Cecal Microbial Diversity and Metabolome Reveal a Reduction in Growth Due to Oxidative Stress Caused by a Low-Energy Diet in Donkeys

Dietary energy level plays an important role in animal growth and development. The present study investigated the effect of dietary energy on the growth performance, antioxidative state, and nutrient digestion of meat donkeys. It simultaneously explored the probable reason for cecal microbiota and metabolome. Twelve meat donkeys (male) aged 1 year with a similar weight (150 ± 25 kg) were divided into two treatment groups: low-energy group (E1) and high-energy group (E2). The experiment was divided into a 10-day pre-trial period and a 135-day trial period. Donkeys in the trial periods were fed diets with digestible energy values (in dry matter) of 12.08 and 13.38 MJ/kg (pre-fattening, 1-45 d), 13.01 and 14.27 MJ/kg (mid-fattening, 46-90 d), and 13.54 and 14.93 MJ/kg (late-fattening, 91-135 d). The results show that E1 decreases body weight, average daily gain (ADG), and the digestibility of crude protein, ether extract, neutral detergent fiber, and acid detergent fiber (<i>p</i> < 0.05), but increases cecal acetate and butyrate concentrations, non-esterified fatty acids (NEFAs) in serum, and the ratio of dry matter intake to ADG(F/G). E1 diminished the activities of catalase and glutathione peroxidase, while it increased the content of interleukin, tumor necrosis factor-alpha, and reactive oxygen species (ROS) (<i>p</i> < 0.05). Cecal microbiome showed that the abundance of <i>Firmicutes</i> and <i>Actinobacteria</i> in E1 was significantly lower than in E2 (<i>p</i> = 0.029, <i>p</i> = 0.002), whereas <i>Bacteroidetes</i> was higher (<i>p</i> = 0.005). E1 increased the genera <i>Ruminococcaceae-UCG-004</i>, <i>Acinetobacter</i>, and <i>Rikenellaceae_RC9_gut_group</i>. Meanwhile, cecal metabolome showed that formyl-5-hydroxykynurenamine, chorismate, 3-sulfinoalanine, and 3-isopropylmalate were upregulated in E1, while brassinolide was downregulated. The altered metabolites were mainly enriched in metabolic pathways related to energy metabolism and metabolism to mitigate oxidative stress in the meat donkeys, such as tryptophan metabolism, brassinosteroid biosynthesis metabolism, etc. In conclusion, low-energy diets resulted in a negative energy balance in meat donkeys, resulting in more nutrients being oxidized to provide energy, inducing oxidative stress, and thereby leading to decreasing growth. The reduction in meat donkey growth from low-energy diets was related to changes in cecum microbiota and metabolites.