Subtle Variations in Dietary-Fiber Fine Structure Differentially Influence the Composition and Metabolic Function of Gut Microbiota

Abstract

The chemical structures of soluble fiber carbohydrates vary from source to source due to numerous possible linkage configurations among monomers. However, it has not been elucidated whether subtle structural variations might impact soluble fiber fermentation by colonic microbiota. In this study, we tested the hypothesis that subtle structural variations in a soluble polysaccharide govern the community structure and metabolic output of fermenting microbiota. We performed in vitro fecal fermentation studies using arabinoxylans (AXs) from different classes of wheat (hard red spring [AXHRS], hard red winter [AXHRW], and spring red winter [AXSRW]) with identical initial microbiota. Carbohydrate analyses revealed that AXSRW was characterized by a significantly shorter backbone and increased branching compared with those of the hard varieties. Amplicon sequencing demonstrated that fermentation of AXSRW resulted in a distinct community structure of significantly higher richness and evenness than those of hard-AX-fermenting cultures. AXSRW favored OTUs within Bacteroides, whereas AXHRW and AXHRS favored Prevotella. Accordingly, metabolic output varied between hard and soft varieties; higher propionate production was observed with AXSRW and higher butyrate and acetate with AXHRW and AXHRS. This study showed that subtle changes in the structure of a dietary fiber may strongly influence the composition and function of colonic microbiota, further suggesting that physiological functions of dietary fibers are highly structure dependent. Thus, studies focusing on interactions among dietary fiber, gut microbiota, and health outcomes should better characterize the structures of the carbohydrates employed. IMPORTANCE Diet, especially with respect to consumption of dietary fibers, is well recognized as one of the most important factors shaping the colonic microbiota composition. Accordingly, many studies have been conducted to explore dietary fiber types that could predictably manipulate the colonic microbiota for improved health. However, the majority of these studies underappreciate the vastness of fiber structures in terms of their microbial utilization and omit detailed carbohydrate structural analysis. In some cases, this causes conflicting results to arise between studies using (theoretically) the same fibers. In this investigation, by performing in vitro fecal fermentation studies using bran arabinoxylans obtained from different classes of wheat, we showed that even subtle changes in the structure of a dietary fiber result in divergent microbial communities and metabolic outputs. This underscores the need for much higher structural resolution in studies investigating interactions of dietary fibers with gut microbiota, both in vitro and in vivo.

Health benefits of whole grain: effects on dietary carbohydrate quality, the gut microbiome, and consequences of processing

“…Dietary fibers that reach the lower bowel undigested can become substrates for microbial hydrolytic enzymes, releasing bound compounds and nutrients that can be utilized by the body (Tannock, 2020; Tungland & Meyer, 2002). The amount, chemical nature, and physical form of dietary fibers arriving in the lower gut are the principle drivers of the composition/diversity of the gut microbiome (Ho Do et al., 2020; Tamura & Brumer, 2021; Tuncil et al., 2020) that can affect pH and composition of digesta and has been linked to health outcomes (Swanson et al., 2020; Tamura & Brumer, 2021) as discussed later in this review.…”

“…Also, fine‐structural differences in XOS and arabinoxylooligosaccharides (AXOS) dictated differential growth of a number of Bacteroides species commonly found in the colon (Mendis et al., 2018). Similarly, subtle variations in the chemical fine‐structure of AXs from different classes of wheat (hard red spring, hard red winter, and spring red winter), with differences in backbone length and branching, led to the development of different community structure when incubated with fecal samples (Tuncil et al., 2020).…”

Fine carbohydrate structure governs the structure and function of human gut microbiota independently of variation in glycosyl residue composition

“…In nature, variation in polysaccharide structure is overwhelmingly associated with differences in the ratios of glycosyl residues that compose the polymer (starch and glycogen being notable exceptions) (22). For example, arabinoxylans extracted from bran of three classes of wheat exhibited coordinate variation in sugar composition and linkage structure (10). These variables may exert independent influences upon microbial community responses to complex substrates.…”

In vitro Colon Fermentation of Soluble Arabinoxylan Is Modified Through Milling and Extrusion

“…The application of heat, pressure, or mechanical forces induces oxidative and hydrolytic reactions, which both modify the native chemical structure (12)(13)(14)(15). Consequently, these structural modifications influence physicochemical properties and may further affect the prebiotic potential of AX (16,17).…”

“…This enzymatic digestion and the resulting metabolism of released monosaccharides lead to the production of beneficial SCFA metabolites and modulates the gut environment (20)(21)(22).Various studies have shown that the in vitro fermentation of AX is strongly linked to the molecular fine structure of AX (23,24). Similarly, Tuncil et al (17) hypothesized that subtle variations in dietary fiber structures may result in altered microbiota compositions. In particular, differences in M w and the branching of soluble cereal AX affect SCFA production and bacterial growth during in vitro fermentation by human fecal microbiota (20,25).…”