Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production

Gary D Wu, Charlene Compher, Eric Z Chen, Sarah A Smith, Rachana D Shah, Kyle Bittinger, Christel Chehoud, Lindsey G Albenberg, Lisa Nessel, Erin Gilroy, Julie Star, Aalim M Weljie, Harry J Flint, David C Metz, Michael J Bennett, Hongzhe Li, Frederic D Bushman, James D Lewis

Research output: Contribution to journalArticle

154 Citations (Scopus)

Abstract

OBJECTIVE: The consumption of an agrarian diet is associated with a reduced risk for many diseases associated with a 'Westernised' lifestyle. Studies suggest that diet affects the gut microbiota, which subsequently influences the metabolome, thereby connecting diet, microbiota and health. However, the degree to which diet influences the composition of the gut microbiota is controversial. Murine models and studies comparing the gut microbiota in humans residing in agrarian versus Western societies suggest that the influence is large. To separate global environmental influences from dietary influences, we characterised the gut microbiota and the host metabolome of individuals consuming an agrarian diet in Western society.

DESIGN AND RESULTS: Using 16S rRNA-tagged sequencing as well as plasma and urinary metabolomic platforms, we compared measures of dietary intake, gut microbiota composition and the plasma metabolome between healthy human vegans and omnivores, sampled in an urban USA environment. Plasma metabolome of vegans differed markedly from omnivores but the gut microbiota was surprisingly similar. Unlike prior studies of individuals living in agrarian societies, higher consumption of fermentable substrate in vegans was not associated with higher levels of faecal short chain fatty acids, a finding confirmed in a 10-day controlled feeding experiment. Similarly, the proportion of vegans capable of producing equol, a soy-based gut microbiota metabolite, was less than that was reported in Asian societies despite the high consumption of soy-based products.

CONCLUSIONS: Evidently, residence in globally distinct societies helps determine the composition of the gut microbiota that, in turn, influences the production of diet-dependent gut microbial metabolites.

Original languageEnglish
Pages (from-to)63-72
Number of pages10
JournalGut
Volume65
Issue number1
Early online date26 Nov 2014
DOIs
Publication statusPublished - Jan 2016

Fingerprint

Metabolomics
Diet
Metabolome
Equol
Vegans
Gastrointestinal Microbiome
Volatile Fatty Acids
Microbiota
Life Style
Health

Cite this

Wu, G. D., Compher, C., Chen, E. Z., Smith, S. A., Shah, R. D., Bittinger, K., ... Lewis, J. D. (2016). Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut, 65(1), 63-72. https://doi.org/10.1136/gutjnl-2014-308209

Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. / Wu, Gary D; Compher, Charlene; Chen, Eric Z; Smith, Sarah A; Shah, Rachana D; Bittinger, Kyle; Chehoud, Christel; Albenberg, Lindsey G; Nessel, Lisa; Gilroy, Erin; Star, Julie; Weljie, Aalim M; Flint, Harry J; Metz, David C; Bennett, Michael J; Li, Hongzhe; Bushman, Frederic D; Lewis, James D.

In: Gut, Vol. 65, No. 1, 01.2016, p. 63-72.

Research output: Contribution to journalArticle

Wu, GD, Compher, C, Chen, EZ, Smith, SA, Shah, RD, Bittinger, K, Chehoud, C, Albenberg, LG, Nessel, L, Gilroy, E, Star, J, Weljie, AM, Flint, HJ, Metz, DC, Bennett, MJ, Li, H, Bushman, FD & Lewis, JD 2016, 'Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production', Gut, vol. 65, no. 1, pp. 63-72. https://doi.org/10.1136/gutjnl-2014-308209
Wu, Gary D ; Compher, Charlene ; Chen, Eric Z ; Smith, Sarah A ; Shah, Rachana D ; Bittinger, Kyle ; Chehoud, Christel ; Albenberg, Lindsey G ; Nessel, Lisa ; Gilroy, Erin ; Star, Julie ; Weljie, Aalim M ; Flint, Harry J ; Metz, David C ; Bennett, Michael J ; Li, Hongzhe ; Bushman, Frederic D ; Lewis, James D. / Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. In: Gut. 2016 ; Vol. 65, No. 1. pp. 63-72.
@article{ec9552a8f69a434ba58e3de41002342f,
title = "Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production",
abstract = "OBJECTIVE: The consumption of an agrarian diet is associated with a reduced risk for many diseases associated with a 'Westernised' lifestyle. Studies suggest that diet affects the gut microbiota, which subsequently influences the metabolome, thereby connecting diet, microbiota and health. However, the degree to which diet influences the composition of the gut microbiota is controversial. Murine models and studies comparing the gut microbiota in humans residing in agrarian versus Western societies suggest that the influence is large. To separate global environmental influences from dietary influences, we characterised the gut microbiota and the host metabolome of individuals consuming an agrarian diet in Western society.DESIGN AND RESULTS: Using 16S rRNA-tagged sequencing as well as plasma and urinary metabolomic platforms, we compared measures of dietary intake, gut microbiota composition and the plasma metabolome between healthy human vegans and omnivores, sampled in an urban USA environment. Plasma metabolome of vegans differed markedly from omnivores but the gut microbiota was surprisingly similar. Unlike prior studies of individuals living in agrarian societies, higher consumption of fermentable substrate in vegans was not associated with higher levels of faecal short chain fatty acids, a finding confirmed in a 10-day controlled feeding experiment. Similarly, the proportion of vegans capable of producing equol, a soy-based gut microbiota metabolite, was less than that was reported in Asian societies despite the high consumption of soy-based products.CONCLUSIONS: Evidently, residence in globally distinct societies helps determine the composition of the gut microbiota that, in turn, influences the production of diet-dependent gut microbial metabolites.",
author = "Wu, {Gary D} and Charlene Compher and Chen, {Eric Z} and Smith, {Sarah A} and Shah, {Rachana D} and Kyle Bittinger and Christel Chehoud and Albenberg, {Lindsey G} and Lisa Nessel and Erin Gilroy and Julie Star and Weljie, {Aalim M} and Flint, {Harry J} and Metz, {David C} and Bennett, {Michael J} and Hongzhe Li and Bushman, {Frederic D} and Lewis, {James D}",
note = "Acknowledgements: This work was supported by Project NIH UH2/3 DK083981 and administrative supplement 04S1 (GDW, FDB and JDL), Scottish Government Food, Land and People programme (HJF), The Molecular Biology Core of the Penn Center for the Molecular Studies in Digestive and Liver Diseases (P30 DK050306), The Joint Penn-CHOP Center for Digestive, Liver and Pancreatic Medicine and Penn Vegan Society. Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions.",
year = "2016",
month = "1",
doi = "10.1136/gutjnl-2014-308209",
language = "English",
volume = "65",
pages = "63--72",
journal = "Gut",
issn = "0017-5749",
publisher = "BMJ Publishing Group",
number = "1",

