H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers
Abstract Background Hydrogen gas (H2) is a common product of carbohydrate fermentation in the human gut microbiome and its accumulation can modulate fermentation. Concentrations of colonic H2 vary between individuals, raising the possibility that H2 concentration may be an important factor different...
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| Format: | Article |
| Language: | English |
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BMC
2023-06-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01565-3 |
| _version_ | 1797801300973322240 |
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| author | Austin Campbell Kristi Gdanetz Alexander W. Schmidt Thomas M. Schmidt |
| author_facet | Austin Campbell Kristi Gdanetz Alexander W. Schmidt Thomas M. Schmidt |
| author_sort | Austin Campbell |
| collection | DOAJ |
| description | Abstract Background Hydrogen gas (H2) is a common product of carbohydrate fermentation in the human gut microbiome and its accumulation can modulate fermentation. Concentrations of colonic H2 vary between individuals, raising the possibility that H2 concentration may be an important factor differentiating individual microbiomes and their metabolites. Butyrate-producing bacteria (butyrogens) in the human gut usually produce some combination of butyrate, lactate, formate, acetate, and H2 in branched fermentation pathways to manage reducing power generated during the oxidation of glucose to acetate and carbon dioxide. We predicted that a high concentration of intestinal H2 would favor the production of butyrate, lactate, and formate by the butyrogens at the expense of acetate, H2, and CO2. Regulation of butyrate production in the human gut is of particular interest due to its role as a mediator of colonic health through anti-inflammatory and anti-carcinogenic properties. Results For butyrogens that contained a hydrogenase, growth under a high H2 atmosphere or in the presence of the hydrogenase inhibitor CO stimulated production of organic fermentation products that accommodate reducing power generated during glycolysis, specifically butyrate, lactate, and formate. Also as expected, production of fermentation products in cultures of Faecalibacterium prausnitzii strain A2-165, which does not contain a hydrogenase, was unaffected by H2 or CO. In a synthetic gut microbial community, addition of the H2-consuming human gut methanogen Methanobrevibacter smithii decreased butyrate production alongside H2 concentration. Consistent with this observation, M. smithii metabolic activity in a large human cohort was associated with decreased fecal butyrate, but only during consumption of a resistant starch dietary supplement, suggesting the effect may be most prominent when H2 production in the gut is especially high. Addition of M. smithii to the synthetic communities also facilitated the growth of E. rectale, resulting in decreased relative competitive fitness of F. prausnitzii. Conclusions H2 is a regulator of fermentation in the human gut microbiome. In particular, high H2 concentration stimulates production of the anti-inflammatory metabolite butyrate. By consuming H2, gut methanogenesis can decrease butyrate production. These shifts in butyrate production may also impact the competitive fitness of butyrate producers in the gut microbiome. Video Abstract |
| first_indexed | 2024-03-13T04:48:22Z |
| format | Article |
| id | doaj.art-508e87466cc345efa61e200a1632778e |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-13T04:48:22Z |
| publishDate | 2023-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-508e87466cc345efa61e200a1632778e2023-06-18T11:20:07ZengBMCMicrobiome2049-26182023-06-0111111510.1186/s40168-023-01565-3H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producersAustin Campbell0Kristi Gdanetz1Alexander W. Schmidt2Thomas M. Schmidt3Department of Microbiology and Immunology, University of MichiganDepartment of Plant, Soil, and Microbial Sciences, Michigan State UniversityDepartment of Internal Medicine, Division of Infectious Diseases, University of MichiganDepartment of Microbiology and Immunology, University of MichiganAbstract Background Hydrogen gas (H2) is a common product of carbohydrate fermentation in the human gut microbiome and its accumulation can modulate fermentation. Concentrations of colonic H2 vary between individuals, raising the possibility that H2 concentration may be an important factor differentiating individual microbiomes and their metabolites. Butyrate-producing bacteria (butyrogens) in the human gut usually produce some combination of butyrate, lactate, formate, acetate, and H2 in branched fermentation pathways to manage reducing power generated during the oxidation of glucose to acetate and carbon dioxide. We predicted that a high concentration of intestinal H2 would favor the production of butyrate, lactate, and formate by the butyrogens at the expense of acetate, H2, and CO2. Regulation of butyrate production in the human gut is of particular interest due to its role as a mediator of colonic health through anti-inflammatory and anti-carcinogenic properties. Results For butyrogens that contained a hydrogenase, growth under a high H2 atmosphere or in the presence of the hydrogenase inhibitor CO stimulated production of organic fermentation products that accommodate reducing power generated during glycolysis, specifically butyrate, lactate, and formate. Also as expected, production of fermentation products in cultures of Faecalibacterium prausnitzii strain A2-165, which does not contain a hydrogenase, was unaffected by H2 or CO. In a synthetic gut microbial community, addition of the H2-consuming human gut methanogen Methanobrevibacter smithii decreased butyrate production alongside H2 concentration. Consistent with this observation, M. smithii metabolic activity in a large human cohort was associated with decreased fecal butyrate, but only during consumption of a resistant starch dietary supplement, suggesting the effect may be most prominent when H2 production in the gut is especially high. Addition of M. smithii to the synthetic communities also facilitated the growth of E. rectale, resulting in decreased relative competitive fitness of F. prausnitzii. Conclusions H2 is a regulator of fermentation in the human gut microbiome. In particular, high H2 concentration stimulates production of the anti-inflammatory metabolite butyrate. By consuming H2, gut methanogenesis can decrease butyrate production. These shifts in butyrate production may also impact the competitive fitness of butyrate producers in the gut microbiome. Video Abstracthttps://doi.org/10.1186/s40168-023-01565-3Gut microbiotaFermentationHydrogen gasButyrateMethanogenResistant starch |
| spellingShingle | Austin Campbell Kristi Gdanetz Alexander W. Schmidt Thomas M. Schmidt H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers Microbiome Gut microbiota Fermentation Hydrogen gas Butyrate Methanogen Resistant starch |
| title | H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| title_full | H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| title_fullStr | H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| title_full_unstemmed | H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| title_short | H2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| title_sort | h2 generated by fermentation in the human gut microbiome influences metabolism and competitive fitness of gut butyrate producers |
| topic | Gut microbiota Fermentation Hydrogen gas Butyrate Methanogen Resistant starch |
| url | https://doi.org/10.1186/s40168-023-01565-3 |
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