Effects of castration-associated hormonal changes on rumen microbiota, metabolism, and meat quality in Holstein cattle

It remains unclear whether hormones and microorganisms affect growth performance and meat quality, and whether there is an interaction between them. In this study, nine Holstein bulls and nine Holstein steers were fed for 270 days under the same management conditions. We combined rumen microbiomics, metabolomics, and epithelial transcriptomics with serum and muscle metabolomics as well as serum hormone detection, to explore how rumen microbes and hormones jointly regulate growth performance and beef quality of Holstein cattle. Compared with bull group, the Lightness ( L* ), Redness ( a* ), Yellowness ( b* ), intramuscular fat and marbling score were significantly increased in steer group ( P < 0.05). Serum testosterone, triiodothyronine, thyroxine, growth hormone, leptin, and glucagon levels were significantly lower in steer group, which also reflected that castration inhibited final body weight (FBW), average daily gain (ADG), dry matter intake (DMI), gain feed ratio (G/F) ( P < 0.05). Cellulase, pectinase, β-glucosidase, acetate, propionate and butyrate were significantly lower, while α-amylase and lipase were significantly higher in steer group ( P < 0.05). The rumen metagenome indicates unclassified_o_Bacteroidales and unclassified_f_Lachnospiraceae were significantly abundant of steer and bull groups, respectively; the functions that determined beef quality were primarily in lipid and fat anabolic pathway; and the hormones and microbes had a strong correlation. Serum and muscle metabolites of steer group were involved in fatty acid metabolism, whereas bull group were primarily involved in amino acid and protein metabolism; and Lysophosphatidylethanolamines (LPE (0:0/20:3) and (20:3/0:0)) significantly influenced marbling score and intramuscular fat. The explanations of comprehensive membership value (CMV) in the rumen microbiome, rumen metabolism, serum metabolism, muscle metabolism, and rumen epithelial genes were 29.90%, 4.50%, 10.50%, 1.60%, and 0.01%. Castration could inhibit growth performance and improve meat quality, by mainly regulating rumen microorganisms (29.90%) and serum metabolism (10.50%); this study also provides a significant theoretical basis for analyzing the regulatory mechanisms of castration on growth performance and meat quality of cattle.