Multi-Omics Reveals That the Rumen Transcriptome, Microbiome, and Its Metabolome Co-regulate Cold Season Adaptability of Tibetan Sheep

Abstract

Tibetan sheep can maintain a normal life and reproduce in harsh environments under extreme cold and lack of nutrition. However, the molecular and metabolic mechanisms underlying the adaptability of Tibetan sheep during the cold season are still unclear. Hence, we conducted a comprehensive analysis of rumen epithelial morphology, epithelial transcriptomics, microbiology and metabolomics in a Tibetan sheep model. The results showed that morphological structure of rumen epithelium of Tibetan sheep in cold season had adaptive changes. Transcriptomics analysis showed that the differential genes were primarily enriched in the PPAR signaling pathway (ko03320), legionellosis (ko05134), phagosome (ko04145), arginine and proline metabolism (ko00330), and metabolism of xenobiotics by cytochrome P450 (ko00980). Unique differential metabolites were identified in cold season, such as cynaroside A, sanguisorbin B and tryptophyl-valine, which were mainly enriched in arachidonic acid metabolism, arachidonic acid metabolism and linolenic acid metabolism pathways, and had certain correlation with microorganisms. Integrated transcriptome-metabolome-microbiome analysis showed that epithelial gene-GSTM3 expression was upregulated in the metabolism of xenobiotics by the cytochrome P450 pathway during the cold season, leading to the downregulation of some harmful metabolites; TLR5 gene expression was upregulated and CD14 gene expression was downregulated in the legionellosis pathway during the cold season. This study comprehensively described the interaction mechanism between the rumen host and microbes and their metabolites in grazing Tibetan sheep during the cold season. Rumen epithelial genes, microbiota and metabolites act together in some key pathways related to cold season adaptation.

Effects of Heated Drinking Water during the Cold Season on Serum Biochemistry, Ruminal Fermentation, Bacterial Community, and Metabolome of Beef Cattle

“…Additionally, the RTW diminished Prevotella, norank_f_p-215-o5, and Succinivibrionaceae, consistent with the findings of He et al [32] and Cui et al [38]. The prominence of Prevotella, principally engaged in degrading non-structural carbohydrates and fostering propionate production [39], aligns with the hypothesis that cold water intake induced beef cattle's augmented energy requirements during cooler periods. Furthermore, our correlation analysis revealed an interplay between microbiota and fermentation parameters.…”

Coevolution of Rumen Epithelial circRNAs with Their Microbiota and Metabolites in Response to Cold-Season Nutritional Stress in Tibetan Sheep

“…To further explore the differences in genetic characteristics, physiological activities, and energy metabolism of Tibetan sheep during altitude acclimatization, this study conducted correlation analysis among circRNAs of rumen epithelium, previously measured rumen microbiota, and rumen microbial metabolites [ 4 , 15 ]. As shown in Figure 7 A, there was a correlation between circRNAs and rumen microbiota.…”

“…At present, studies on circRNAs have mainly focused on the gastrointestinal tract of humans [ 11 ] and mice [ 14 ], while studies related to circRNAs in the rumen epithelium of ruminants have rarely been reported. Therefore, based on previous research [ 4 , 15 ], this study revealed nutritional stress of Tibetan sheep in the cold season through the interaction of rumen epithelial circRNAs with microbiota and metabolites, further explored the coevolutionary effect between the host genome and microbial genome, and provided a basis for analyzing the response of Tibetan sheep to nutritional stress in the cold season on the Qinghai-Tibet Plateau.…”

Global DNA Methylation, miRNA, and mRNA Profiles in Sheep Skeletal Muscle Promoted by Hybridization

“…Systems biology research driven by multiomics will bring in new trends and paradigms. Multiomics allows a comprehensive understanding of the systematic study of biology and can integrate genomics, epigenomics, transcriptomics, etc., to systematically analyze the mechanisms and phenotypes of complex life systems. − Zhan et al used transcriptomics and metabolomics and obtained 120 differentially expressed genes (DEGs) and 171 significantly changed metabolites that contributed to the content of intramuscular fat through fat accumulation and regulation of lipolysis in Enshi black pork . Using results obtained from the longissimus dorsi muscle, Zhang et al found some genes, miRNAs, and lncRNA related to intramuscular fat deposition and bone development, and proposed the miRNA ssc-let-7a as the main modulator of fat deposition through the regulation of GALNT15 (N-acetylgalactosaminyltransferases 15), PPARGC1A (PPARG coactivator 1 alpha), and FKBP5 (FKBP prolyl isomerase 5) genes .…”