Cross-Feeding and Enzymatic Catabolism for Mannan-Oligosaccharide Utilization by the Butyrate-Producing Gut Bacterium Roseburia hominis A2-183

Bhattacharya, Abhishek; Majtorp, Lovisa; Birgersson, Simon; Wiemann, Mathias; Sreenivas, Krishnan; Verbrugghe, Phebe; Aken, Olivier Van; Niel, Ed W. J. van; Stålbrand, Henrik

doi:10.3390/microorganisms10122496

Cited by 5 publications

(6 citation statements)

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“…For example, the production of succinate by Bacteroidetes strains is intriguing for host homeostasis and inflammation regulation ( 34 ), while the production of GABA, an inhibitory neurotransmitter, could impact anxiety and depression disorders in mammals ( 35 ). In contrast, Firmicutes strains showed increased metabolite production in the presence of glucose and dietary carbohydrates, such as lactic acid ( 36 ). Interestingly, nicotinic acid production by S. variabile and E. rectale, irrespective of the culture condition, suggested a potential link to host nicotinamide adenine dinucleotide biosynthesis and a contribution to a symbiotic relationship in the gut microbiota ( 37 ).…”

Section: Discussionmentioning

confidence: 99%

In-depth characterization of a selection of gut commensal bacteria reveals their functional capacities to metabolize dietary carbohydrates with prebiotic potential

Bedu-Ferrari,

Biscarrat,

Pepke

et al. 2024

mSystems

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The microbial utilization of dietary carbohydrates is closely linked to the pivotal role of the gut microbiome in human health. Inherent to the modulation of complex microbial communities, a prebiotic implies the selective utilization of a specific substrate, relying on the metabolic capacities of targeted microbes. In this study, we investigated the metabolic capacities of 17 commensal bacteria of the human gut microbiome toward dietary carbohydrates with prebiotic potential. First, in vitro experiments allowed the classification of bacterial growth and fermentation profiles in response to various carbon sources, including agave inulin, corn fiber, polydextrose, and citrus pectin. The influence of phylogenetic affiliation appeared to statistically outweigh carbon sources in determining the degree of carbohydrate utilization. Second, we narrowed our focus on six commensal bacteria representative of the Bacteroidetes and Firmicutes phyla to perform an untargeted high-resolution liquid chromatography–mass spectrometry metabolomic analysis: Bacteroides xylanisolvens , Bacteroides thetaiotaomicron , Bacteroides intestinalis , Subdoligranulum variabile , Roseburia intestinalis, and Eubacterium rectale exhibited distinct metabolomic profiles in response to different carbon sources. The relative abundance of bacterial metabolites was significantly influenced by dietary carbohydrates, with these effects being strain-specific and/or carbohydrate-specific. Particularly, the findings indicated an elevation in short-chain fatty acids and other metabolites, including succinate, gamma-aminobutyric acid, and nicotinic acid. These metabolites were associated with putative health benefits. Finally, an RNA-Seq transcriptomic approach provided deeper insights into the underlying mechanisms of carbohydrate metabolization. Restricting our focus on four commensal bacteria, including B. xylanisolvens , B. thetaiotaomicron, S. variabile, and R. intestinalis , carbon sources did significantly modulate the level of bacterial genes related to the enzymatic machinery involved in the metabolization of dietary carbohydrates. This study provides a holistic view of the molecular strategies induced during the dynamic interplay between dietary carbohydrates with prebiotic potential and gut commensal bacteria. IMPORTANCE This study explores at a molecular level the interactions between commensal health-relevant bacteria and dietary carbohydrates holding prebiotic potential. We showed that prebiotic breakdown involves the specific activation of gene expression related to carbohydrate metabolism. We also identified metabolites produced by each bacteria that are potentially related to our digestive health. The characterization of the functional activities of health-relevant bacteria toward prebiotic substances can yield a better application of prebiotics in clinical interventions and personalized nutrition. Overall, this study highlights the importance of identifying the impact of prebiotics at a low resolution of the gut microbiota to characterize the activities of targeted bacteria that can play a crucial role in our health.

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Section: Discussionmentioning

confidence: 99%

In-depth characterization of a selection of gut commensal bacteria reveals their functional capacities to metabolize dietary carbohydrates with prebiotic potential

Bedu-Ferrari,

Biscarrat,

Pepke

et al. 2024

mSystems

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“…Cross-feeding mechanisms between bifidobacteria and potent butyrate-producing microorganisms have been reported by multiple researchers ( Rios-Covian et al, 2015 ; Moens et al, 2016 ; Rivière et al, 2016 ). Moens et al (2016) , for instance, reported specific cross-feeding interactions between different Bifidobacterium species and the butyrate-producing Faecalibacterium prausnitzii when providing the prebiotic inulin as a single nutrient source, while Bhattacharya et al (2022) observed metabolic interactions between Roseburia hominis and Bifidobacterium adolescentis upon dosing beta-mannan-oligosaccharides. Furthermore, the observed butyrogenic potential of EpiCor confirmed findings obtained in previous studies.…”

Section: Discussionmentioning

confidence: 99%

Saccharomyces cerevisiae derived postbiotic alters gut microbiome metabolism in the human distal colon resulting in immunomodulatory potential in vitro

Duysburgh,

Miclotte,

Green

et al. 2024

Front. Microbiol.

