Prebiotic Supplementation of In Vitro Fecal Fermentations Inhibits Proteolysis by Gut Bacteria, and Host Diet Shapes Gut Bacterial Metabolism and Response to Intervention

Abstract

Metabolism of protein by gut bacteria is potentially detrimental due to the production of toxic metabolites, such as ammonia, amines, p-cresol, and indole. The consumption of prebiotic carbohydrates results in specific changes in the composition and/or activity of the microbiota that may confer benefits to host well-being and health. Here, we have studied the impact of prebiotics on proteolysis within the gut in vitro. Anaerobic stirred batch cultures were inoculated with feces from omnivores (n = 3) and vegetarians (n = 3) and four protein sources (casein, meat, mycoprotein, and soy protein) with and without supplementation by an oligofructose-enriched inulin. Bacterial counts and concentrations of short-chain fatty acids (SCFA), ammonia, phenol, indole, and p-cresol were monitored during fermentation. Addition of the fructan prebiotic Synergy1 increased levels of bifidobacteria (P = 0.000019 and 0.000013 for omnivores and vegetarians, respectively). Branched-chain fatty acids (BCFA) were significantly lower in fermenters with vegetarians’ feces (P = 0.004), reduced further by prebiotic treatment. Ammonia production was lower with Synergy1. Bacterial adaptation to different dietary protein sources was observed through different patterns of ammonia production between vegetarians and omnivores. In volunteer samples with high baseline levels of phenol, indole, p-cresol, and skatole, Synergy1 fermentation led to a reduction of these compounds. IMPORTANCE Dietary protein intake is high in Western populations, which could result in potentially harmful metabolites in the gut from proteolysis. In an in vitro fermentation model, the addition of prebiotics reduced the negative consequences of high protein levels. Supplementation with a prebiotic resulted in a reduction of proteolytic metabolites in the model. A difference was seen in protein fermentation between omnivore and vegetarian gut microbiotas: bacteria from vegetarian donors grew more on soy and Quorn than on meat and casein, with reduced ammonia production. Bacteria from vegetarian donors produced less branched-chain fatty acids (BCFA).

Dietary Inulin Supplementation Modulates Short-Chain Fatty Acid Levels and Cecum Microbiota Composition and Function in Chickens Infected With Salmonella

“…Some studies also showed that prebiotics, such as fructooligosaccharide and xylooligosaccharide, had an inhibitory effect on proteolysis (Lecerf et al, 2012). These results therefore suggested that inulin might decreasing the availability of amino acids for proteolytic bacteria, thus reducing ammonia production (Wang et al, 2019). Microbial metabolites derived from the fermentation of amino acids or proteins, mainly ammonia, amines, indole compounds, and hydrogen sulfide, are potentially detrimental to gut integrity, which could be responsible for SE-infectionrelated impairment of the mucosal barrier (Song et al, 2020).…”

Gut microbiota metabolites in autistic children: An epigenetic perspective

“…The result was a substantial progression of gastrointestinal and neuro-behavioral [ 52 ]. Cumulative research findings pointed to a range of metabolites produced by Clostridiaceae , which include indole derivate phenols and p-cresol [ 53 , 54 , 55 ]. The toxin-producing Clostridia are glyphosate-resistant bacteria, and the exposure of children to this environmental pesticide may increase the abundance of Clostridia in their guts, which can lead to ASD progression [ 56 ].…”

Gut Microbiota Metabolism and Interaction with Food Components

“…On the contrary, proteolytic fermentation occurs in the distal colon, producing branched-chain fatty acids (BCFAs) and potentially detrimental metabolites such as ammonia (from amino acid deamination and urea hydrolysis), indoles, and phenols (from amino acid (AAs) carboxylation). Therefore, the intake of foods composed entirely of animal or plant ingredients alters the microbial community [29,31].…”