Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>

ABSTRACT Ancestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber conte...

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Autores principales:	Gary S. Frost, Gemma E. Walton, Jonathan R. Swann, Arianna Psichas, Adele Costabile, Laura P. Johnson, Matt Sponheimer, Glenn R. Gibson, Timothy G. Barraclough
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5856f932fd41435c896f00eee8fe477c
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spelling	oai:doaj.org-article:5856f932fd41435c896f00eee8fe477c2021-11-15T15:47:38ZImpacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>10.1128/mBio.00853-142150-7511https://doaj.org/article/5856f932fd41435c896f00eee8fe477c2014-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00853-14https://doaj.org/toc/2150-7511ABSTRACT Ancestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber content higher than that of present-day diets. We investigated how diet affects gut microbiota and colon cells by comparing human microbial communities with those from a primate that has an extreme plant-based diet, namely, the gelada baboon, which is a grazer. The effects of potato (high starch) versus grass (high lignin and cellulose) diets on human-derived versus gelada-derived fecal communities were compared in vitro. We especially focused on the production of short-chain fatty acids, which are hypothesized to be key metabolites influencing appetite regulation pathways. The results confirmed that diet has a major effect on bacterial numbers, short-chain fatty acid production, and the release of hormones involved in appetite suppression. The potato diet yielded greater production of short-chain fatty acids and hormone release than the grass diet, even in the gelada cultures, which we had expected should be better adapted to the grass diet. The strong effects of diet on hormone release could not be explained, however, solely by short-chain fatty acid concentrations. Nuclear magnetic resonance spectroscopy found changes in additional metabolites, including betaine and isoleucine, that might play key roles in inhibiting and stimulating appetite suppression pathways. Our study results indicate that a broader array of metabolites might be involved in triggering gut hormone release in humans than previously thought. IMPORTANCE One theory for rising levels of obesity in western populations is that the body’s mechanisms for controlling appetite evolved to match ancestral diets with more low-energy plant foods. We investigated this idea by comparing the effects of diet on appetite suppression pathways via the use of gut bacterial communities from humans and gelada baboons, which are modern-day primates with an extreme diet of low-energy plant food, namely, grass. We found that diet does play a major role in affecting gut bacteria and the production of a hormone that suppresses appetite but not in the direction predicted by the ancestral diet hypothesis. Also, bacterial products were correlated with hormone release that were different from those normally thought to play this role. By comparing microbiota and diets outside the natural range for modern humans, we found a relationship between diet and appetite pathways that was more complex than previously hypothesized on the basis of more-controlled studies of the effects of single compounds.Gary S. FrostGemma E. WaltonJonathan R. SwannArianna PsichasAdele CostabileLaura P. JohnsonMatt SponheimerGlenn R. GibsonTimothy G. BarracloughAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 3 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Gary S. Frost Gemma E. Walton Jonathan R. Swann Arianna Psichas Adele Costabile Laura P. Johnson Matt Sponheimer Glenn R. Gibson Timothy G. Barraclough Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
description	ABSTRACT Ancestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber content higher than that of present-day diets. We investigated how diet affects gut microbiota and colon cells by comparing human microbial communities with those from a primate that has an extreme plant-based diet, namely, the gelada baboon, which is a grazer. The effects of potato (high starch) versus grass (high lignin and cellulose) diets on human-derived versus gelada-derived fecal communities were compared in vitro. We especially focused on the production of short-chain fatty acids, which are hypothesized to be key metabolites influencing appetite regulation pathways. The results confirmed that diet has a major effect on bacterial numbers, short-chain fatty acid production, and the release of hormones involved in appetite suppression. The potato diet yielded greater production of short-chain fatty acids and hormone release than the grass diet, even in the gelada cultures, which we had expected should be better adapted to the grass diet. The strong effects of diet on hormone release could not be explained, however, solely by short-chain fatty acid concentrations. Nuclear magnetic resonance spectroscopy found changes in additional metabolites, including betaine and isoleucine, that might play key roles in inhibiting and stimulating appetite suppression pathways. Our study results indicate that a broader array of metabolites might be involved in triggering gut hormone release in humans than previously thought. IMPORTANCE One theory for rising levels of obesity in western populations is that the body’s mechanisms for controlling appetite evolved to match ancestral diets with more low-energy plant foods. We investigated this idea by comparing the effects of diet on appetite suppression pathways via the use of gut bacterial communities from humans and gelada baboons, which are modern-day primates with an extreme diet of low-energy plant food, namely, grass. We found that diet does play a major role in affecting gut bacteria and the production of a hormone that suppresses appetite but not in the direction predicted by the ancestral diet hypothesis. Also, bacterial products were correlated with hormone release that were different from those normally thought to play this role. By comparing microbiota and diets outside the natural range for modern humans, we found a relationship between diet and appetite pathways that was more complex than previously hypothesized on the basis of more-controlled studies of the effects of single compounds.
format	article
author	Gary S. Frost Gemma E. Walton Jonathan R. Swann Arianna Psichas Adele Costabile Laura P. Johnson Matt Sponheimer Glenn R. Gibson Timothy G. Barraclough
author_facet	Gary S. Frost Gemma E. Walton Jonathan R. Swann Arianna Psichas Adele Costabile Laura P. Johnson Matt Sponheimer Glenn R. Gibson Timothy G. Barraclough
author_sort	Gary S. Frost
title	Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_short	Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_full	Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_fullStr	Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_full_unstemmed	Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>
title_sort	impacts of plant-based foods in ancestral hominin diets on the metabolism and function of gut microbiota <italic toggle="yes">in vitro</italic>
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/5856f932fd41435c896f00eee8fe477c
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Impacts of Plant-Based Foods in Ancestral Hominin Diets on the Metabolism and Function of Gut Microbiota <italic toggle="yes">In Vitro</italic>

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