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 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.

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Prebiotics and community composition influence gas production of the human gut microbiota

10.1101/2020.01.30.928085 ◽

2020 ◽

Author(s):

Xiaoqian Yu ◽

Thomas Gurry ◽

Le Thanh Tu Nguyen ◽

Hunter S. Richardson ◽

Eric J. Alm

Keyword(s):

Fatty Acids ◽

Chemical Composition ◽

Gut Microbiota ◽

Community Composition ◽

Human Body ◽

Ex Vivo ◽

Short Chain Fatty Acids ◽

Gas Production ◽

Human Gut ◽

Human Gut Microbiota

AbstractPrebiotics 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 byproduct 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 is affected by the chemical composition of the prebiotic and by the composition of the microbiota. We first constructed a linear systems model based on mass and electron balance and compared the theoretical product range 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 inter-individual differences in H2 production during inulin degradation was 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 like methanogenesis depend more strongly on microbiome composition.ImportancePrebiotic fermentation in the gut often leads to the co-production 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 taken into account 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 was strongly affected by the oxidation state of the probiotic, while rare metabolisms such as methane production was less affected by the chemical nature of the substrate and entirely dependent on the presence of Methanobacteria in the microbiota.

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Effect of resistant starch structure on short-chain fatty acids production by human gut microbiota fermentation in vitro

Starch - Stärke ◽

10.1002/star.201200166 ◽

2013 ◽

Vol 65 (5-6) ◽

pp. 509-516 ◽

Cited By ~ 22

Author(s):

Zhongkai Zhou ◽

Xiaohong Cao ◽

Julia Y. H. Zhou

Keyword(s):

Fatty Acids ◽

Gut Microbiota ◽

Resistant Starch ◽

Short Chain Fatty Acids ◽

Short Chain ◽

Human Gut ◽

Human Gut Microbiota ◽

Starch Structure ◽

Chain Fatty Acids

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Functional heterogeneity in the fermentation capabilities of the healthy human gut microbiota

10.1101/2020.01.17.910638 ◽

2020 ◽

Cited By ~ 3

Author(s):

Thomas Gurry ◽

Le Thanh Tu Nguyen ◽

Xiaoqian Yu ◽

Eric J Alm

Keyword(s):

Gut Microbiota ◽

Therapeutic Strategy ◽

Ex Vivo ◽

Short Chain Fatty Acids ◽

Human Gut ◽

Healthy Human ◽

Human Gut Microbiota ◽

Functional Differences ◽

Rrna Sequencing

AbstractThe human gut microbiota is known for its highly heterogeneous composition across different individuals. However, relatively little is known about functional differences in its ability to ferment complex polysaccharides. Through ex vivo measurements from healthy human donors, we show that individuals vary markedly in their microbial metabolic phenotypes (MMPs), mirroring differences in their microbiota composition, and resulting in the production of different quantities and proportions of Short Chain Fatty Acids (SCFAs) from the same inputs. We also show that aspects of these MMPs can be predicted from composition using 16S rRNA sequencing. From experiments performed using the same dietary fibers in vivo, we demonstrate that an ingested bolus of fiber is almost entirely consumed by the microbiota upon passage. We leverage our ex vivo data to construct a model of SCFA production and absorption in vivo, and argue that inter-individual differences in quantities of absorbed SCFA are directly related to differences in production. Taken together, these data suggest that personalized dietary fiber supplementation based on an individual’s MMP is an attractive therapeutic strategy for treating diseases associated with SCFA production.

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Functional heterogeneity in the fermentation capabilities of the healthy human gut microbiota

PLoS ONE ◽

10.1371/journal.pone.0254004 ◽

2021 ◽

Vol 16 (7) ◽

pp. e0254004

Author(s):

Thomas Gurry ◽

Le Thanh Tu Nguyen ◽

Xiaoqian Yu ◽

Eric J. Alm

Keyword(s):

Gut Microbiota ◽

Ex Vivo ◽

Short Chain Fatty Acids ◽

Human Gut ◽

Healthy Human ◽

Human Gut Microbiota ◽

Functional Differences ◽

Rrna Sequencing ◽

Quantitative Understanding

The human gut microbiota is known for its highly heterogeneous composition across different individuals. However, relatively little is known about functional differences in its ability to ferment complex polysaccharides. Through ex vivo measurements from healthy human donors, we show that individuals vary markedly in their microbial metabolic phenotypes (MMPs), mirroring differences in their microbiota composition, and resulting in the production of different quantities and proportions of Short Chain Fatty Acids (SCFAs) from the same inputs. We also show that aspects of these MMPs can be predicted from composition using 16S rRNA sequencing. From experiments performed using the same dietary fibers in vivo, we demonstrate that an ingested bolus of fiber is almost entirely consumed by the microbiota upon passage. We leverage our ex vivo data to construct a model of SCFA production and absorption in vivo, and argue that inter-individual differences in quantities of absorbed SCFA are directly related to differences in production. Though in vivo studies are required to confirm these data in the context of the gut, in addition to in vivo read outs of SCFAs produced in response to specific fiber spike-ins, these data suggest that optimizing SCFA production in a given individual through targeted fiber supplementation requires quantitative understanding of their MMP.

