Rumen microbiota-host transcriptome interaction mediates the protective effects of trans-10, cis-12 CLA on facilitating weaning transition of lambs

Chunlei Yang; Xiangfei Deng; Peter Lund; Haixia Liu; Xingwang Ding; Zhengwei Fu; Naifeng Zhang; Jinjun Li; Lifeng Dong

doi:10.1016/j.aninu.2022.11.002

Rumen microbiota-host transcriptome interaction mediates the protective effects of trans-10, cis-12 CLA on facilitating weaning transition of lambs

Anim Nutr. 2022 Nov 21:12:345-359. doi: 10.1016/j.aninu.2022.11.002. eCollection 2023 Mar.

Authors

Chunlei Yang¹, Xiangfei Deng¹, Peter Lund², Haixia Liu³, Xingwang Ding³, Zhengwei Fu¹, Naifeng Zhang⁴, Jinjun Li⁵, Lifeng Dong⁴

Affiliations

¹ College of Biotechnology and Bioengineering, Zhejiang University of Technology, Hangzhou, 310014, China.
² Department of Animal Science, Aarhus University, AU Foulum, DK-8830, Tjele, Denmark.
³ Jiangsu Agri-animal Husbandry Vocational College, Taizhou, 225300, China.
⁴ Institute of Feed Research, Chinese Academy of Agricultural Sciences/Sino-US Joint Lab on Nutrition and Metabolism of Ruminant, Beijing, 100081, China.
⁵ Institute of Food Sciences, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China.

Abstract

Developing alternatives to antibiotics for prevention of gastrointestinal dysbiosis in early-weaning farmed animals is urgently needed. This study was to explore the potential effects of trans-10, cis-12 conjugated linoleic acid (CLA) on maintaining ruminal homeostasis of young ruminants during the weaning transition period. Thirty neonatal lambs were selected (6 lambs per group) and euthanized for rumen microbial and epithelial analysis. The lambs were weaned at 28 d and experienced the following 5 treatments: euthanized on d 28 as the pre-weaning control (CON0), fed starter feed for 5 (CON5) or 21 (CON21) d, fed starter feed with 1% of CLA supplemented for 5 (CLA5) or 21 (CLA21) d. Results showed that the average daily weight gain and dry matter intake were significantly higher in CLA5 than CON5 group. As compared with the CON5 and CON21 group, the relative abundances of volatile fatty acid (VFA) producing bacteria including Bacteroides, Treponema, Parabacteroides and Anaerovibrio, as well as the concentrations of acetate, butyrate and total VFA were significantly increased in CLA5 and CLA21 group, respectively. Integrating microbial profiling and epithelial transcriptome results showed that 7 downregulated inflammatory signaling-related host genes IL2RA, CXCL9, CD4, CCR4, LTB, SPP1, and BCL2A1 with CLA supplementation were significantly negatively correlated with both VFA concentration and VFA producing bacteria, while 3 (GPX2, SLC27A2 and ALDH3A1) and 2 (GSTM3 and GSTA1) upregulated metabolism-related genes, significantly positively correlated with either VFA concentration or VFA producing bacteria, respectively. To confirm the effects of CLA on epithelial signal transduction, in vitro experiment was further conducted by treating rumen epithelial cells without or with IL-17A + TNF-α for 12 h after pretreatment of 100 μM CLA or not (6 replicates per treatment). The results demonstrated the anti-inflammatory effect of CLA via suppressing the protein expression of NF-кB p-p65/p65 with the activation of peroxisome proliferator-activated receptor gamma (PPARγ). In conclusion, CLA supplementation enhanced the ruminal microbiota-driven transcriptional regulation in healthy rumen epithelial development via rumen VFA production, and CLA may therefore serve as an alternative way to alleviate early-weaning stress and improve physiological and metabolic conditions of young ruminants.

Keywords: Epithelial transcriptome; Peroxisome proliferator-activated receptor gamma; Rumen microbiota; Trans-10,cis-12 conjugated linoleic acid; Weaning stress.