Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota

ABSTRACT Prebiotics confer benefits to human health, often by promoting the growth of gut bacteria that produce metabolites valuable to the human body, such as short-chain fatty acids (SCFAs). While prebiotic selection has strongly focused on maximizing the production of SCFAs, less attention has be...

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Autores principales:	Xiaoqian Yu, Thomas Gurry, Le Thanh Tu Nguyen, Hunter S. Richardson, Eric J. Alm
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	functional heterogeneity gut microbiome intestinal gas prebiotics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3e22db128cac403d8732909e85ec983e
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spelling	oai:doaj.org-article:3e22db128cac403d8732909e85ec983e2021-11-15T16:19:09ZPrebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota10.1128/mBio.00217-202150-7511https://doaj.org/article/3e22db128cac403d8732909e85ec983e2020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00217-20https://doaj.org/toc/2150-7511ABSTRACT Prebiotics confer benefits to human health, often by promoting the growth of gut bacteria that produce metabolites valuable to the human body, such as short-chain fatty acids (SCFAs). While prebiotic selection has strongly focused on maximizing the production of SCFAs, less attention has been paid to gases, a by-product of SCFA production that also has physiological effects on the human body. Here, we investigate how the content and volume of gas production by human gut microbiota are affected by the chemical composition of the prebiotic and the community composition of the microbiota. We first constructed a linear system model based on mass and electron balance and compared the theoretical product ranges of two prebiotics, inulin and pectin. Modeling shows that pectin is more restricted in product space, with less potential for H2 but more potential for CO2 production. An ex vivo experimental system showed pectin degradation produced significantly less H2 than inulin, but CO2 production fell outside the theoretical product range, suggesting fermentation of fecal debris. Microbial community composition also impacted results: methane production was dependent on the presence of Methanobacteria, while interindividual differences in H2 production during inulin degradation were driven by a Lachnospiraceae taxon. Overall, these results suggest that both the chemistry of the prebiotic and the composition of the microbiota are relevant to gas production. Metabolic processes that are relatively prevalent in the microbiome, such as H2 production, will depend more on substrate, while rare metabolisms such as methanogenesis depend more strongly on microbiome composition. IMPORTANCE Prebiotic fermentation in the gut often leads to the coproduction of short-chain fatty acids (SCFAs) and gases. While excess gas production can be a potential problem for those with functional gut disorders, gas production is rarely considered during prebiotic design. In this study, we combined the use of theoretical models and an ex vivo experimental platform to illustrate that both the chemical composition of the prebiotic and the community composition of the human gut microbiota can affect the volume and content of gas production during prebiotic fermentation. Specifically, more prevalent metabolic processes such as hydrogen production were strongly affected by the oxidation state of the probiotic, while rare metabolisms such as methane production were less affected by the chemical nature of the substrate and entirely dependent on the presence of Methanobacteria in the microbiota.Xiaoqian YuThomas GurryLe Thanh Tu NguyenHunter S. RichardsonEric J. AlmAmerican Society for Microbiologyarticlefunctional heterogeneitygut microbiomeintestinal gasprebioticsMicrobiologyQR1-502ENmBio, Vol 11, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	functional heterogeneity gut microbiome intestinal gas prebiotics Microbiology QR1-502
spellingShingle	functional heterogeneity gut microbiome intestinal gas prebiotics Microbiology QR1-502 Xiaoqian Yu Thomas Gurry Le Thanh Tu Nguyen Hunter S. Richardson Eric J. Alm Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
description	ABSTRACT Prebiotics confer benefits to human health, often by promoting the growth of gut bacteria that produce metabolites valuable to the human body, such as short-chain fatty acids (SCFAs). While prebiotic selection has strongly focused on maximizing the production of SCFAs, less attention has been paid to gases, a by-product of SCFA production that also has physiological effects on the human body. Here, we investigate how the content and volume of gas production by human gut microbiota are affected by the chemical composition of the prebiotic and the community composition of the microbiota. We first constructed a linear system model based on mass and electron balance and compared the theoretical product ranges of two prebiotics, inulin and pectin. Modeling shows that pectin is more restricted in product space, with less potential for H2 but more potential for CO2 production. An ex vivo experimental system showed pectin degradation produced significantly less H2 than inulin, but CO2 production fell outside the theoretical product range, suggesting fermentation of fecal debris. Microbial community composition also impacted results: methane production was dependent on the presence of Methanobacteria, while interindividual differences in H2 production during inulin degradation were driven by a Lachnospiraceae taxon. Overall, these results suggest that both the chemistry of the prebiotic and the composition of the microbiota are relevant to gas production. Metabolic processes that are relatively prevalent in the microbiome, such as H2 production, will depend more on substrate, while rare metabolisms such as methanogenesis depend more strongly on microbiome composition. IMPORTANCE Prebiotic fermentation in the gut often leads to the coproduction of short-chain fatty acids (SCFAs) and gases. While excess gas production can be a potential problem for those with functional gut disorders, gas production is rarely considered during prebiotic design. In this study, we combined the use of theoretical models and an ex vivo experimental platform to illustrate that both the chemical composition of the prebiotic and the community composition of the human gut microbiota can affect the volume and content of gas production during prebiotic fermentation. Specifically, more prevalent metabolic processes such as hydrogen production were strongly affected by the oxidation state of the probiotic, while rare metabolisms such as methane production were less affected by the chemical nature of the substrate and entirely dependent on the presence of Methanobacteria in the microbiota.
format	article
author	Xiaoqian Yu Thomas Gurry Le Thanh Tu Nguyen Hunter S. Richardson Eric J. Alm
author_facet	Xiaoqian Yu Thomas Gurry Le Thanh Tu Nguyen Hunter S. Richardson Eric J. Alm
author_sort	Xiaoqian Yu
title	Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
title_short	Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
title_full	Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
title_fullStr	Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
title_full_unstemmed	Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota
title_sort	prebiotics and community composition influence gas production of the human gut microbiota
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/3e22db128cac403d8732909e85ec983e
work_keys_str_mv	AT xiaoqianyu prebioticsandcommunitycompositioninfluencegasproductionofthehumangutmicrobiota AT thomasgurry prebioticsandcommunitycompositioninfluencegasproductionofthehumangutmicrobiota AT lethanhtunguyen prebioticsandcommunitycompositioninfluencegasproductionofthehumangutmicrobiota AT huntersrichardson prebioticsandcommunitycompositioninfluencegasproductionofthehumangutmicrobiota AT ericjalm prebioticsandcommunitycompositioninfluencegasproductionofthehumangutmicrobiota
_version_	1718426899013697536

Prebiotics and Community Composition Influence Gas Production of the Human Gut Microbiota

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