Fine Carbohydrate Structure of Dietary Resistant Glucans Governs the Structure and Function of Human Gut Microbiota.

Arianna D Romero Marcia,Renee E Oles,Tianming Yao,Stephen R Lindemann,Ming-Hsu Chen

doi:10.3390/nu13092924

Arianna D Romero Marcia, Renee E Oles + Show 3 more

Open Access

https://doi.org/10.3390/nu13092924

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Journal: Nutrients	Publication Date: Aug 24, 2021
Citations: 15	License type: CC BY 4.0

Affiliation: Purdue University West Lafayette

Abstract

Increased dietary fiber consumption has been shown to increase human gut microbial diversity, but the mechanisms driving this effect remain unclear. One possible explanation is that microbes are able to divide metabolic labor in consumption of complex carbohydrates, which are composed of diverse glycosidic linkages that require specific cognate enzymes for degradation. However, as naturally derived fibers vary in both sugar composition and linkage structure, it is challenging to separate out the impact of each of these variables. We hypothesized that fine differences in carbohydrate linkage structure would govern microbial community structure and function independently of variation in glycosyl residue composition. To test this hypothesis, we fermented commercially available soluble resistant glucans, which are uniformly composed of glucose linked in different structural arrangements, in vitro with fecal inocula from each of three individuals. We measured metabolic outputs (pH, gas, and short-chain fatty acid production) and community structure via 16S rRNA amplicon sequencing. We determined that community metabolic outputs from identical glucans were highly individual, emerging from divergent initial microbiome structures. However, specific operational taxonomic units (OTUs) responded similarly in growth responses across individuals’ microbiota, though in context-dependent ways; these data suggested that certain taxa were more efficient in competing for some structures than others. Together, these data support the hypothesis that variation in linkage structure, independent of sugar composition, governs compositional and functional responses of microbiota.

Highlights

Significant differences in glucan structure were revealed by carbohydrate linkage analysis (Figure 1). These glucans were categorized as mixed linkage α-glucans (A–C), resistant maltodextrins (D, G and J–M), and polydextroses (E and H)
Arabinoxylans extracted from bran of three classes of wheat exhibited coordinate variation in sugar composition and linkage structure [10]
In this study we aimed to separate these two variables by using glucans that varied in fine structure but were composed entirely of glucose, as substrates for gut microbiota in experimental fermentations

Summary

Introduction

The diversity and idiosyncrasy of diets makes it challenging to identify how the individual components thereof influence gut microbiome structure and function in predictable ways across individuals. One class of food components known to significantly shape the gut microbiome’s structure and function, and, thereby, human health, is fermentable dietary fibers, which are resistant to hydrolysis by human enzymes but are degraded by colonic microbes, increasing and maintaining diversity of the gut microbiome [5]. The task of linking fiber polysaccharides with predictable gut microbiome responses is made more difficult in that complex carbohydrates vary in both composition (i.e., the types and ratios of sugars that compose the polymer) and in structure (i.e., how those sugars are linked via glycosidic bonds). Polysaccharides can vary across multiple structural dimensions, including monosaccharide composition, anomeric configurations, glycosidic linkages, linear chain lengths, and branch chain compositions [6]

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