Uncovering differences in rye and wheat degradation by human gut microbiota applying a quantitative multi-metaOmics in vitro approach

Abstract

While wheat is the most common grain used in bread-making worldwide, rye is popular in many European countries too. Rye is associated with several health benefits, which is attributed to its comparatively higher fiber content (primarily fructans and arabinoxylans) that promote production of short chain fatty acids (SCFA) by gut microbiota, in particular butyrate. Intervention studies revealed bacterial alterations upon rye administration, however, the detailed mechanisms involved in its degradation are not understood. We grew fecal communities (n=20) on pre-digested rye and wheat, respectively, demonstrating that rye was yielding higher cell and SCFA concentrations in almost all samples along with distinct abundances of many taxa. A multi metaOmics (metagenomics/metatranscriptomics) approach (n=5 donors) showed higher bacterial growth rates for most taxa on rye compared to wheat. The higher growth rate of rye was accompanied by increased expression of genes involved in growth and energy generation suggesting higher carbon substrate accessibility. The carbohydrate active enzyme repertoire was greatly distinct between communities growing on the two substrates with several specific glycoside hydrolases increasingly expressed in rye containing cultures. Agathobacter faecis was revealed as the key butyrogenic species for rye degradation and its expression pattern based on metagenome assembled genomes showed adaptation to growth on rye via expression of genes involved in arabinoxylan degradation and fructose (major monomer of fructans) uptake. Our study verifies higher SCFA production from rye over wheat and gives detailed insights into molecular mechanisms involved. It supports that the observed health benefits of rye are mediated by gut microbiota.