Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Edward C. Deehan; Zhengxiao Zhang; Alessandra Riva; Anissa M. Armet; Maria Elisa Perez-Muñoz; Nguyen K. Nguyen; Jacqueline A. Krysa; Benjamin Seethaler; Yuan-Yuan Zhao; Janis Cole; Fuyong Li; Bela Hausmann; Andreas Spittler; Julie-Anne Nazare; Nathalie M. Delzenne; Jonathan M. Curtis; Wendy V. Wismer; Spencer D. Proctor; Jeffrey A. Bakal; Stephan C. Bischoff; Dan Knights; Catherine J. Field; David Berry; Carla M. Prado; Jens Walter

doi:10.1186/s40168-022-01248-5

Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Edward C. Deehan^* (Co-first Author), Zhengxiao Zhang (Co-first Author), Alessandra Riva, Anissa M. Armet, Maria Elisa Perez-Muñoz, Nguyen K. Nguyen, Jacqueline A. Krysa, Benjamin Seethaler, Yuan-Yuan Zhao, Janis Cole, Fuyong Li, Bela Hausmann, Andreas Spittler, Julie-Anne Nazare, Nathalie M. Delzenne, Jonathan M. Curtis, Wendy V. Wismer, Spencer D. Proctor, Jeffrey A. Bakal, Stephan C. BischoffDan Knights, Catherine J. Field, David Berry, Carla M. Prado, Jens Walter^*

^*Corresponding author for this work

Research output: Journal Publications and Reviews › RGC 21 - Publication in refereed journal › peer-review

88 Citations (Scopus)

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Abstract

Background: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25–35 kg/m²) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers.

Results: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC.

Conclusion: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization.

Trial registration: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015.

Original language	English
Article number	77
Journal	Microbiome
Volume	10
Online published	13 May 2022
DOIs	https://doi.org/10.1186/s40168-022-01248-5
Publication status	Published - 2022
Externally published	Yes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Research Keywords

Adults
Dietary fiber
Gut microbiota
Inflammation
Insulin resistance
Obesity
Satiety

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This full text is made available under CC-BY 4.0. https://creativecommons.org/licenses/by/4.0/

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10.1186/s40168-022-01248-5

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Deehan, E. C., Zhang, Z., Riva, A., Armet, A. M., Perez-Muñoz, M. E., Nguyen, N. K., Krysa, J. A., Seethaler, B., Zhao, Y.-Y., Cole, J., Li, F., Hausmann, B., Spittler, A., Nazare, J.-A., Delzenne, N. M., Curtis, J. M., Wismer, W. V., Proctor, S. D., Bakal, J. A., ... Walter, J. (2022). Elucidating the role of the gut microbiota in the physiological effects of dietary fiber. Microbiome, 10, Article 77. https://doi.org/10.1186/s40168-022-01248-5

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title = "Elucidating the role of the gut microbiota in the physiological effects of dietary fiber",

abstract = "Background: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25–35 kg/m2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. Results: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC. Conclusion: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization. Trial registration: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015.",

keywords = "Adults, Dietary fiber, Gut microbiota, Inflammation, Insulin resistance, Obesity, Satiety",

author = "Deehan, {Edward C.} and Zhengxiao Zhang and Alessandra Riva and Armet, {Anissa M.} and Perez-Mu{\~n}oz, {Maria Elisa} and Nguyen, {Nguyen K.} and Krysa, {Jacqueline A.} and Benjamin Seethaler and Yuan-Yuan Zhao and Janis Cole and Fuyong Li and Bela Hausmann and Andreas Spittler and Julie-Anne Nazare and Delzenne, {Nathalie M.} and Curtis, {Jonathan M.} and Wismer, {Wendy V.} and Proctor, {Spencer D.} and Bakal, {Jeffrey A.} and Bischoff, {Stephan C.} and Dan Knights and Field, {Catherine J.} and David Berry and Prado, {Carla M.} and Jens Walter",

year = "2022",

doi = "10.1186/s40168-022-01248-5",

language = "English",

volume = "10",

journal = "Microbiome",

issn = "2049-2618",

publisher = "BioMed Central Ltd.",

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Deehan, EC, Zhang, Z, Riva, A, Armet, AM, Perez-Muñoz, ME, Nguyen, NK, Krysa, JA, Seethaler, B, Zhao, Y-Y, Cole, J, Li, F, Hausmann, B, Spittler, A, Nazare, J-A, Delzenne, NM, Curtis, JM, Wismer, WV, Proctor, SD, Bakal, JA, Bischoff, SC, Knights, D, Field, CJ, Berry, D, Prado, CM & Walter, J 2022, 'Elucidating the role of the gut microbiota in the physiological effects of dietary fiber', Microbiome, vol. 10, 77. https://doi.org/10.1186/s40168-022-01248-5

TY - JOUR

T1 - Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

AU - Deehan, Edward C.

