The rumen is divided into multiple rumen sacs based on anatomical structure, and each has its unique physiological environment. Tarim wapiti preserved roughage tolerance after domestication, and adaptation to the desertified environment led to the development of a unique rumen shape and intraruminal environment. In this work, six Tarim wapiti were chosen and tested for fermentation parameters, microbes, and histomorphology in four rumen areas (Dorsal sac, DS; Ventral sac, VS; Caudodorsal blind sac, CDBS; Caudoventral blind sac, CVBS). Tarim wapiti’s rumen blind sac had better developed rumen histomorphology, the ventral sac was richer in VFAs, and the dominant bacteria varied most notably in the phylum Firmicutes, which was enriched in the caudoventral blind sac. The ventral sac biomarkers focused on carbohydrate fermentation-associated bacteria, the dorsal sac focused on N recycling, and the caudoventral blind sac identified the only phylum-level bacterium, Firmicutes; we were surprised to find a probiotic bacterium, Bacillus clausii, identified as a biomarker in the ventral sac. This research provides a better understanding of rumen fermentation parameters, microorganisms, and histomorphology in the Tarim wapiti rumen within a unique ecological habitat, laying the groundwork for future regulation targeting the rumen microbiota and subsequent animal production improvement.

Under long-term ecological stress, the Tarim wapiti (Cervus elaphus yarkandensis) has evolved unique adaptations in digestive physiology and energy metabolism. A multi-omics comparison of three Tarim wapiti and five Karakul sheep was used to examine the synergistic mechanism between rumen bacteria, short-chain fatty acids, and host epithelial regulation in order to clarify the mechanism of high roughage digestion efficiency in Tarim wapiti. Metagenomic sequencing (Illumina NovaSeq 6000) and gas chromatography revealed that Tarim wapiti exhibited significantly higher acetate and total VFA (TVFA) concentrations compared to Karakul sheep (p < 0.01), accompanied by lower ruminal pH and propionate levels. Core microbiota analysis identified Bacteroidetes (relative abundance: 52.3% vs. 48.1%), Prevotellaceae (22.7% vs. 19.4%), and Prevotella (18.9% vs. 15.6%) as dominant taxa in both species, with significant enrichment of Bacteroidetes in wapiti (p < 0.01). Functional annotation (PICRUSt2) demonstrated enhanced glycan biosynthesis (KEGG ko00511), DNA replication/repair (ko03430), and glycoside hydrolases (GH20, GH33, GH92, GH97) in wapiti (FDR < 0.05). Transcriptomic profiling (RNA-Seq) of rumen epithelium showed upregulated expression of SCFA transporters (PAT1: 2.1-fold, DRA: 1.8-fold, AE2: 2.3-fold; p < 0.01) and pH regulators (Na⁺/K⁺ ATPase: 1.7-fold; p < 0.05) in wapiti. Integrated analysis revealed coordinated microbial–host interactions through three key modules: (1) Bacteroidetes-driven polysaccharide degradation, (2) GHs-mediated fiber fermentation, and (3) epithelial transporters facilitating short-chain fatty acids absorption. These evolutionary adaptations, particularly the Bacteroidetes–short-chain fatty acids–transporter axis, likely underpin the wapiti’s superior roughage utilization efficiency, providing molecular insights for improving ruminant feeding strategies in an arid environment.