A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans

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A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans. / Benítez-Páez, Alfonso; Kjølbæk, Louise; Gómez Del Pulgar, Eva M; Brahe, Lena Kirchner; Astrup, Arne; Matysik, Silke; Schött, Hans-Frieder; Krautbauer, Sabrina; Liebisch, Gerhard; Boberska, Joanna; Claus, Sandrine; Rampelli, Simone; Brigidi, Patrizia; Larsen, Lesli Hingstrup; Sanz, Yolanda; MyNewGut Consortium.

In: mSystems, Vol. 4, No. 4, e00209-19, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Benítez-Páez, A, Kjølbæk, L, Gómez Del Pulgar, EM, Brahe, LK, Astrup, A, Matysik, S, Schött, H-F, Krautbauer, S, Liebisch, G, Boberska, J, Claus, S, Rampelli, S, Brigidi, P, Larsen, LH, Sanz, Y & MyNewGut Consortium 2019, 'A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans', mSystems, vol. 4, no. 4, e00209-19. https://doi.org/10.1128/mSystems.00209-19

APA

Benítez-Páez, A., Kjølbæk, L., Gómez Del Pulgar, E. M., Brahe, L. K., Astrup, A., Matysik, S., ... MyNewGut Consortium (2019). A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans. mSystems, 4(4), [e00209-19]. https://doi.org/10.1128/mSystems.00209-19

Vancouver

Benítez-Páez A, Kjølbæk L, Gómez Del Pulgar EM, Brahe LK, Astrup A, Matysik S et al. A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans. mSystems. 2019;4(4). e00209-19. https://doi.org/10.1128/mSystems.00209-19

Author

Benítez-Páez, Alfonso ; Kjølbæk, Louise ; Gómez Del Pulgar, Eva M ; Brahe, Lena Kirchner ; Astrup, Arne ; Matysik, Silke ; Schött, Hans-Frieder ; Krautbauer, Sabrina ; Liebisch, Gerhard ; Boberska, Joanna ; Claus, Sandrine ; Rampelli, Simone ; Brigidi, Patrizia ; Larsen, Lesli Hingstrup ; Sanz, Yolanda ; MyNewGut Consortium. / A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans. In: mSystems. 2019 ; Vol. 4, No. 4.

Bibtex

@article{cbdbe4282cd94f90a1b456343274a1c8,
title = "A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans",
abstract = "Long-term consumption of dietary fiber is generally considered beneficial for weight management and metabolic health, but the results of interventions vary greatly depending on the type of dietary fibers involved. This study provides a comprehensive evaluation of the effects of a specific dietary fiber consisting of a wheat-bran extract enriched in arabinoxylan-oligosaccharides (AXOS) in a human intervention trial. An integrated multi-omics analysis has been carried out to evaluate the effects of an intervention trial with an AXOS-enriched diet in overweight individuals with indices of metabolic syndrome. Microbiome analyses were performed by shotgun DNA sequencing in feces; in-depth metabolomics using nuclear magnetic resonance in fecal, urine, and plasma samples; and massive lipid profiling using mass spectrometry in fecal and serum/plasma samples. In addition to their bifidogenic effect, we observed that AXOS boost the proportion of Prevotella species. Metagenome analysis showed increases in the presence of bacterial genes involved in vitamin/cofactor production, glycan metabolism, and neurotransmitter biosynthesis as a result of AXOS intake. Furthermore, lipidomics analysis revealed reductions in plasma ceramide levels. Finally, we observed associations between Prevotella abundance and short-chain fatty acids (SCFAs) and succinate concentration in feces and identified a potential protective role of Eubacterium rectale against metabolic disease given that its abundance was positively associated with plasma phosphatidylcholine levels, thus hypothetically reducing bioavailability of choline for methylamine biosynthesis. The metagenomics, lipidomics, and metabolomics data integration indicates that sustained consumption of AXOS orchestrates a wide variety of changes in the gut microbiome and the host metabolism that collectively would impact on glucose homeostasis. (This study has been registered at ClinicalTrials.gov under identifier NCT02215343)IMPORTANCE The use of dietary fiber food supplementation as a strategy to reduce the burden of diet-related diseases is a matter of study given its cost-effectiveness and the positive results demonstrated in clinical trials. This multi-omics assessment, on different biological samples of overweight subjects with signs of metabolic syndrome, sheds light on the early and less evident effects of short-term AXOS intake on intestinal microbiota and host metabolism. We observed a deep influence of AXOS on gut microbiota beyond their recognized bifidogenic effect by boosting concomitantly a wide diversity of butyrate producers and Prevotella copri, a microbial species abundant in non-Westernized populations with traditional lifestyle and diets enriched in fresh unprocessed foods. A comprehensive evaluation of hundreds of metabolites unveiled new benefits of the AXOS intake, such as reducing the plasma ceramide levels. Globally, we observed that multiple effects of AXOS consumption seem to converge in reversing the glucose homeostasis impairment.This study has been registered at ClinicalTrials.gov under identifier NCT02215343.",
keywords = "Faculty of Science, AXOS, Dietary fiber, Glucose homeostasis, Lipidomics, Metabolic syndrome, Metabolomics, Microbiome, Overweight",
author = "Alfonso Ben{\'i}tez-P{\'a}ez and Louise Kj{\o}lb{\ae}k and {G{\'o}mez Del Pulgar}, {Eva M} and Brahe, {Lena Kirchner} and Arne Astrup and Silke Matysik and Hans-Frieder Sch{\"o}tt and Sabrina Krautbauer and Gerhard Liebisch and Joanna Boberska and Sandrine Claus and Simone Rampelli and Patrizia Brigidi and Larsen, {Lesli Hingstrup} and Yolanda Sanz and {MyNewGut Consortium}",
note = "CURIS 2019 NEXS 184 Copyright {\circledC} 2019 Ben{\'i}tez-P{\'a}ez et al.",
year = "2019",
doi = "10.1128/mSystems.00209-19",
language = "English",
volume = "4",
journal = "mSystems",
issn = "2379-5077",
publisher = "American Society for Microbiology",
number = "4",

