Response of Ruminal Microbiota–Host Gene Interaction to High-Altitude Environments in Tibetan Sheep

Abstract

Altitude is the main external environmental pressure affecting the production performance of Tibetan sheep, and the adaptive evolution of many years has formed a certain response mechanism. However, there are few reports on the response of ruminal microbiota and host genomes of Tibetan sheep to high-altitude environments. Here, we conducted an integrated analysis of volatile fatty acids (VFAs), microbial diversity (16S rRNA), epithelial morphology, and epithelial transcriptome in the rumen of Tibetan sheep at different altitudes to understand the changes in ruminal microbiota–host interaction in response to high altitude. The differences in the nutritional quality of forage at different altitudes, especially the differences in fiber content (ADF/NDF), led to changes in rumen VFAs of Tibetan sheep, in which the A/P value (acetic acid/propionic acid) was significantly decreased (p < 0.05). In addition, the concentrations of IgA and IgG in Middle-altitude (MA) and High-altitude Tibetan sheep (HA) were significantly increased (p < 0.05), while the concentrations of IgM were significantly increased in MA (p < 0.05). Morphological results showed that the width of the rumen papilla and the thickness of the basal layer increased significantly in HA Tibetan sheep (p < 0.05). The 16S rRNA analysis found that the rumen microbial diversity of Tibetan sheep gradually decreased with increasing altitude, and there were some differences in phylum- and genus-level microbes at the three altitudes. RDA analysis found that the abundance of the Rikenellaceae RC9 gut group and the Ruminococcaceae NK4A214 group increased with altitudes. Furthermore, a functional analysis of the KEGG microbial database found the “lipid metabolism” function of HA Tibetan sheep to be significantly enriched. WGCNA revealed that five gene modules were enriched in “energy production and conversion”, “lipid transport and metabolism”, and “defense mechanisms”, and cooperated with microbiota to regulate rumen fermentation and epithelial immune barrier function, so as to improve the metabolism and immune level of Tibetan sheep at high altitude.

Synergistic Responses of Tibetan Sheep Rumen Microbiota, Metabolites, and the Host to the Plateau Environment

“…(Figures 11 and S8), the content of butyryl-CoA downstream can be reduced, thus affecting the content of butyric acid in the rumens of high-altitude Tibetan sheep. This was consistent with our previous results [14], which also confirmed that rumen microbial metabolites interact with host genes to regulate the body pathway (Figure 11). In addition, differentially expressed genes and metabolites were enriched in the cAMP signaling pathway (Figure S9), which participates in the regulation of the PKA pathway by reducing the level of the metabolite dopamine, resulting in increased expression of the downstream gene CREB5, thus stimulating neurons, regulating body traits, and adjusting to the environmental pressure of plateau mutation.…”

“…Fructoselysine can be converted to butyric acid [23], which is the main energy substance in ruminants and is involved in ketogenic metabolism [24]. These findings suggest that Tibetan sheep in the 3500 m area are more suitable for grazing and breeding, and similar results were also found in our previous studies [14]. The differential metabolite L-kynurenine decreases with altitude, and studies have found that kynurenine is associated with hypoxia and ischemia in animals [25].…”

“…It was found that the phenotypic traits of ruminants were affected by rumen microbiota, and their functions could be reflected by rumen metabolites [15]. Our previous studies have confirmed that there are differences in microbiota at different altitudes [14]. Further combined analysis of the microbiome and metabolome revealed that Fibrobacteres and Synergistetes were significantly correlated with metabolites.…”

“…Microbial genes in the rumens of high-altitude ruminants are coenriched in the metabolite VFA production pathway, providing persistent energy for the host. Additionally, the microbiome coevolves with the host genome to adapt to the extreme environment [10].Our previous studies also found differences in rumen microbiota abundance and composition of Tibetan sheep at different altitudes [14]. Host genes and microbiota are involved in the regulation of ruminal fermentation metabolism and epithelial immune barrier function.…”

Fat deposition, fatty acid profiles, antioxidant capacity and differentially expressed genes in subcutaneous fat of Tibetan sheep fed wheat‐based diets with and without xylanase supplementation

“…The Tibetan sheep ( Ovis aries ) thrives in harsh environments approximately 3000 m above sea level and represents (Sha et al, 2022). However, the Tibetan sheep face a number of challenges on the Qinghai‐Tibetan Plateau, including prolonged cold weather, low oxygen content in the air, and strong ultraviolet radiation, leading to both growth retardation and poor reproductive performance (Zhou et al, 2022).…”