this fiber. Variation in propionate production was linked to both compositional shifts and baseline composition, with PCs derived from shifts of the global microbial community showing the strongest associations. These findings constitute a proof-of-concept for the merit of an ecological framework that considers features of the wider gut microbial community for the prediction of metabolic outcomes of dietary fiber fermentation. This provides a basis to personalize the use of dietary fiber in nutritional application and to stratify human populations by relevant gut microbiota features to account for the inconsistent health effects in human intervention studies. TRIAL REGISTRATION: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015. BioMed Central 2020-08-19 /pmc/articles/PMC7439537/ /pubmed/32814582 http://dx.doi.org/10.1186/s40168-020-00887-w Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nguyen, Nguyen K.
Deehan, Edward C.
Zhang, Zhengxiao
Jin, Mingliang
Baskota, Nami
Perez-Muñoz, Maria Elisa
Cole, Janis
Tuncil, Yunus E.
Seethaler, Benjamin
Wang, Ting
Laville, Martine
Delzenne, Nathalie M.
Bischoff, Stephan C.
Hamaker, Bruce R.
Martínez, Inés
Knights, Dan
Bakal, Jeffrey A.
Prado, Carla M.
Walter, Jens
Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title_full Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title_fullStr Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title_full_unstemmed Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title_short Gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
title_sort gut microbiota modulation with long-chain corn bran arabinoxylan in adults with overweight and obesity is linked to an individualized temporal increase in fecal propionate
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439537/
https://www.ncbi.nlm.nih.gov/pubmed/32814582
http://dx.doi.org/10.1186/s40168-020-00887-w
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