Abstract
BackgroundDairy cows utilize human-inedible, low-value plant biomass to produce milk, a low-cost product with rich nutrients and high proteins. This process largely relies on rumen microbes that ferment lignocellulose and cellulose to produce volatile fatty acids (VFAs). The VFAs are absorbed and partly metabolized by the stratified squamous rumen epithelium, which is mediated by diverse cell types. Here, we applied a metagenomic binning approach to explore the individual microbes involved in fiber digestion and performed single-cell RNA sequencing on rumen epithelial cells to investigate the cell subtypes contributing to VFA absorption and metabolism.ResultsThe 52 mid-lactating dairy cows in our study (parity = 2.62 ± 0.91) had milk yield of 33.10 ± 6.72 kg. We determined the fiber digestion and fermentation capacities of 186 bacterial genomes using metagenomic binning and identified specific bacterial genomes with strong cellulose/xylan/pectin degradation capabilities that were highly associated with the biosynthesis of VFAs. Furthermore, we constructed a rumen epithelial single-cell map consisting of 18 rumen epithelial cell subtypes based on the transcriptome of 20,728 individual epithelial cells. A systematic survey of the expression profiles of genes encoding candidates for VFA transporters revealed that IGFBP5+ cg-like spinous cells uniquely highly expressed SLC16A1 and SLC4A9, suggesting that this cell type may play important roles in VFA absorption. Potential cross-talk between the microbiome and host cells and their roles in modulating the expression of key genes in the key rumen epithelial cell subtypes were also identified.ConclusionsWe discovered the key individual microbial genomes and epithelial cell subtypes involved in fiber digestion, VFA uptake and metabolism, respectively, in the rumen. The integration of these data enables us to link microbial genomes and epithelial single cells to the trophic system.1dVKuikNrJ1xsEB1JvqD2DVideo abstract
Highlights
Dairy cows utilize human-inedible, low-value plant biomass to produce milk, a low-cost product with rich nutrients and high proteins
All 186 metagenome‐assembled genomes (MAGs) had < 95% average nucleotide identity (ANI), which means that these 186 species were nonredundant
Clusters 1, 2, and 9 were predicted to be three spinous cell subtypes (SC_13) because they did not express the basal cell markers but slightly expressed the spinous cell marker KRT10 [33] or granule cell marker DLK2 (Fig. 4B). These indicated that they may serve as the spinous cell types between basal cell and terminally differentiated granulear cell, and we identified their highly expressed genes (Figure S5D)
Summary
Dairy cows utilize human-inedible, low-value plant biomass to produce milk, a low-cost product with rich nutrients and high proteins. This process largely relies on rumen microbes that ferment lignocellulose and cel‐ lulose to produce volatile fatty acids (VFAs). Xue et al Microbiome (2022) 10:11 into volatile fatty acids (VFAs), and how are the VFAs absorbed by the host is crucial for improving the efficiency of animal production. Such a process largely relies on the symbiotic microbiota in the rumen [3]. The fiber digestion and fermentation functions of uncultivated microbial genomes in the rumen of lactating Holstein dairy cattle (one of the most common milk-producing dairy cattle) are still under investigated
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