Procyanidin—Cell Wall Interactions within Apple Matrices Decrease the Metabolization of Procyanidins by the Human Gut Microbiota and the Anti-Inflammatory Effect of the Resulting Microbial Metabolome In Vitro

Abstract

B-type oligomeric procyanidins in apples constitute an important source of polyphenols in the human diet. Their role in health is not known, although it is suggested that they generate beneficial bioactive compounds upon metabolization by the gut microbiota. During apple processing, procyanidins interact with cell-wall polysaccharides and form stable complexes. These interactions need to be taken into consideration in order to better assess the biological effects of fruit constituents. Our objectives were to evaluate the impact of these interactions on the microbial metabolization of cell walls and procyanidins, and to investigate the potential anti-inflammatory activity of the resulting metabolome, in addition to analyzing the taxonomical changes which the microbiota undergo. In vitro fermentation of three model apple matrices with microbiota from 4 healthy donors showed that the binding of procyanidins to cell-wall polysaccharides, whether covalently or non-covalently, substantially reduced procyanidin degradation. Although cell wall-unbound procyanidins negatively affected carbohydrate fermentation, they generated more hydroxyphenylvaleric acid than bound procyanidins, and increased the abundance of Adlercreutzia and Gordonibacter genera. The best results in terms of production of anti-inflammatory bioactive metabolites were observed from the apple matrix with no bonds between procyanidins and cell wall polysaccharides, although the matrix with non-covalent bonds was not far behind.

Interactions between cell wall polysaccharides and polyphenols: Effect of molecular internal structure

“…One of their beneficial health effects is the prevention of oxidation of lipids and proteins in the stomach (Boléa, Ginies, Vallier, & Dufour, 2019; Gobert et al., 2014; Lee et al., 2020). Furthermore, many recent studies have shown that CPS–polyphenol complexes have a positive effect in the colon (Grant et al., 2020; Kardum & Glibetic, 2018; Le Bourvellec et al., 2019; Monfoulet et al., 2020; Phan et al., 2020; Tarko & Duda‐Chodak, 2020). Polyphenols can be released from their complexes through the action of enzymes or microorganisms in the intestinal tract and biotransformed by the colonic microbial metabolism (i.e., from the nonabsorbable to the absorbed form).…”

“…Although many NEPPs and complex polyphenols, for example, proanthocyanidins, have very low bioavailability in the upper gut, their resulting metabolites (mostly phenolic acids), produced by the colonic microbiota, are highly available (Aura et al., 2013; Palafox‐Carlos, Ayala‐Zavala, & González‐Aguilar, 2011; Saura‐Calixto et al., 2010). This process can also be modulated by interactions with CPSs, both noncovalent and covalent (Le Bourvellec et al., 2019; Saura‐Calixto, 2011). Compared to unbound polyphenols, interactions with CPSs reduce the degradation of procyanidins during digestion and the production of anti‐inflammatory bioactive metabolites, but favor butyrate production, which is known for its beneficial effects on health.…”

“…Consequently, processing prior to ingestion may modify the nutritional quality of foods, with particular effects on their metabolism via the gut microbiota. There is already abundant evidence that CPS–polyphenol interactions modulate the fermentation of polyphenols in the gut (Le Bourvellec et al., 2019; Monfoulet et al., 2020; Phan et al., 2020; Tarko & Duda‐Chodak, 2020). It is likely that these effects translate into changes in the bioactive metabolites present and their potential beneficial effects, which might have far‐reaching implications for food processing and human health.…”

Mulberry leaf phenolics and fiber exert anti‐obesity through the gut microbiota‐host metabolism pathway

“…Covalent or noncovalent binding of proanthocyanidins with cell wall polysaccharides significantly reduced the degradation effect of human intestinal flora on proanthocyanidins. However, when there was no binding between proanthocyanidins and cell wall polysaccharides, the best anti‐inflammatory effect was achieved (Le Bourvellec et al., 2019).…”

Revealing microbial species diversity using sequence capture by hybridization

“…Three OTUs (146, 393 and 1761) derived from the 16S rDNA V3-V5 region were identified in a previous in vitro study [23] involving four microbial faecal communities that were incubated with a mixture of purified apple polyphenols and polysaccharides (Data S1, available in the online version of this Fig. 1.…”