}

RIS

TY - JOUR

T1 - A multi-omics approach to unraveling the microbiome-mediated effects of arabinoxylan oligosaccharides in overweight humans

AU - Benítez-Páez, Alfonso

AU - Kjølbæk, Louise

AU - Gómez Del Pulgar, Eva M

AU - Brahe, Lena Kirchner

AU - Astrup, Arne

AU - Matysik, Silke

AU - Schött, Hans-Frieder

AU - Krautbauer, Sabrina

AU - Liebisch, Gerhard

AU - Boberska, Joanna

AU - Claus, Sandrine

AU - Rampelli, Simone

AU - Brigidi, Patrizia

AU - Larsen, Lesli Hingstrup

AU - Sanz, Yolanda

AU - MyNewGut Consortium

N1 - CURIS 2019 NEXS 184 Copyright © 2019 Benítez-Páez et al.

PY - 2019

Y1 - 2019

N2 - Long-term consumption of dietary fiber is generally considered beneficial for weight management and metabolic health, but the results of interventions vary greatly depending on the type of dietary fibers involved. This study provides a comprehensive evaluation of the effects of a specific dietary fiber consisting of a wheat-bran extract enriched in arabinoxylan-oligosaccharides (AXOS) in a human intervention trial. An integrated multi-omics analysis has been carried out to evaluate the effects of an intervention trial with an AXOS-enriched diet in overweight individuals with indices of metabolic syndrome. Microbiome analyses were performed by shotgun DNA sequencing in feces; in-depth metabolomics using nuclear magnetic resonance in fecal, urine, and plasma samples; and massive lipid profiling using mass spectrometry in fecal and serum/plasma samples. In addition to their bifidogenic effect, we observed that AXOS boost the proportion of Prevotella species. Metagenome analysis showed increases in the presence of bacterial genes involved in vitamin/cofactor production, glycan metabolism, and neurotransmitter biosynthesis as a result of AXOS intake. Furthermore, lipidomics analysis revealed reductions in plasma ceramide levels. Finally, we observed associations between Prevotella abundance and short-chain fatty acids (SCFAs) and succinate concentration in feces and identified a potential protective role of Eubacterium rectale against metabolic disease given that its abundance was positively associated with plasma phosphatidylcholine levels, thus hypothetically reducing bioavailability of choline for methylamine biosynthesis. The metagenomics, lipidomics, and metabolomics data integration indicates that sustained consumption of AXOS orchestrates a wide variety of changes in the gut microbiome and the host metabolism that collectively would impact on glucose homeostasis. (This study has been registered at ClinicalTrials.gov under identifier NCT02215343)IMPORTANCE The use of dietary fiber food supplementation as a strategy to reduce the burden of diet-related diseases is a matter of study given its cost-effectiveness and the positive results demonstrated in clinical trials. This multi-omics assessment, on different biological samples of overweight subjects with signs of metabolic syndrome, sheds light on the early and less evident effects of short-term AXOS intake on intestinal microbiota and host metabolism. We observed a deep influence of AXOS on gut microbiota beyond their recognized bifidogenic effect by boosting concomitantly a wide diversity of butyrate producers and Prevotella copri, a microbial species abundant in non-Westernized populations with traditional lifestyle and diets enriched in fresh unprocessed foods. A comprehensive evaluation of hundreds of metabolites unveiled new benefits of the AXOS intake, such as reducing the plasma ceramide levels. Globally, we observed that multiple effects of AXOS consumption seem to converge in reversing the glucose homeostasis impairment.This study has been registered at ClinicalTrials.gov under identifier NCT02215343.

