Coping with extremes: the rumen transcriptome and microbiome co-regulate plateau adaptability of Xizang goat

Abstract

The interactions between the rumen microbiota and the host are crucial for the digestive and absorptive processes of ruminants, and they are heavily influenced by the climatic conditions of their habitat. Owing to the harsh conditions of the high-altitude habitat, little is known about how ruminants regulate the host transcriptome and the composition of their rumen microbiota. Using the model species of goats, we examined the variations in the rumen microbiota, transcriptome regulation, and climate of the environment between high altitude (Lhasa, Xizang; 3650 m) and low altitude (Chengdu, Sichuan, China; 500 m) goats. The results of 16 S rRNA sequencing revealed variations in the abundance, diversity, and composition of rumen microbiota. Papillibacter, Quinella, and Saccharofermentans were chosen as potential microbes for the adaptation of Xizang goats to the harsh climate of the plateau by the Spearman correlation study of climate and microbiota. Based on rumen transcriptome sequencing analysis, 244 genes were found to be differentially expressed between Xizang goats and low-altitude goats, with 127 genes showing up-regulation and 117 genes showing down-regulation. SLC26A9, GPX3, ARRDC4, and COX1 were identified as potential candidates for plateau adaptation in Xizang goats. Moreover, the metabolism of fatty acids, arachidonic acids, pathway involving cytokines and their receptors could be essential for adaptation to plateau hypoxia and cold endurance. The expression of GPX3, a gene linked to plateau acclimatization in Xizang goats, was linked to the abundance of Anaerovibrio, and the expression of SLC26A9 was linked to the quantity of Selenomonas, according to ruminal microbiota and host Spearman correlation analysis. Our findings imply that in order to adapt harsh plateau conditions, Xizang goats have evolved to maximize digestion and absorption as well as to have a rumen microbiota suitable for the composition of their diet.

Keywords: Climate; Plateau adaptability; Rumen microbiota; Transcriptome; Xizang goat.

Fig. 1

Comparison of climate change in the living environment of Xizang goats and low-altitude goats. (A) Comparison of changes in average high temperatures. (B) Comparison of changes in average low temperatures. (C) Comparison of changes in average humidity. (D) Comparison of changes in average UV index. Lhasa represents high altitude, and Chengdu represents low altitude

Fig. 2

Comparison of changes in rumen microbiota α and β diversity in Xizang and low-altitude goats. (A) Chao1. (B) Shannon. (C) ACE. (D) PD-whole-tree. (E) PcoA. ⁎ denotes significant, ⁎⁎ denotes highly significant, ⁎⁎⁎ denotes extremely significant, Xizang goats represent HGRM, Low-altitude goats represent LGRM)

Fig. 3

Comparison of changes in rumen microbiota composition between Xizang and low-altitude goats. (A) Composition of microbiota phylum level in Xizang and low-altitude goats. (B) Composition of microbiota genus level in Xizang and low-altitude goats. (C) Cladogram generated from the LEfSe analysis indicating the phylogenetic distribution from phylum to genus levels of the microbiota of Xizang goats and low-altitude goats. (D) Histogram of LDA scores to identify differentially abundant bacterial genera between Xizang goats and low-altitude goats

Fig. 4

Correlation analysis between rumen microbiota and climate. ⁎ denotes significant, ⁎⁎ denotes highly significant, ⁎⁎⁎ denotes extremely significant

Fig. 5

DEGs in Xizang and low-altitude goats. (A) Trends in overall gene expression levels and expression in Xizang and low-altitude goats. (B) Clustering of DEGs in Xizang goats and low-altitude goats. (C) Volcano maps of DEGs in Xizang and low-altitude goats. Xizang goats represent HGRT, Low-altitude goats represent LGRT

Fig. 6

Functional enrichment analysis of DEGs. (A) Gene ontology (GO) classification map. (B, C) KEGG enrichment map of all differential genes

Fig. 7

Verification of DEGs using qRT-PCR

Fig. 8

Interactions between rumen plateau adaptation-related host genes and rumen microbes. ⁎ denotes significant, ⁎⁎ denotes highly significant, ⁎⁎⁎ denotes extremely significant