Gut microbiome composition is linked to whole grain-induced immunological improvements

Abstract

The involvement of the gut microbiota in metabolic disorders, and the ability of whole grains to affect both host metabolism and gut microbial ecology, suggest that some benefits of whole grains are mediated through their effects on the gut microbiome. Nutritional studies that assess the effect of whole grains on both the gut microbiome and human physiology are needed. We conducted a randomized cross-over trial with four-week treatments in which 28 healthy humans consumed a daily dose of 60 g of whole-grain barley (WGB), brown rice (BR), or an equal mixture of the two (BR+WGB), and characterized their impact on fecal microbial ecology and blood markers of inflammation, glucose and lipid metabolism. All treatments increased microbial diversity, the Firmicutes/Bacteroidetes ratio, and the abundance of the genus Blautia in fecal samples. The inclusion of WGB enriched the genera Roseburia, Bifidobacterium and Dialister, and the species Eubacterium rectale, Roseburia faecis and Roseburia intestinalis. Whole grains, and especially the BR+WGB treatment, reduced plasma interleukin-6 (IL-6) and peak postprandial glucose. Shifts in the abundance of Eubacterium rectale were associated with changes in the glucose and insulin postprandial response. Interestingly, subjects with greater improvements in IL-6 levels harbored significantly higher proportions of Dialister and lower abundance of Coriobacteriaceae. In conclusion, this study revealed that a short-term intake of whole grains induced compositional alterations of the gut microbiota that coincided with improvements in host physiological measures related to metabolic dysfunctions in humans.

Figure 1

Experimental design. Time line of the randomized crossover trial. Three four-week dietary treatments were assessed in succession. The treatments were interspaced by two-week washout (WO) periods. Blood and stool samples (indicated by arrows) were collected during the baseline (BL) and at the end of each treatment period.

Figure 2

Associations among host physiological characteristics and their correlation with bacterial populations in fecal samples at baseline. Heatmap displaying correlation coefficients between metabolic and physiological parameters of the study population at baseline (a). Correlations between hs-CRP with body fat (b), LBP with body fat (c), hs-CRP and LBP (d), hs-CRP and Ruminococcaceae (e), LBP with Ruminococcaceae (f) and Oscillibacter with postprandial AUC glucose (g). Pearson's correlation (r) and the corresponding P-values are presented.

Figure 3

Immunological and metabolic improvements induced through whole-grain consumption. Plasma IL-6 levels in the entire subject population (a), in overweight participants (b), and in females (c). Maximum postprandial glucose levels in the entire subject population (d) and overweight subjects (e) during the three treatments (BR, BR+WGB, WGB) and at baseline. *P< 0.05, **P< 0.01, ^§P< 0.1.

Figure 4

Abundance of specific taxa in subjects that showed differences in their IL-6 response to whole grains. Subjects were classified into terciles according to the magnitude of the change in plasma IL-6 levels induced by whole-grain consumption (BR+B treatment versus baseline). The proportions of bacterial taxa in fecal samples during the baseline were compared in the three terciles and significant differences existed in the proportions of Veillonellaceae (a), Dialister (b) and Coriobacteriaceae (c) in fecal samples during baseline. *P< 0.05, **P< 0.01.