Metabolic and muscular adaptations to dietary succinate in Tan sheep: Insights from transcriptomics

Succinate (SUC), a dietary feed additive, is known to influence muscle fiber structure and lipid metabolism, thereby enhancing meat quality in livestock. This study evaluated the effects of SUC supplementation on growth performance, meat quality, muscle fiber morphology, and transcriptomic profiles of the liver and longissimus thoracis (LT) muscle in Tan sheep. Thirty 5-month-old male Tan sheep (31.48 ± 0.25 kg) were randomly allocated to three dietary treatments (n = 10 per group): control (CON) group (basal diet), SUC1 group (basal diet + 1.0% SUC), and SUC2 group (basal diet + 2.0% SUC). The trial lasted for 60 d. During d 1 to 15, adding SUC to the diet linearly increased average daily gain (ADG) (P = 0.003) and dry matter intake (DMI) (P < 0.001). During d 46 to 60, both ADG (P = 0.002) and DMI (P < 0.001) increased linearly. Over the overall period, DMI increased linearly (P < 0.001), and the feed to gain ratio (F/G) decreased linearly (P < 0.001). Carcass weight (P < 0.001) and dressing percentage (P = 0.004) increased linearly with SUC inclusion. Meat quality improved in both SUC groups, with significantly lower shear force (P = 0.004) and cooking loss (P < 0.001), and higher intramuscular fat (IMF) (P = 0.004) content and LT redness (a∗) value (P = 0.036). Succinate supplementation reduced muscle fiber diameter and cross-sectional area of type I and IIa fibers, while increasing type I and IIa fiber density (P < 0.05). Transcriptomic analyses revealed that SUC altered the expression of genes involved in muscle development, fiber-type transition, lipid metabolism, and circadian rhythm in both liver and LT tissues. Notably, the circadian rhythm pathway was enriched in both tissues, with differential expression of PER3, NR1D1, and NPAS2. Molecular docking demonstrated strong binding affinity of SUC to NPAS2 via stable hydrogen bonding, suggesting regulatory roles in circadian and muscle-related pathways. In conclusion, dietary SUC promotes metabolic and muscular adaptations in Tan sheep, improving feed efficiency and meat quality. Under the conditions of this experiment, considering growth performance, feed efficiency, and meat quality, a 1% dietary inclusion of SUC appears to be a practical optimum.