AB - Long-term consumption of dietary fiber is generally considered beneficial for weight management and metabolic health, but the results of interventions vary greatly depending on the type of dietary fibers involved. This study provides a comprehensive evaluation of the effects of a specific dietary fiber consisting of a wheat-bran extract enriched in arabinoxylan-oligosaccharides (AXOS) in a human intervention trial. An integrated multi-omics analysis has been carried out to evaluate the effects of an intervention trial with an AXOS-enriched diet in overweight individuals with indices of metabolic syndrome. Microbiome analyses were performed by shotgun DNA sequencing in feces; in-depth metabolomics using nuclear magnetic resonance in fecal, urine, and plasma samples; and massive lipid profiling using mass spectrometry in fecal and serum/plasma samples. In addition to their bifidogenic effect, we observed that AXOS boost the proportion of Prevotella species. Metagenome analysis showed increases in the presence of bacterial genes involved in vitamin/cofactor production, glycan metabolism, and neurotransmitter biosynthesis as a result of AXOS intake. Furthermore, lipidomics analysis revealed reductions in plasma ceramide levels. Finally, we observed associations between Prevotella abundance and short-chain fatty acids (SCFAs) and succinate concentration in feces and identified a potential protective role of Eubacterium rectale against metabolic disease given that its abundance was positively associated with plasma phosphatidylcholine levels, thus hypothetically reducing bioavailability of choline for methylamine biosynthesis. The metagenomics, lipidomics, and metabolomics data integration indicates that sustained consumption of AXOS orchestrates a wide variety of changes in the gut microbiome and the host metabolism that collectively would impact on glucose homeostasis. (This study has been registered at ClinicalTrials.gov under identifier NCT02215343)IMPORTANCE The use of dietary fiber food supplementation as a strategy to reduce the burden of diet-related diseases is a matter of study given its cost-effectiveness and the positive results demonstrated in clinical trials. This multi-omics assessment, on different biological samples of overweight subjects with signs of metabolic syndrome, sheds light on the early and less evident effects of short-term AXOS intake on intestinal microbiota and host metabolism. We observed a deep influence of AXOS on gut microbiota beyond their recognized bifidogenic effect by boosting concomitantly a wide diversity of butyrate producers and Prevotella copri, a microbial species abundant in non-Westernized populations with traditional lifestyle and diets enriched in fresh unprocessed foods. A comprehensive evaluation of hundreds of metabolites unveiled new benefits of the AXOS intake, such as reducing the plasma ceramide levels. Globally, we observed that multiple effects of AXOS consumption seem to converge in reversing the glucose homeostasis impairment.This study has been registered at ClinicalTrials.gov under identifier NCT02215343.

KW - Faculty of Science

KW - AXOS

KW - Dietary fiber

KW - Glucose homeostasis

KW - Lipidomics

KW - Metabolic syndrome

KW - Metabolomics

KW - Microbiome

KW - Overweight

U2 - 10.1128/mSystems.00209-19

DO - 10.1128/mSystems.00209-19

M3 - Journal article

C2 - 31138673

VL - 4

JO - mSystems

JF - mSystems

SN - 2379-5077

IS - 4

M1 - e00209-19

ER -

ID: 221258134