Variable responses of human microbiomes to dietary supplementation with resistant starch

Abstract

Background: The fermentation of dietary fiber to various organic acids is a beneficial function provided by the microbiota in the human large intestine. In particular, butyric acid contributes to host health by facilitating maintenance of epithelial integrity, regulating inflammation, and influencing gene expression in colonocytes. We sought to increase the concentration of butyrate in 20 healthy young adults through dietary supplementation with resistant starch (unmodified potato starch-resistant starch (RS) type 2).

Methods: Fecal samples were collected from individuals to characterize butyrate concentration via liquid chromatography and composition of the microbiota via surveys of 16S rRNA-encoding gene sequences from the Illumina MiSeq platform. Random Forest and LEfSe analyses were used to associate responses in butyrate production to features of the microbiota.

Results: RS supplementation increased fecal butyrate concentrations in this cohort from 8 to 12 mmol/kg wet feces, but responses varied widely between individuals. Individuals could be categorized into three groups based upon butyrate concentrations before and during RS: enhanced, high, and low (n = 11, 3, and 6, respectively). Fecal butyrate increased by 67 % in the enhanced group (from 9 to 15 mmol/kg), while it remained ≥11 mmol/kg in the high group and ≤8 mmol/kg in the low group. Microbiota analyses revealed that the relative abundance of RS-degrading organisms-Bifidobacterium adolescentis or Ruminococcus bromii-increased from ~2 to 9 % in the enhanced and high groups, but remained at ~1.5 % in the low group. The lack of increase in RS-degrading bacteria in the low group may explain why there was no increase in fecal butyrate in response to RS. The microbiota of individuals in the high group were characterized by an elevated abundance of the butyrogenic microbe Eubacterium rectale (~6 % in high vs. 3 % in enhanced and low groups) throughout the study.

Conclusions: We document the heterogeneous responses in butyrate concentrations upon RS supplementation and identify characteristic of the microbiota that appear to underlie this variation. This study complements and extends other studies that call for personalized approaches to manage beneficial functions provided by gut microbiomes.

Fig. 1

Experimental design. Participants supplemented their habitual diets with resistant starch. Filled symbols represent points at which fecal samples were collected

Fig. 2

Median butyrate concentrations for each individual before (triangles) and during consumption of RS (circles). Dotted and dashed lines denote the median values for butyrate before and during RS, respectively, for the entire study population

Fig. 3

Clustering individuals based upon their butyrate response to RS. a Three groups generated by k-means clustering. b Median butyrate concentrations before and during RS supplementation. c Average butyrate concentrations before and during RS in the three groups

Fig. 4

Identifying microbiota features that distinguish the low from other groups. a Median abundance of OTUs taxonomically related to B. adolescentis and R. bromii before and during RS for each individual. b Summed abundance of the two proposed RS-degrading OTUs before and during RS in the three groups

Fig. 5

The relative abundance of OTU 4 Eubacterium rectale distinguishes the high from other groups. a Median abundance of OTU 4 before and during RS for each individual. Individuals in whom the abundance of this OTU increased with RS are marked with an asterisk (LEfSe p < 0.05). b Abundance of OTU 4 before and during RS in the three groups