Temporal variation selects for diet–microbe co-metabolic traits in the gut of Gorilla spp

Abstract

Although the critical role that our gastrointestinal microbes play in host physiology is now well established, we know little about the factors that influenced the evolution of primate gut microbiomes. To further understand current gut microbiome configurations and diet-microbe co-metabolic fingerprints in primates, from an evolutionary perspective, we characterized fecal bacterial communities and metabolomic profiles in 228 fecal samples of lowland and mountain gorillas (G. g. gorilla and G. b. beringei, respectively), our closest evolutionary relatives after chimpanzees. Our results demonstrate that the gut microbiomes and metabolomes of these two species exhibit significantly different patterns. This is supported by increased abundance of metabolites and bacterial taxa associated with fiber metabolism in mountain gorillas, and enrichment of markers associated with simple sugar, lipid and sterol turnover in the lowland species. However, longitudinal sampling shows that both species' microbiomes and metabolomes converge when hosts face similar dietary constraints, associated with low fruit availability in their habitats. By showing differences and convergence of diet-microbe co-metabolic fingerprints in two geographically isolated primate species, under specific dietary stimuli, we suggest that dietary constraints triggered during their adaptive radiation were potential factors behind the species-specific microbiome patterns observed in primates today.

Rates of gut microbiome divergence in mammals

“…Microbiome composition can fluctuate in response to dietary and environmental changes. Seasonal availability of food and modifications to the diet of individuals have been shown to influence microbiome composition in several mammalian species (Amato et al, 2014;Davenport et al, 2014;Degnan et al, 2012;Gomez et al, 2016;Kohl & Dearing, 2014;Sun et al, 2016;Turnbaugh et al, 2009). In humans, adopting a high-protein diet increases the abundance of bile-tolerant bacteria, whereas a plant-based diet enriches microbial taxa that specialize in carbohydrate fermentation (David et al, 2014;O'Keefe et al, 2015), paralleling the differences observed in gut microbiomes of hunter-gathers vs. humans in industrialized societies (Morton et al, 2015;Rampelli et al, 2015).…”

Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux's sifakas (Propithecus verreauxi)

“…At the genus level, Prevotella increased markedly during months characterized by fruit consumption, similar to what has been found in western lowland gorillas (Gomez et al. 2016). In ruminants, Prevotella digest noncellulosic polysaccharides and pectin (White, Lamed, Bayer, & Flint, 2014), and in humans, high levels of Prevotella have been associated with a carbohydrate‐ and sugar‐rich diet (Wu et al., 2011).…”

“…For example, western lowland gorillas ( Gorilla gorilla ) display an increase in the abundance of microbes involved in fiber breakdown in response to low fruit availability (Gomez et al. 2016). In black howler monkeys ( Alouatta pigra ), an increase in the abundance of Ruminococcaceae, which are efficient fermenters of nonsoluble carbohydrates, was noted during periods of reduced energy intake and might be a mechanism to compensate for low food quality (Amato et al., 2015).…”

“…In wildlife, naturally occurring changes in food availability often cause seasonal shifts in energy intake and diet composition (e.g., Norscia, Carrai, & Borgognini-Tarli, 2006;Wrangham, Conklin-Brittain, & Hunt, 1998) and may, consequently, also affect the gut microbiota. For example, western lowland gorillas (Gorilla gorilla) display an increase in the abundance of microbes involved in fiber breakdown in response to low fruit availability (Gomez et al 2016). In black howler monkeys (Alouatta pigra), an increase in the abundance of Ruminococcaceae, which are efficient fermenters of nonsoluble carbohydrates, was noted during periods of reduced energy intake and might be a mechanism to compensate for low food quality (Amato et al, 2015).…”

Microbial genomes from non-human primate gut metagenomes expand the primate-associated bacterial tree of life with over 1000 novel species

“…Recent studies of NHPs uncovered part of their hidden microbial diversity but only very partially contributed to the extension of the genetic blueprint of the microbiome in these hosts. Several 16S rRNA gene amplicon sequencing studies investigated the microbiome composition of NHPs [24][25][26][27][28][29][30][31][32], and some, including a meta-analysis [33], investigated the overlap and specificity of microbial communities associated with humans and NHPs [34][35][36]. Yet, because this approach has a limited phylogenetic resolution and lacks functional characterization, many co-diversification aspects cannot be studied.…”