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Microbiota-Associated Metabolites and Related Immunoregulation in Colorectal Cancer

Cancers ◽

10.3390/cancers13164054 ◽

2021 ◽

Vol 13 (16) ◽

pp. 4054

Author(s):

Yan Chen ◽

Ying-Xuan Chen

Keyword(s):

Colorectal Cancer ◽

Fatty Acids ◽

Gut Microbiota ◽

Immune Responses ◽

Short Chain Fatty Acids ◽

Short Chain ◽

Indole Derivatives ◽

Human Gut ◽

Growing Body ◽

Specific Influence

A growing body of research has found close links between the human gut microbiota and colorectal cancer (CRC), associated with the direct actions of specific bacteria and the activities of microbiota-derived metabolites, which are implicated in complex immune responses, thus influencing carcinogenesis. Diet has a significant impact on the structure of the microbiota and also undergoes microbial metabolism. Some metabolites, such as short-chain fatty acids (SCFAs) and indole derivatives, act as protectors against cancer by regulating immune responses, while others may promote cancer. However, the specific influence of these metabolites on the host is conditional. We reviewed the recent insights on the relationships among diet, microbiota-derived metabolites, and CRC, focusing on their intricate immunomodulatory responses, which might influence the progression of colorectal cancer.

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Dietary Fatty Acids Sustain the Growth of the Human Gut Microbiota

Applied and Environmental Microbiology ◽

10.1128/aem.01525-18 ◽

2018 ◽

Vol 84 (21) ◽

Cited By ~ 21

Author(s):

Richard Agans ◽

Alex Gordon ◽

Denise Lynette Kramer ◽

Sergio Perez-Burillo ◽

José A. Rufián-Henares ◽

...

Keyword(s):

Fatty Acids ◽

Small Intestine ◽

Fatty Acid ◽

Gut Microbiota ◽

Short Chain Fatty Acids ◽

Dietary Fatty Acids ◽

Dietary Fats ◽

High Fat ◽

Human Gut ◽

Content Type

ABSTRACTWhile a substantial amount of dietary fats escape absorption in the human small intestine and reach the colon, the ability of resident microbiota to utilize these dietary fats for growth has not been investigated in detail. In this study, we used anin vitromultivessel simulator system of the human colon to reveal that the human gut microbiota is able to utilize typically consumed dietary fatty acids to sustain growth. Gut microbiota adapted quickly to a macronutrient switch from a balanced Western diet-type medium to its variant lacking carbohydrates and proteins. We defined specific genera that increased in their abundances on the fats-only medium, includingAlistipes,Bilophila, and several genera of the classGammaproteobacteria. In contrast, the abundances of well-known glycan and protein degraders, includingBacteroides,Clostridium, andRoseburiaspp., were reduced under such conditions. The predicted prevalences of microbial genes coding for fatty acid degradation enzymes and anaerobic respiratory reductases were significantly increased in the fats-only environment, whereas the abundance of glycan degradation genes was diminished. These changes also resulted in lower microbial production of short-chain fatty acids and antioxidants. Our findings provide justification for the previously observed alterations in gut microbiota observed in human and animal studies of high-fat diets.IMPORTANCEIncreased intake of fats in many developed countries has raised awareness of potentially harmful and beneficial effects of high fat consumption on human health. Some dietary fats escape digestion in the small intestine and reach the colon where they can be metabolized by gut microbiota. We show that human gut microbes are able to maintain a complex community when supplied with dietary fatty acids as the only nutrient and carbon sources. Such fatty acid-based growth leads to lower production of short-chain fatty acids and antioxidants by community members, which potentially have negative health consequences on the host.

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Enrichment of Food With Tannin Extracts Promotes Healthy Changes in the Human Gut Microbiota

Frontiers in Microbiology ◽

10.3389/fmicb.2021.625782 ◽

2021 ◽

Vol 12 ◽

Author(s):

Silvia Molino ◽

Alberto Lerma-Aguilera ◽

Nuria Jiménez-Hernández ◽

María José Gosalbes ◽

José Ángel Rufián-Henares ◽

...

Keyword(s):

Gut Microbiota ◽

Short Chain Fatty Acids ◽

Human Gut ◽

Human Gut Microbiota ◽

Wood Extracts ◽

Potential Benefits ◽

Next Generation Sequencing Ngs ◽

Generation Sequencing ◽

Booster Effect

Food and food bioactive components are major drivers of modulation of the human gut microbiota. Tannin extracts consist of a mix of bioactive compounds, which are already exploited in the food industry for their chemical and sensorial properties. The aim of our study was to explore the viability of associations between tannin wood extracts of different origin and food as gut microbiota modulators. 16S rRNA amplicon next-generation sequencing (NGS) was used to test the effects on the gut microbiota of tannin extracts from quebracho, chestnut, and tara associated with commercial food products with different composition in macronutrients. The different tannin-enriched and non-enriched foods were submitted to in vitro digestion and fermentation by the gut microbiota of healthy subjects. The profile of the short chain fatty acids (SCFAs) produced by the microbiota was also investigated. The presence of tannin extracts in food promoted an increase of the relative abundance of the genus Akkermansia, recognized as a marker of a healthy gut, and of various members of the Lachnospiraceae and Ruminococcaceae families, involved in SCFA production. The enrichment of foods with tannin extracts had a booster effect on the production of SCFAs, without altering the profile given by the foods alone. These preliminary results suggest a positive modulation of the gut microbiota with potential benefits for human health through the enrichment of foods with tannin extracts.

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