Food Starch Structure Impacts Gut Microbiome Composition

ABSTRACT Starch is a major source of energy in the human diet and is consumed in diverse forms. Resistant starch (RS) escapes small intestinal digestion and is fermented in the colon by the resident microbiota, with beneficial impacts on colonic function and host health, but the impacts of the micro...

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Autores principales: Frederick J. Warren, Naoki M. Fukuma, Deirdre Mikkelsen, Bernadine M. Flanagan, Barbara A. Williams, Allan T. Lisle, Páraic Ó Cuív, Mark Morrison, Michael J. Gidley
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:06510caff8004017ad2bea7da095cb412021-11-15T15:24:22ZFood Starch Structure Impacts Gut Microbiome Composition10.1128/mSphere.00086-182379-5042https://doaj.org/article/06510caff8004017ad2bea7da095cb412018-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00086-18https://doaj.org/toc/2379-5042ABSTRACT Starch is a major source of energy in the human diet and is consumed in diverse forms. Resistant starch (RS) escapes small intestinal digestion and is fermented in the colon by the resident microbiota, with beneficial impacts on colonic function and host health, but the impacts of the micro- and nanoscale structure of different physical forms of food starch on the broader microbial community have not been described previously. Here, we use a porcine in vitro fermentation model to establish that starch structure dramatically impacts microbiome composition, including the key amylolytic species, and markedly alters both digestion kinetics and fermentation outcomes. We show that three characteristic food forms of starch that survive digestion in the small intestine each give rise to substantial and distinct changes in the microbiome and in fermentation products. Our results highlight the complexity of starch fermentation processes and indicate that not all forms of RS in foods are degraded or fermented in the same way. This work points the way for the design of RS with tailored degradation by defined microbial communities, informed by an understanding of how substrate structure influences the gut microbiome, to improve nutritive value and/or health benefits. IMPORTANCE Dietary starch is a major component in the human diet. A proportion of the starch in our diet escapes digestion in the small intestine and is fermented in the colon. In this study, we use a model of the colon, seeded with porcine feces, in which we investigate the fermentation of a variety of starches with structures typical of those found in foods. We show that the microbial community changes over time in our model colon are highly dependent on the structure of the substrate and how accessible the starch is to colonic microbes. These findings have important implications for how we classify starches reaching the colon and for the design of foods with improved nutritional properties.Frederick J. WarrenNaoki M. FukumaDeirdre MikkelsenBernadine M. FlanaganBarbara A. WilliamsAllan T. LislePáraic Ó CuívMark MorrisonMichael J. GidleyAmerican Society for Microbiologyarticlecarbohydrate structurefermentationmicrobial ecologyresistant starchshort-chain fatty acidsMicrobiologyQR1-502ENmSphere, Vol 3, Iss 3 (2018)
institution DOAJ
collection DOAJ
language EN
topic carbohydrate structure
fermentation
microbial ecology
resistant starch
short-chain fatty acids
Microbiology
QR1-502
spellingShingle carbohydrate structure
fermentation
microbial ecology
resistant starch
short-chain fatty acids
Microbiology
QR1-502
Frederick J. Warren
Naoki M. Fukuma
Deirdre Mikkelsen
Bernadine M. Flanagan
Barbara A. Williams
Allan T. Lisle
Páraic Ó Cuív
Mark Morrison
Michael J. Gidley
Food Starch Structure Impacts Gut Microbiome Composition
description ABSTRACT Starch is a major source of energy in the human diet and is consumed in diverse forms. Resistant starch (RS) escapes small intestinal digestion and is fermented in the colon by the resident microbiota, with beneficial impacts on colonic function and host health, but the impacts of the micro- and nanoscale structure of different physical forms of food starch on the broader microbial community have not been described previously. Here, we use a porcine in vitro fermentation model to establish that starch structure dramatically impacts microbiome composition, including the key amylolytic species, and markedly alters both digestion kinetics and fermentation outcomes. We show that three characteristic food forms of starch that survive digestion in the small intestine each give rise to substantial and distinct changes in the microbiome and in fermentation products. Our results highlight the complexity of starch fermentation processes and indicate that not all forms of RS in foods are degraded or fermented in the same way. This work points the way for the design of RS with tailored degradation by defined microbial communities, informed by an understanding of how substrate structure influences the gut microbiome, to improve nutritive value and/or health benefits. IMPORTANCE Dietary starch is a major component in the human diet. A proportion of the starch in our diet escapes digestion in the small intestine and is fermented in the colon. In this study, we use a model of the colon, seeded with porcine feces, in which we investigate the fermentation of a variety of starches with structures typical of those found in foods. We show that the microbial community changes over time in our model colon are highly dependent on the structure of the substrate and how accessible the starch is to colonic microbes. These findings have important implications for how we classify starches reaching the colon and for the design of foods with improved nutritional properties.
format article
author Frederick J. Warren
Naoki M. Fukuma
Deirdre Mikkelsen
Bernadine M. Flanagan
Barbara A. Williams
Allan T. Lisle
Páraic Ó Cuív
Mark Morrison
Michael J. Gidley
author_facet Frederick J. Warren
Naoki M. Fukuma
Deirdre Mikkelsen
Bernadine M. Flanagan
Barbara A. Williams
Allan T. Lisle
Páraic Ó Cuív
Mark Morrison
Michael J. Gidley
author_sort Frederick J. Warren
title Food Starch Structure Impacts Gut Microbiome Composition
title_short Food Starch Structure Impacts Gut Microbiome Composition
title_full Food Starch Structure Impacts Gut Microbiome Composition
title_fullStr Food Starch Structure Impacts Gut Microbiome Composition
title_full_unstemmed Food Starch Structure Impacts Gut Microbiome Composition
title_sort food starch structure impacts gut microbiome composition
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/06510caff8004017ad2bea7da095cb41
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AT barbaraawilliams foodstarchstructureimpactsgutmicrobiomecomposition
AT allantlisle foodstarchstructureimpactsgutmicrobiomecomposition
AT paraicocuiv foodstarchstructureimpactsgutmicrobiomecomposition
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AT michaeljgidley foodstarchstructureimpactsgutmicrobiomecomposition
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