Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons

Abstract

Wild animals may encounter multiple challenges especially food shortage and altered diet composition in their suboptimal ranges. Yet, how the gut microbiome responds to dietary changes remains poorly understood. Prior studies on wild animal microbiomes have typically leaned upon relatively coarse dietary records and individually unresolved fecal samples. Here, we conducted a longitudinal study integrating 514 time-series individually recognized fecal samples with parallel fine-grained dietary data from two Skywalker hoolock gibbon (Hoolock tianxing) groups populating high-altitude mountainous forests in western Yunnan Province, China. 16S rRNA gene amplicon sequencing showed a remarkable seasonal fluctuation in the gibbons’ gut microbial community structure both across individuals and between the social groups, especially driven by the relative abundances of Lanchnospiraceae and Oscillospiraceae associated with fluctuating consumption of leaf. Metagenomic functional profiling revealed that diverse metabolisms associated with cellulose degradation and short-chain fatty acids (SCFAs) production were enriched in the high-leaf periods possibly to compensate for energy intake. Genome-resolved metagenomics further enabled the resolving metabolic capacities associated with carbohydrate breakdown among community members which exhibited a high degree of functional redundancy. Our results highlight a taxonomically and functionally sensitive gut microbiome actively responding to the seasonally shifting diet, facilitating the survival and reproduction of the endangered gibbon species in their suboptimal habitats.

Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations

“…We followed the adult female of each group (A2 in group NK and B2 in group BC) for on average eight days per month, each day from the time gibbons left their sleeping trees in the morning until they returned to the sleeping trees in the afternoon 63 , 64 . During follows, we recorded all feeding activities (5-min scan and ad libitum), recording the start time, end time, food species and food type (e.g., leaves, fruit, flower, animals, and others) of each feeding bout for the focal individual 25 . To calculate the dietary composition for each gibbon, the recorded feeding times allocated to the same food type were added and then divided by the total feeding time in a full-day.…”

“…The viral and microbial metagenomic reads were trimmed and filtered using fastp v0.21.0 with default parameters 25 , 67 . For the high-quality metagenomic reads, superhost subtraction was performed against the H. tianxing genomes using Bowtie2 v2.2.9 to remove contaminant sequences from the gibbons 68 .…”

“…The investigation of gut phageome dynamics in wild animals possibly associated with dietary variations faces multiple challenges, especially in quantifying diet and collecting fresh feces of individually recognized animals for consecutive days 25 . Specifically, the elusive nature of many wild animals (e.g., predators, ungulates, etc.)…”

“…Gaoligong, Yunnan, China in 15 months. A recent microbiome study has showed that the gut prokaryotes of these gibbons responded to the seasonal diet compositionally and functionally 25 . In this study, we focus specifically on the eco-evolutionary dynamics of gut phageomes by analyzing a massive longitudinal dataset of viral metagenomes (VMs) and microbial metagenomes (MMs) for the six gibbons.…”

Editorial: Community series in the wildlife gut microbiome and its implication for conservation biology, volume II

“…The macroscopic spatiotemporal dynamics of environmental variables exert a substantial influence on the structure, function, and adaptive evolution of the host-microbiome (Ma et al, 2019 ; Li et al, 2023 ). The changes in dietary resources due to seasonal fluctuations can induce alterations in the community structure of the host microbiome, thereby significantly impacting the physiological functions of the host (Huang et al, 2022 ; Li et al, 2023 ). The issue was investigated by Qin et al and Li et al in this topic.…”