AU - Zhang, Zhengxiao

AU - Riva, Alessandra

AU - Armet, Anissa M.

AU - Perez-Muñoz, Maria Elisa

AU - Nguyen, Nguyen K.

AU - Krysa, Jacqueline A.

AU - Seethaler, Benjamin

AU - Zhao, Yuan-Yuan

AU - Cole, Janis

AU - Li, Fuyong

AU - Hausmann, Bela

AU - Spittler, Andreas

AU - Nazare, Julie-Anne

AU - Delzenne, Nathalie M.

AU - Curtis, Jonathan M.

AU - Wismer, Wendy V.

AU - Proctor, Spencer D.

AU - Bakal, Jeffrey A.

AU - Bischoff, Stephan C.

AU - Knights, Dan

AU - Field, Catherine J.

AU - Berry, David

AU - Prado, Carla M.

AU - Walter, Jens

PY - 2022

Y1 - 2022

N2 - Background: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25–35 kg/m2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. Results: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC. Conclusion: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization. Trial registration: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015.

AB - Background: Dietary fiber is an integral part of a healthy diet, but questions remain about the mechanisms that underlie effects and the causal contributions of the gut microbiota. Here, we performed a 6-week exploratory trial in adults with excess weight (BMI: 25–35 kg/m2) to compare the effects of a high-dose (females: 25 g/day; males: 35 g/day) supplement of fermentable corn bran arabinoxylan (AX; n = 15) with that of microbiota-non-accessible microcrystalline cellulose (MCC; n = 16). Obesity-related surrogate endpoints and biomarkers of host-microbiome interactions implicated in the pathophysiology of obesity (trimethylamine N-oxide, gut hormones, cytokines, and measures of intestinal barrier integrity) were assessed. We then determined whether clinical outcomes could be predicted by fecal microbiota features or mechanistic biomarkers. Results: AX enhanced satiety after a meal and decreased homeostatic model assessment of insulin resistance (HOMA-IR), while MCC reduced tumor necrosis factor-α and fecal calprotectin. Machine learning models determined that effects on satiety could be predicted by fecal bacterial taxa that utilized AX, as identified by bioorthogonal non-canonical amino acid tagging. Reductions in HOMA-IR and calprotectin were associated with shifts in fecal bile acids, but correlations were negative, suggesting that the benefits of fiber may not be mediated by their effects on bile acid pools. Biomarkers of host-microbiome interactions often linked to bacterial metabolites derived from fiber fermentation (short-chain fatty acids) were not affected by AX supplementation when compared to non-accessible MCC. Conclusion: This study demonstrates the efficacy of purified dietary fibers when used as supplements and suggests that satietogenic effects of AX may be linked to bacterial taxa that ferment the fiber or utilize breakdown products. Other effects are likely microbiome independent. The findings provide a basis for fiber-type specific therapeutic applications and their personalization. Trial registration: Clinicaltrials.gov, NCT02322112, registered on July 3, 2015.

KW - Adults

KW - Dietary fiber

KW - Gut microbiota

KW - Inflammation

KW - Insulin resistance

KW - Obesity

KW - Satiety

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UR - https://www.scopus.com/record/pubmetrics.uri?eid=2-s2.0-85130069099&origin=recordpage

U2 - 10.1186/s40168-022-01248-5

DO - 10.1186/s40168-022-01248-5

M3 - RGC 21 - Publication in refereed journal

C2 - 35562794

SN - 2049-2618

VL - 10

JO - Microbiome

JF - Microbiome

M1 - 77

ER -

Elucidating the role of the gut microbiota in the physiological effects of dietary fiber

Abstract

UN SDGs

Research Keywords

Publisher's Copyright Statement

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