Gut microbiomes of wild great apes fluctuate seasonally in response to diet

Abstract

The microbiome is essential for extraction of energy and nutrition from plant-based diets and may have facilitated primate adaptation to new dietary niches in response to rapid environmental shifts. Here we use 16S rRNA sequencing to characterize the microbiota of wild western lowland gorillas and sympatric central chimpanzees and demonstrate compositional divergence between the microbiotas of gorillas, chimpanzees, Old World monkeys, and modern humans. We show that gorilla and chimpanzee microbiomes fluctuate with seasonal rainfall patterns and frugivory. Metagenomic sequencing of gorilla microbiomes demonstrates distinctions in functional metabolic pathways, archaea, and dietary plants among enterotypes, suggesting that dietary seasonality dictates shifts in the microbiome and its capacity for microbial plant fiber digestion versus growth on mucus glycans. These data indicate that great ape microbiomes are malleable in response to dietary shifts, suggesting a role for microbiome plasticity in driving dietary flexibility, which may provide fundamental insights into the mechanisms by which diet has driven the evolution of human gut microbiomes.

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

“…To investigate the extent to which the composition of the gut microbiome overlaps across different primates for both known and currently uncharacterized microbes, we meta-analyzed a large set of gut microbiomes from humans and non-human primates (NHPs) that are publically available. Six datasets were considered for NHPs [30,[37][38][39][40][41] spanning 22 host species from 14 different countries in 5 continents (Additional file 1: Table S1 and Additional file 2: Figure S1), totaling 203 metagenomic samples that we retrieved and curated for this work. Microbiome samples from adult human healthy individuals were retrieved from 47 datasets considered in a recent meta-analysis [11] on 9428 human gut metagenomes and used as a comparative resource.…”

“…1a and Additional file 1: Table S1) to test the influence of folivory on its composition and function and highlighted that host phylogeny has a stronger influence than diet. With a similar approach, [30] shotgun sequenced 19 wild western lowland gorillas (Gorilla gorilla gorilla) in the Republic of the Congo as part of a 16S rRNA study including sympatric chimpanzees and modern human microbiomes that demonstrated the compositional divergence between the primate clades' microbiome and the seasonal shift in response to changing dietary habits throughout the year. Orkin et al [40] exposed similar seasonal patterns linked with water and food availability by surveying the microbiome of 20 wild white-faced capuchin monkeys (Cebus capucinus imitator) in Costa Rica.…”

“…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.…”

“…Yet, because this approach has a limited phylogenetic resolution and lacks functional characterization, many co-diversification aspects cannot be studied. Some studies have also applied shotgun metagenomics on NHP microbiomes [30,[37][38][39][40][41], but all of them employed a reference-based computational profiling approach, which solely allows the identification of the very few known microbial species present in NHPs, disregarding those that have not been characterized yet.…”

Correlation and causation between the microbiome, Wolbachia and host functional traits in natural populations of drosophilid flies

“…(Chevalier et al, ; David et al, ; Ferguson et al, ; Jehrke, Stewart, Droste, & Beller, ; Obadia, Keebaugh, Yamada, Ludington, & Ja, ; Ramsby, Hoogenboom, Whalan, & Webster, ), which may differ systematically between laboratory and field conditions. Where studied, considerable variation in the gut microbiota composition has been demonstrated in natural animal populations (Adair, Wilson, Bost, & Douglas, ; Hicks et al, ; Jones et al, ; Martinson, Douglas, & Jaenike, ; Webster, Consuegra, Hitchings, & Leaniz, ), but whether and how this variation relates to functional traits of the animal host is largely unknown.…”