Sodium butyrate promotes gastrointestinal development of preweaning bull calves via inhibiting inflammation, balancing nutrient metabolism, and optimizing microbial community functions

Huiyue Zhong; Wenjing Yu; Min Wang; Bo Lin; Xuezhao Sun; Nan Zheng; Jiaqi Wang; Shengguo Zhao

doi:10.1016/j.aninu.2023.04.004

Sodium butyrate promotes gastrointestinal development of preweaning bull calves via inhibiting inflammation, balancing nutrient metabolism, and optimizing microbial community functions

Anim Nutr. 2023 Apr 25:14:88-100. doi: 10.1016/j.aninu.2023.04.004. eCollection 2023 Sep.

Authors

Huiyue Zhong¹, Wenjing Yu², Min Wang³, Bo Lin², Xuezhao Sun^{4

5}, Nan Zheng¹, Jiaqi Wang¹, Shengguo Zhao¹

Affiliations

¹ State Key Laboratory of Animal Nutrition, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100193, China.
² Department of Animal Science and Technology, Guangxi University, Nanning, 530005, China.
³ Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, 410125, China.
⁴ Jilin Inter-regional Cooperation Centre for the Scientific and Technological Innovation of Ruminant Precision Nutrition and Smart and Ecological Farming, Jilin Agricultural Science and Technology University, Jilin, 132109, China.
⁵ Grasslands Research Centre, AgResearch Limited, Palmerston North, New Zealand.

Abstract

Butyrate promotes the growth and gastrointestinal development of calves. But, the mechanisms behind its effects on signaling pathways of the gastrointestinal tract and rumen microbiome is unclear. This study aimed to reveal transcriptomic pathways of gastrointestinal epithelium and microbial community in response to butyrate supplementation in calves fed a high fiber starter. Fourteen Holstein bull calves (39.9 ± 3.7 kg, 14 d of age) were assigned to 2 groups (sodium butyrate group, SB; control group, Ctrl). The SB group received 0.5% SB supplementation. At d 51, the calves were slaughtered to obtain samples for analysis of the transcriptome of the rumen and jejunum epithelium as well as ruminal microbial metagenome. Sodium butyrate supplementation resulted in a higher performance in average daily gain and development of jejunum and rumen papillae. In both the rumen and jejunum epithelium, SB down-regulated pathways related to inflammation including NF-κB (PPKCB, CXCL8, CXCL12), interleukin-17 (IL17A, IL17B, MMP9), and chemokine (CXCL12, CCL4, CCL8) and up-regulated immune pathways including the intestinal immune network for immunoglobulin A (IgA) production (CD28). Meanwhile, in the jejunum epithelium, SB regulated pathways related to nutritional metabolism including nitrogen metabolism (CA1, CA2, CA3), synthesis and degradation of ketone bodies (HMGCS2, BDH1, LOC100295719), fat digestion and absorption (PLA2G2F, APOA1, APOA4), and the PPAR signaling pathway (FABP4, FABP6, CYP4A11). The metagenome showed that SB greatly increased the relative abundance of Bacillus subtilis and Eubacterium limosum, activated ruminal microbial carbohydrate metabolism pathways and increased the abundance of carbohydrate hydrolysis enzymes. In conclusion, butyrate exhibited promoting effects on growth and gastrointestinal development by inhibiting inflammation, enhancing immunity and energy harvesting, and activating microbial carbohydrate metabolism. These findings provide new insights into the potential mechanisms behind the beneficial effects of butyrate in calf nutrition.

Keywords: Calf; Gastrointestinal development; Inflammation; Microbiome; Sodium butyrate; Transcriptomics.