Divergent short-chain fatty acid production and succession of colonic microbiota arise in fermentation of variously-sized wheat bran fractions

Yunus E. Tuncil,Bruce R. Hamaker,Riya D. Thakkar,Stephen R. Lindemann,Arianna D. Romero Marcia

doi:10.1038/s41598-018-34912-8

Yunus E. Tuncil, Bruce R. Hamaker + Show 3 more

Open Access

https://doi.org/10.1038/s41598-018-34912-8

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Abstract

Though the physical structuring of insoluble dietary fiber sources may strongly impact their processing by microbiota in the colon, relatively little mechanistic information exists to explain how these aspects affect microbial fiber fermentation. Here, we hypothesized that wheat bran fractions varying in size would be fermented differently by gut microbiota, which would lead to size-dependent differences in metabolic fate (as short-chain fatty acids; SCFAs) and community structure. To test this hypothesis, we performed an in vitro fermentation assay in which wheat bran particles from a single source were separated by sieving into five size fractions and inoculated with fecal microbiota from three healthy donors. SCFA production, measured by gas chromatography, uncovered size fraction-dependent relationships between total SCFAs produced as well as the molar ratios of acetate, propionate, and butyrate. 16S rRNA sequencing revealed that these size-dependent metabolic outcomes were accompanied by the development of divergent microbial community structures. We further linked these distinct results to subtle, size-dependent differences in chemical composition. These results suggest that physical context can drive differences in microbiota composition and function, that fiber-microbiota interaction studies should consider size as a variable, and that manipulating the size of insoluble fiber-containing particles might be used to control gut microbiome composition and metabolic output.

Highlights

The human colon is one of the most densely-colonized microbial habitats found on earth, being home to tens of trillions of microbial cells[1,2]; these are collectively termed the colonic microbiota
Many research groups have determined that (1) this loss of species from the colonic microbiota is linked to consumption of the high-fat, low-fiber Western diet ( differences exist within Western populations with respect to habitual diets and gut microbiome diversity8) (2) that, in mice, these extinctions compound irrevocably over generations, and (3) that higher consumption of fermentable dietary fibers increases the diversity of the colonic microbiota[9].The mechanisms driving these losses in diversity remain poorly understood[10], which inhibits design of dietary strategies to stably increase colonic microbiota diversity as a means to prevent or treat chronic disease
We tested whether wheat bran particle size would impact the metabolism and community structure of fecal microbiota through in vitro batch fermentations of wheat bran size fractions, which had been previously digested enzymatically in vitro to mimic transit through the stomach and small intestine and inoculated with fecal microbiota from three healthy donors

Summary

Introduction

The human colon is one of the most densely-colonized microbial habitats found on earth, being home to tens of trillions of microbial cells[1,2]; these are collectively termed the colonic microbiota. Anaerobic metabolism of dietary fibers by colonic microbiota results in short-chain fatty acids (SCFAs; acetate, propionate, and butyrate) as the predominant terminal products of fermentation; these SCFAs are increasingly understood to modulate host physiological processes and are thought to contribute to health through multiple mechanisms[15,16,17,18,19]. Similar results were observed in two independent in vivo studies, in which consumption of a wheat bran-enriched diet increased butyrate concentrations in the feces of obese[26] and overweight[27] humans. These changes were attributed to stimulation of members of Lachnospiraceae in the colons of these subjects. Increased butyrate formation in the large intestine through wheat bran fermentation was reported to suppress chemically-induced tumors in rodents[28,29]

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