Castration alters the cecal microbiota and inhibits growth in Holstein cattle

Abstract To determine the effects of castration on growth performance, serum hormone levels, cecal microbiota composition, and metabolites in cattle. A total of 18 Holstein bulls and steers were divided into bull and steer groups and randomly assigned to 3 pens (3 cattle per pen, and each cattle were separated by a fence) to determine the average daily gain (ADG), daily dry matter intake (DMI), and feed efficiency (G/F). After the finishing trial, six cattle per group were randomly slaughtered. Serum was collected to measure the hormone concentration, and the cecal content was collected to measure the pH, short-chain fatty acids, and digestive enzyme activities. Metagenome sequencing and untargeted metabolomics were used to investigate the microbiota composition, functional profiles, and differential metabolites of the cecal contents. We found that castration significantly decreased ADG, DMI, and G/F in cattle (P < 0.05). The serum testosterone, thyroxine, growth hormone (P < 0.05), and triiodothyronine (P < 0.01) concentrations significantly decreased in the steer group when compared to those of the bull group. The activities of cellulase, xylanase, pectinase, and β-glucosidase (P < 0.05) significantly decreased in the steer group, whereas the activities of lipase and α-amylase significantly increased. Moreover, castration significantly decreased the relative abundance of Ruminococcaceae_bacterium, Treponema_porcinum, Oscillibacter_sp. (P < 0.05), and Alistipes_senegalensis (P < 0.01), whereas the relative abundance of Phocaeicola_plebeius (P < 0.05) was significantly increased. Also, the relative abundance of Phocaeicola_plebeius was negatively correlated with testosterone levels, and the function of the cecal microbiota was enriched in the GH29 and GH97 families in the steer group. Metabolomic analysis indicated that castration increased the levels of L-valine, L-phenylalanine, L-aspartic acid, L-isoleucine, L-lysine, methionine, L-glutamic acid, and L-leucine, while decreasing the levels of α-ketoglutaric acid through the 2-oxocarboxylic acid metabolism pathway. In addition, α-ketoglutaric acid was negatively correlated with Oscillibacter_sp. (P < 0.01). Overall, castration can inhibit cattle growth by altering the composition of the cecal microbiota. Therefore, this study provides a theoretical and practical basis for improving the growth performance of steers.