Variable responses of human and non-human primate gut microbiomes to a Western diet

Abstract

Background: The human gut microbiota interacts closely with human diet and physiology. To better understand the mechanisms behind this relationship, gut microbiome research relies on complementing human studies with manipulations of animal models, including non-human primates. However, due to unique aspects of human diet and physiology, it is likely that host-gut microbe interactions operate differently in humans and non-human primates.

Results: Here, we show that the human microbiome reacts differently to a high-protein, high-fat Western diet than that of a model primate, the African green monkey, or vervet (Chlorocebus aethiops sabaeus). Specifically, humans exhibit increased relative abundance of Firmicutes and reduced relative abundance of Prevotella on a Western diet while vervets show the opposite pattern. Predictive metagenomics demonstrate an increased relative abundance of genes associated with carbohydrate metabolism in the microbiome of only humans consuming a Western diet.

Conclusions: These results suggest that the human gut microbiota has unique properties that are a result of changes in human diet and physiology across evolution or that may have contributed to the evolution of human physiology. Therefore, the role of animal models for understanding the relationship between the human gut microbiota and host metabolism must be re-focused.

Fig. 1

A Western diet reduces gut microbial diversity in humans but not vervets. Chao1 estimates (average ± SD) of microbial community richness at 1000 sequence reads per sample for vervets and humans consuming a non-Western vs. a Western diet. Star indicates significant differences (FDR-corrected p < 0.05) in microbial richness between diets. Western humans are from Italy (Schnorr et al. [3]) and the USA (Yatsunenko et al. [2]). Non-western humans are from Tanzania (Hadza, Schnorr et al. [3]), Venezuela (Guahibo, Yatsunenko et al. [2]), and Malawi (Yatsunenko et al. [2]). (N = 13 non-Western vervets; N = 14 Western vervets; N = 17 non-Western (Schnorr et al.) humans; N = 11 Western (Schnorr et al.) humans; N = 76 non-Western (Yatsunenko et al.) humans; N = 118 Western (Yatsunenko et al.) humans)

Fig. 2

The vervet gut microbiome resembles a non-Western human gut microbiome regardless of the vervet diet. Non-metric multi-dimensional scaling (NMDS) plot based on unweighted UniFrac distances illustrating clustering patterns in gut microbiomes across sampling groups at the OTU level

Fig. 3

Human and vervet gut microbiomes react differently to a Western diet. Relative abundances of key a phyla and b genera in humans and vervets consuming non-Western and Western diets. Western humans are from Italy (Schnorr et al. [3]) and the USA (Yatsunenko et al. [2]). Non-Western humans are from Tanzania (Hadza, Schnorr et al. [3]), Venezuela (Guahibo, Yatsunenko et al. [2]), and Malawi (Yatsunenko et al. [2]). Stars indicate significant differences (FDR-corrected p < 0.05) in relative abundances between diets for both humans and vervets. However, Bacteroides relative abundances were not significantly different between diets for vervets