Impact of carbohydrate substrate complexity on the diversity of the human colonic microbiota

Chung, Wing Sun Faith; Walker, Alan W.; Vermeiren, Joan; Sheridan, Paul O.; Bosscher, Douwina; Garcia-Campayo, Vicenta; Parkhill, Julian; Flint, Harry J.; Duncan, Sylvia H.

doi:10.1093/femsec/fiy201

Cited by 38 publications

(43 citation statements)

References 37 publications

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“…1c), were consistently lower in the fermentor vessels maintained at pH 5.5 than both the original inocula samples and fermentor vessels at pH 6.5. Similar initial reductions in OTU diversity have been reported previously (28) and are assumed to result mainly from the more limited substrate diversity and constant environmental conditions compared to the situation in vivo. Dead cells derived from higher up in the gastrointestinal tract, which can still be detected in fecal inocula using DNA-based methods, may also be a contributing factor, as these will be rapidly washed out of the fermentor systems as the growth medium is continuously replenished.…”

Section: Resultssupporting

confidence: 78%

Pivotal Roles for pH, Lactate, and Lactate-Utilizing Bacteria in the Stability of a Human Colonic Microbial Ecosystem

et al. 2020

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Lactate can be produced by many gut bacteria, but in adults its accumulation in the colon is often an indicator of microbiota perturbation. Using continuous culture anaerobic fermentor systems, we found that lactate concentrations remained low in communities of human colonic bacteria maintained at pH 6.5, even when dl-lactate was infused at 10 or 20 mM. In contrast, lower pH (5.5) led to periodic lactate accumulation following lactate infusion in three fecal microbial communities examined. Lactate accumulation was concomitant with greatly reduced butyrate and propionate production and major shifts in microbiota composition, with Bacteroidetes and anaerobic Firmicutes being replaced by Actinobacteria, lactobacilli, and Proteobacteria. Pure-culture experiments confirmed that Bacteroides and Firmicutes isolates were susceptible to growth inhibition by relevant concentrations of lactate and acetate, whereas the lactate-producer Bifidobacterium adolescentis was resistant. To investigate system behavior further, we used a mathematical model (microPop) based on 10 microbial functional groups. By incorporating differential growth inhibition, our model reproduced the chaotic behavior of the system, including the potential for lactate infusion both to promote and to rescue the perturbed system. The modeling revealed that system behavior is critically dependent on the proportion of the community able to convert lactate into butyrate or propionate. Communities with low numbers of lactate-utilizing bacteria are inherently less stable and more prone to lactate-induced perturbations. These findings can help us to understand the consequences of interindividual microbiota variation for dietary responses and microbiota changes associated with disease states. IMPORTANCE Lactate is formed by many species of colonic bacteria, and can accumulate to high levels in the colons of inflammatory bowel disease subjects. Conversely, in healthy colons lactate is metabolized by lactate-utilizing species to the short-chain fatty acids butyrate and propionate, which are beneficial for the host. Here, we investigated the impact of continuous lactate infusions (up to 20 mM) at two pH values (6.5 and 5.5) on human colonic microbiota responsiveness and metabolic outputs. At pH 5.5 in particular, lactate tended to accumulate in tandem with decreases in butyrate and propionate and with corresponding changes in microbial composition. Moreover, microbial communities with low numbers of lactate-utilizing bacteria were inherently less stable and therefore more prone to lactate-induced perturbations. These investigations provide clear evidence of the important role these lactate utilizers may play in health maintenance. These should therefore be considered as potential new therapeutic probiotics to combat microbiota perturbations.

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Section: Resultssupporting

confidence: 78%

Pivotal Roles for pH, Lactate, and Lactate-Utilizing Bacteria in the Stability of a Human Colonic Microbial Ecosystem

et al. 2020

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“…Although, some of the undigested cell wall material passes into the large intestine and can be fermented as an energy source for the gut microbiota. The degree of fermentation, however, relies on many factors, including the type of polysaccharides present (cellulose is slowly fermented and lignin is resistant to hydrolysis), the food matrix (accessibility of polysaccharides to bacterial enzymes) and its complexity [73,74]. Fermentation by microorganisms will promote the release of nutrients that escape digestion in the upper GIT [75].…”

Section: Encapsulationmentioning

confidence: 99%

Plant Cell Walls: Impact on Nutrient Bioaccessibility and Digestibility

Holland

Ryden

Edwards

et al. 2020

Foods

112

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Cell walls are important structural components of plants, affecting both the bioaccessibility and subsequent digestibility of the nutrients that plant-based foods contain. These supramolecular structures are composed of complex heterogeneous networks primarily consisting of cellulose, and hemicellulosic and pectic polysaccharides. The composition and organization of these different polysaccharides vary depending on the type of plant tissue, imparting them with specific physicochemical properties. These properties dictate how the cell walls behave in the human gastrointestinal tract, and how amenable they are to digestion, thereby modulating nutrient release from the plant tissue. This short narrative review presents an overview of our current knowledge on cell walls and how they impact nutrient bioaccessibility and digestibility. Some of the most relevant methods currently used to characterize the food matrix and the cell walls are also described.

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“…F. prausnitzii can metabolize substrates from both host and dietary sources, with some variability between strains [ 13 ]. One of these substrates, apple pectin, has been reproducibly reported to favor an increase in F. prausnitzii abundance in monoculture [ 20 ], complex communities [ 21 , 22 ] and humans [ 23 ].…”

Section: Introductionmentioning

confidence: 99%

Metabolic Response of Faecalibacterium prausnitzii to Cell-Free Supernatants from Lactic Acid Bacteria

et al. 2020

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Interest in preventive or therapeutic strategies targeting gut microbiota is increasing. Such strategies may involve the direct replenishment of the gut microbiota with single strains or strain mixtures, or the manipulation of strain abundance through dietary intervention, including lactic acid bacteria. A few candidate species associated with health benefits have been identified, including Faecalibacterium prausnitzii. Given its growth requirements, modulation of this bacterium has not been extensively studied. In this investigation, we explored the capacity of cell-free supernatants of different Lactobacillus, Streptococcus, Lactococcus, and Bifidobacterium strains to stimulate the growth of F. prausnitzii A2-165. Modulation by four strains with the greatest capacity to stimulate growth or delay lysis, Lactococcus lactis subsp. lactis CNCM I-1631, Lactococcus lactis subsp. cremoris CNCM I-3558, Lactobacillus paracasei CNCM I-3689, and Streptococcus thermophilus CNCM I-3862, was further characterized by transcriptomics. The response of F. prausnitzii to cell-free supernatants from these four strains revealed several shared characteristics, in particular, upregulation of carbohydrate metabolism and cell wall-related genes and downregulation of replication and mobilome genes. Overall, this study suggests differential responses of F. prausnitzii to metabolites produced by different strains, providing protection against cell death, with an increase in peptidoglycan levels for cell wall formation, and reduced cell mobilome activity.

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Impact of carbohydrate substrate complexity on the diversity of the human colonic microbiota

Cited by 38 publications

References 37 publications

Pivotal Roles for pH, Lactate, and Lactate-Utilizing Bacteria in the Stability of a Human Colonic Microbial Ecosystem

Pivotal Roles for pH, Lactate, and Lactate-Utilizing Bacteria in the Stability of a Human Colonic Microbial Ecosystem

Plant Cell Walls: Impact on Nutrient Bioaccessibility and Digestibility

Metabolic Response of Faecalibacterium prausnitzii to Cell-Free Supernatants from Lactic Acid Bacteria

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