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Dietary Fiber Treatment Corrects the Composition of Gut Microbiota, Promotes SCFA Production, and Suppresses Colon Carcinogenesis.

ABSTRACT: Epidemiological studies propose a protective role for dietary fiber in colon cancer (CRC). One possible mechanism of fiber is its fermentation property in the gut and ability to change microbiota composition and function. Here, we investigate the role of a dietary fiber mixture in polyposis and elucidate potential mechanisms using TS4Cre×cAPC^l°^x468 mice. Stool microbiota profiling was performed, while functional prediction was done using PICRUSt. Stool short-chain fatty acid (SCFA) metabolites were measured. Histone acetylation and expression of SCFA butyrate receptor were assessed. We found that SCFA-producing bacteria were lower in the polyposis mice, suggesting a decline in the fermentation product of dietary fibers with polyposis. Next, a high fiber diet was given to polyposis mice, which significantly increased SCFA-producing bacteria as well as SCFA levels. This was associated with an increase in SCFA butyrate receptor and a significant decrease in polyposis. In conclusion, we found polyposis to be associated with dysbiotic microbiota characterized by a decline in SCFA-producing bacteria, which was targetable by high fiber treatment, leading to an increase in SCFA levels and amelioration of polyposis. The prebiotic activity of fiber, promoting beneficial bacteria, could be the key mechanism for the protective effects of fiber on colon carcinogenesis. SCFA-promoting fermentable fibers are a promising dietary intervention to prevent CRC.

SUBMITTER: Bishehsari F

PROVIDER: S-EPMC5852598 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Dietary Fiber Treatment Corrects the Composition of Gut Microbiota, Promotes SCFA Production, and Suppresses Colon Carcinogenesis.

Bishehsari Faraz F Engen Phillip A PA Preite Nailliw Z NZ Tuncil Yunus E YE Naqib Ankur A Shaikh Maliha M Rossi Marco M Wilber Sherry S Green Stefan J SJ Hamaker Bruce R BR Khazaie Khashayarsha K Voigt Robin M RM Forsyth Christopher B CB Keshavarzian Ali A

Genes 20180216 2

Epidemiological studies propose a protective role for dietary fiber in colon cancer (CRC). One possible mechanism of fiber is its fermentation property in the gut and ability to change microbiota composition and function. Here, we investigate the role of a dietary fiber mixture in polyposis and elucidate potential mechanisms using TS4Cre×cAPC<sup>l</sup>°<sup>x468</sup> mice. Stool microbiota profiling was performed, while functional prediction was done using PICRUSt. Stool short-chain fatty aci ...[more]

PMID: 29462896

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Project description: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.

Project description:This study was to investigate time-course effects of different types of dietary fiber on the energy values, fecal microbiota and short-chain fatty acid (SCFA) concentration in growing pigs. A total of 24 barrows (initial body weight, 19.8 ± 0.5 kg) were assigned to 4 dietary treatments based on body weight (BW) in a completely randomized design, including a basal diet (CON) and 3 fiber-rich diets replacing corn, soybean meal and soybean oil in the CON diet with 20% sugar beet pulp (SBP), defatted rice bran (DFRB) or soybean hull (SBH), respectively. Fresh feces were sampled on d 7, 14 and 21, followed by 5 d total feces and urine collections. The results showed that there were no differences in DE and ME between any of the fiber ingredients on d 7, 14 or 21. However, fiber inclusion decreased the DE and ME of the diet (P < 0.05) regardless of the time effect. Principal coordinate analysis (PCoA) revealed distinctly different microbial communities on the DFRB diet and SBH diet across different times (P < 0.05) and the fecal microbiota of the 4 diet groups demonstrated notably distinct clusters at each time point (P < 0.05). With adaptation time increased from 7 to 21 d, cellulose-degrading bacteria and SCFA-producing bacteria (e.g., Ruminococcaceae _UCG-014, Rikenellaceae _RC9_gut_group and Bifidobacterium) increased in the fiber inclusion diets, and pathogenic genera (e.g., Streptococcus and Selenomonas) were increased in the basal diet (P < 0.05). Furthermore, the gut microbiota of growing pigs adapted more easily and quickly to the SBP diet compared to the DFRB diet, as reflected by the concentration of propionate, butyrate, isovalerate and total SCFA which increased with time for growing pigs fed the DFRB diet (P < 0.05). Collectively, our results indicated at least 7 d adaptation was required to evaluate the energy values of fiber-rich ingredients, as the hindgut microbiota of growing pigs may need more time to adapt to a high fiber diet, especially for insoluble dietary fiber.

Dataset Information

Dietary Fiber Treatment Corrects the Composition of Gut Microbiota, Promotes SCFA Production, and Suppresses Colon Carcinogenesis.

Publications

Dietary Fiber Treatment Corrects the Composition of Gut Microbiota, Promotes SCFA Production, and Suppresses Colon Carcinogenesis.

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