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The yeast-based postbiotic EpiCor is a well-studied formulation, consisting of a complex mixture of bioactive molecules. In clinical studies, EpiCor postbiotic has been shown to reduce intestinal symptoms in a constipated population and support mucosal defense in healthy subjects. Anti-inflammatory potential and butyrogenic properties have been reported in vitro, suggesting a possible link between EpiCor’s gut modulatory activity and immunomodulation. The current study used a standardized in vitro gut model, the Simulator of the Human Intestinal Microbial Ecosystem (SHIME®), to obtain a deeper understanding on host-microbiome interactions and potential microbiome modulation following repeated EpiCor administration. It was observed that EpiCor induced a functional shift in carbohydrate fermentation patterns in the proximal colon environment. Epicor promoted an increased abundance of Bifidobacterium in both the proximal and distal colon, affecting overall microbial community structure. Co-occurrence network analysis at the phylum level provided additional evidence of changes in the functional properties of microbial community promoted by EpiCor, increasing positive associations between Actinobacteria with microbes belonging to the Firmicutes phylum. These results, together with a significant increase in butyrate production provide additional support of EpiCor benefits to gut health. Investigation of host-microbiome interactions confirmed the immunomodulatory potential of the applied test product. Specific microbial alterations were observed in the distal colon, with metabotyping indicating that specific metabolic pathways, such as bile acid and tryptophan metabolism, were affected following EpiCor supplementation. These results, especially considering many effects were seen distally, further strengthen the position of EpiCor as a postbiotic with health promoting functionality in the gut, which could be further assessed in vivo.

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“…For example, the production of succinate by Bacteroidetes strains is intriguing for host homeostasis and inflammation regulation [34], while the production of GABA, an inhibitory neurotransmitter, could impact anxiety and depression disorders in mammals [35]. In contrast, Firmicutes strains showed increased metabolite production in the presence of glucose and dietary carbohydrates, such as lactic acid [36]. Interestingly, nicotinic acid production by S.…”

Section: Bacterial Responses To Dietary Carbohydrates Were Significan...mentioning

confidence: 99%

In-depth characterisation of a selection of gut commensal bacteria reveals their functional capacities to metabolise dietary carbohydrates with prebiotic potential

Bedu-Ferrari,

Biscarrat,

Pepke

et al. 2024

Preprint

View full text Add to dashboard Cite

The microbial utilisation of dietary carbohydrates is closely linked to the pivotal role of the gut microbiome in human health. We investigated the metabolic capacities of 17 commensal bacteria of the human gut microbiome toward dietary carbohydrates with prebiotic potential. First,in vitroexperiments allowed the classification of bacterial growth and fermentation profiles in response to carbon sources, including agave inulin, corn fiber, polydextrose and citrus pectin. The influence of phylogenetic affiliation appeared to statistically outweigh carbon sources in determining the degrees of carbohydrate utilisation. Secondly, we focused on six commensal bacteria representative of the Bacteroidetes and Firmicutes phyla to perform an untargeted metabolomic analysis.Bacteroides xylanisolvens,Bacteroides thetaiotaomicron,Bacteroides intestinalis,Subdoligranulum variabile,Roseburia intestinalisandEubacterium rectaleexhibited distinct metabolomic profiles in response to different carbon sources. The relative abundance of bacterial metabolites was significantly influenced by dietary carbohydrates, with these effects being strain-specific and/or carbohydrate-specific. We found an elevation in short-chain fatty acids and other metabolites, including succinate, gamma-aminobutyric acid, and nicotinic acid. These metabolites were associated with putative health benefits. Finally, an RNA-Seq transcriptomic approach provided insights into the underlying mechanisms of carbohydrate metabolisation. Restricting our focus on four commensal bacteria,B. xylanisolvens,B. thetaiotaomicron,S. variabileandR. intestinalis, carbon sources did significantly modulate the level of bacterial genes related to the enzymatic machinery involved in the metabolisation of dietary carbohydrates. This study provides a holistic view of the molecular strategies induced during the dynamic interplay between dietary carbohydrates with prebiotic potential and gut commensal bacteria.

show abstract

Cross-Feeding and Enzymatic Catabolism for Mannan-Oligosaccharide Utilization by the Butyrate-Producing Gut Bacterium Roseburia hominis A2-183

Cited by 5 publications

References 62 publications

In-depth characterization of a selection of gut commensal bacteria reveals their functional capacities to metabolize dietary carbohydrates with prebiotic potential

In-depth characterization of a selection of gut commensal bacteria reveals their functional capacities to metabolize dietary carbohydrates with prebiotic potential

Saccharomyces cerevisiae derived postbiotic alters gut microbiome metabolism in the human distal colon resulting in immunomodulatory potential in vitro

In-depth characterisation of a selection of gut commensal bacteria reveals their functional capacities to metabolise dietary carbohydrates with prebiotic potential

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