Integrated multi-omics of the ruminal microbiome and host metabolome reveals compensatory growth in response to dietary energy restriction and re-alimentation in growing beef bulls

Understanding the mechanisms of dietary energy on compensatory growth in beef cattle is crucial for improving feed efficiency and mitigating the environmental footprint of beef production. The objectives of the study were to investigate the effects of dietary energy restriction and subsequent re-alimentation on growth performance, nutrient digestibility, ruminal microbiome, plasma metabolites, and nitrogen metabolism in growing beef bulls. Twelve 6–8-month-old Simmental crossbred bulls (initial body weight: 226 ± 24 kg) were randomly allocated to two groups ( n = 6 per group): the dietary energy restriction group (REC) was fed a diet containing 9.25 MJ/kg metabolizable energy (ME) for 4 weeks (energy restriction period), followed by a 2-week re-alimentation period with a 10.29 MJ/kg ME diet, while the control group (CON) was fed the 10.29 MJ/kg ME diet consistently throughout the experimental period. Dietary energy restriction significantly decreased body weight and average daily gain (ADG) compared to CON ( P < 0.05). However, no significant differences were observed by the end of the re-alimentation period ( P > 0.05), demonstrating successful compensatory growth through dietary energy modulation. Ruminal propionate, total volatile fatty acids, ammonium nitrogen, and microbial crude protein (MCP) concentrations significantly decreased in the energy restriction treatment compared to CON ( P < 0.05), but MCP exceeded the levels in CON after dietary energy re-alimentation ( P < 0.05). Energy restriction also significantly increased urinary nitrogen excretion ( P = 0.002), driven by imbalanced amino acid metabolism and significantly increased urinary urea ( P = 0.038), which significantly reduced protein synthesis and nitrogen retention ( P = 0.017). Metagenomics analysis revealed that energy restriction significantly increased the relative abundances of Limosilactobacillus , Enterococcus , and Aliarcobacter ( P < 0.05), while decreasing those of Gemmatirosa and Mesorhizobium ( P < 0.05). Dietary energy re-alimentation significantly increased the relative abundance of Gramella , Acetobacter , Phaeobacter , and Flammeovirga ( P < 0.05). These bacteria are associated with pathways related to amination, transamination, and microbial protein synthesis. Integrated multi-omics revealed shifts in the ruminal microbiome and host metabolome, particularly in pathways related to ruminal urea hydrolysis, biosynthesis of glutamate, glutamine, and alanine, and post-absorptive amino acid metabolism, which collectively enhanced protein synthesis and compensatory growth. These findings establish a practical feeding strategy to optimize feed efficiency and enhance compensatory growth in beef bulls via short-term dietary energy manipulation.