}

TY - JOUR

T1 - Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production

AU - Wu, Gary D

AU - Compher, Charlene

AU - Chen, Eric Z

AU - Smith, Sarah A

AU - Shah, Rachana D

AU - Bittinger, Kyle

AU - Chehoud, Christel

AU - Albenberg, Lindsey G

AU - Nessel, Lisa

AU - Gilroy, Erin

AU - Star, Julie

AU - Weljie, Aalim M

AU - Flint, Harry J

AU - Metz, David C

AU - Bennett, Michael J

AU - Li, Hongzhe

AU - Bushman, Frederic D

AU - Lewis, James D

N1 - Acknowledgements: This work was supported by Project NIH UH2/3 DK083981 and administrative supplement 04S1 (GDW, FDB and JDL), Scottish Government Food, Land and People programme (HJF), The Molecular Biology Core of the Penn Center for the Molecular Studies in Digestive and Liver Diseases (P30 DK050306), The Joint Penn-CHOP Center for Digestive, Liver and Pancreatic Medicine and Penn Vegan Society. Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://group.bmj.com/group/rights-licensing/permissions.

PY - 2016/1

Y1 - 2016/1

N2 - OBJECTIVE: The consumption of an agrarian diet is associated with a reduced risk for many diseases associated with a 'Westernised' lifestyle. Studies suggest that diet affects the gut microbiota, which subsequently influences the metabolome, thereby connecting diet, microbiota and health. However, the degree to which diet influences the composition of the gut microbiota is controversial. Murine models and studies comparing the gut microbiota in humans residing in agrarian versus Western societies suggest that the influence is large. To separate global environmental influences from dietary influences, we characterised the gut microbiota and the host metabolome of individuals consuming an agrarian diet in Western society.DESIGN AND RESULTS: Using 16S rRNA-tagged sequencing as well as plasma and urinary metabolomic platforms, we compared measures of dietary intake, gut microbiota composition and the plasma metabolome between healthy human vegans and omnivores, sampled in an urban USA environment. Plasma metabolome of vegans differed markedly from omnivores but the gut microbiota was surprisingly similar. Unlike prior studies of individuals living in agrarian societies, higher consumption of fermentable substrate in vegans was not associated with higher levels of faecal short chain fatty acids, a finding confirmed in a 10-day controlled feeding experiment. Similarly, the proportion of vegans capable of producing equol, a soy-based gut microbiota metabolite, was less than that was reported in Asian societies despite the high consumption of soy-based products.CONCLUSIONS: Evidently, residence in globally distinct societies helps determine the composition of the gut microbiota that, in turn, influences the production of diet-dependent gut microbial metabolites.

AB - OBJECTIVE: The consumption of an agrarian diet is associated with a reduced risk for many diseases associated with a 'Westernised' lifestyle. Studies suggest that diet affects the gut microbiota, which subsequently influences the metabolome, thereby connecting diet, microbiota and health. However, the degree to which diet influences the composition of the gut microbiota is controversial. Murine models and studies comparing the gut microbiota in humans residing in agrarian versus Western societies suggest that the influence is large. To separate global environmental influences from dietary influences, we characterised the gut microbiota and the host metabolome of individuals consuming an agrarian diet in Western society.DESIGN AND RESULTS: Using 16S rRNA-tagged sequencing as well as plasma and urinary metabolomic platforms, we compared measures of dietary intake, gut microbiota composition and the plasma metabolome between healthy human vegans and omnivores, sampled in an urban USA environment. Plasma metabolome of vegans differed markedly from omnivores but the gut microbiota was surprisingly similar. Unlike prior studies of individuals living in agrarian societies, higher consumption of fermentable substrate in vegans was not associated with higher levels of faecal short chain fatty acids, a finding confirmed in a 10-day controlled feeding experiment. Similarly, the proportion of vegans capable of producing equol, a soy-based gut microbiota metabolite, was less than that was reported in Asian societies despite the high consumption of soy-based products.CONCLUSIONS: Evidently, residence in globally distinct societies helps determine the composition of the gut microbiota that, in turn, influences the production of diet-dependent gut microbial metabolites.

U2 - 10.1136/gutjnl-2014-308209

DO - 10.1136/gutjnl-2014-308209

M3 - Article

VL - 65

SP - 63

EP - 72

JO - Gut

JF - Gut

SN - 0017-5749

IS - 1

ER -