A Comparison Between High- and Low-Performing Lambs and Their Impact on the Meat Quality and Development Level Using a Multi-Omics Analysis of Rumen Microbe–Muscle–Liver Interactions

Through an integrated multi-omics analysis of rumen microbial communities, muscle transcriptomes, metabolic profiles, and liver metabolic profiles, this study systematically compared high- and low-performing lambs to elucidate their divergent effects on meat quality attributes and growth development. A total of 100 male lambs with similar birth weight (3.07 ± 0.06 kg) were selected within 72 h. All test lambs were synchronized weaning at 45 days of age and uniformly fed the same diet (total mixed ration) in the same pen until 180 days of age, with ad libitum access to food and water throughout this period. Subsequently, the eight lambs with the highest (HADG) and lowest (LADG) average daily gains were slaughtered for performance evaluation and multi-omics analysis. This study found that HADG lambs increased body weight, muscle fiber diameter, eye muscle area, improved amino acid (histidine, arginine, valine, isoleucine, essential amino acid/total amino acid, and essential amino acid/nonessential amino acid), and fatty acid (linoleic acid, behenic acid, and arachidonic acid) composition enhanced rumen enzymes (pepsase, lipase, xylanase, amylase, and carboxymethyl cellulose) and promoted efficient fermentation (<i>p</i> < 0.05). Analysis of microbial populations indicated a notable increase in <i>Prevotella</i> levels within the rumen of HADG lambs. Furthermore, the rumen markers <i>Schwartzia</i> and <i>Streptococcus</i> exhibited significant correlations with differential meat quality traits. Analysis of the muscle transcriptome indicated a significant correlation between the turquoise module and host phenotypes, particularly body weight. Additionally, muscle metabolism is primarily concentrated within the black module; however, it exhibits a significant correlation with the host body phenotype in the yellow module (<i>p</i> < 0.05). Moreover, liver metabolites, rumen microbes, host phenotype, and muscle transcripts were significantly correlated (<i>p</i> < 0.05). In conclusion, the interactions among rumen microbes, muscle, and liver in lambs promote rumen fermentation, which in turn regulate muscle transcriptional activity and modify metabolic profiles in both the liver and muscle. Moreover, <i>PCK1</i>, <i>SPP1</i>, <i>FGF7</i>, <i>NR4A1</i>, <i>DUSP5</i>, <i>GADD45B</i>, etc., can be candidate genes for muscle growth and development. This finding provides a theoretical basis for further exploiting the production potential of Hu lambs.