2. Academic Validation
  3. Early-life ruminal microbiome-derived indole-3-carboxaldehyde and prostaglandin D2 are effective promoters of rumen development

Early-life ruminal microbiome-derived indole-3-carboxaldehyde and prostaglandin D2 are effective promoters of rumen development

  • Genome Biol. 2024 Mar 4;25(1):64. doi: 10.1186/s13059-024-03205-x.
Daming Sun # 1 2,  Gaorui Bian # 3,  Kai Zhang 1,  Ning Liu 1,  Yuyang Yin 4,  Yuanlong Hou 2,  Fei Xie 1,  Weiyun Zhu 1,  Shengyong Mao 1,  Junhua Liu 5
Affiliations

Affiliations

  • 1 Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China.
  • 2 Laboratory of Metabolism and Drug Target Discovery, State Key Laboratory of Natural Medicines, College of Pharmacy, China Pharmaceutical University, Nanjing, 210009, China.
  • 3 College of Animal Science and Food Engineering, Jinling Institute of Technology, Nanjing, 210038, China.
  • 4 Huzhou Academy of Agricultural Sciences, Huzhou, 313000, China.
  • 5 Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, National Center for International Research On Animal Gut Nutrition, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, 210095, China. liujunhua0011@163.com.
  • # Contributed equally.
PMID: 38438919 DOI: 10.1186/s13059-024-03205-x
Abstract

Background: The function of diverse ruminal microbes is tightly linked to rumen development and host physiology. The system of ruminal microbes is an excellent model to clarify the fundamental ecological relationships among complex nutrient-microbiome-host interactions. Here, neonatal lambs are introduced to different dietary regimes to investigate the influences of early-life crosstalk between nutrients and microbiome on rumen development.

Results: We find starchy corn-soybean starter-fed lambs exhibit the thickest ruminal epithelia and fiber-rich alfalfa hay-fed lambs have the thickest rumen muscle. Metabolome and metagenome data reveal that indole-3-carboxaldehyde (3-IAld) and prostaglandin D2 (PGD2) are the top characteristic ruminal metabolites associated with ruminal epithelial and muscular development, which depend on the enhanced ruminal microbial synthesis potential of 3-IAld and PGD2. Moreover, Microbial Culture experiment first demonstrates that Bifidobacterium pseudolongum is able to convert tryptophan into 3-IAld and Candida albicans is a key producer for PGD2. Transcriptome Sequencing of the ruminal epithelia and smooth muscle shows that ruminal epithelial and muscular development is accompanied by Wnt and CA2+ signaling pathway activation. Primary cell cultures further confirm that 3-IAld promotes ruminal epithelial cell proliferation depending on AhR-wnt/β-catenin signaling pathway and PGD2 accelerates ruminal smooth muscle cell proliferation via CA2+ signaling pathway. Furthermore, we find that 3-IAld and PGD2 infusion promote ruminal epithelial and musculature development in lambs.

Conclusions: This study demonstrates that early-life ruminal microbiome-derived 3-IAld and PGD2 are effective promoters of rumen development, which enhances our understanding of nutrient-microbiome-host interactions in early life.

Keywords

Lamb; Microbial–host interaction; Rumen development; Solid diet.

Figures
Products