Regulatory effects of tea polysaccharides on hepatic inflammation, gut microbiota dysbiosis, and serum metabolomic signatures in beef cattle under heat stress

Abstract

Background: Long-term heat stress (HS) severely restricts the growth performance of beef cattle and causes various health problems. The gut microbiota plays a crucial role in HS-associated inflammation and immune stress involving lymphocyte function. This study investigated the effects of dietary tea polysaccharide (TPS), a natural acidic glycoprotein, on HS-induced anorexia, inflammation, and gut microbiota dysbiosis in Simmental beef cattle.

Methods: The cattle were divided into two groups, receiving either normal chow or normal chow plus TPS (8 g/kg, 0.8%). Transcriptome sequencing analysis was used to analysis the differential signaling pathway of liver tissue. 16S rDNA sequencing was performed to analysis gut microbiota of beef cattle. Serum metabolite components were detected by untargeted metabolomics analysis.

Results: Hepatic transcriptomics analysis revealed that differentially expressed genes in TPS-fed cattle were primarily enriched in immune processes and lymphocyte activation. TPS administration significantly reduced the expression of the TLR4/NF-κB inflammatory signaling pathway, alleviating HS-induced hepatic inflammation. Gut microbiota analysis revealed that TPS improved intestinal homeostasis in HS-affected cattle by increasing bacterial diversity and increasing the relative abundances of Akkermansia and Alistipes while decreasing the Firmicutes-to-Bacteroidetes ratio and the abundance of Agathobacter. Liquid chromatography-tandem mass spectrometry (LC‒MS/MS) analysis indicated that TPS significantly increased the levels of long-chain fatty acids, including stearic acid, linolenic acid, arachidonic acid, and adrenic acid, in the serum of cattle.

Conclusion: These findings suggest that long-term consumption of tea polysaccharides can ameliorate heat stress-induced hepatic inflammation and gut microbiota dysbiosis in beef cattle, suggesting a possible liver-gut axis mechanism to mitigate heat stress.

Keywords: gut micobiota; inflammation; liver; long-chain fatty acids; tea polysaccharides.

FIGURE 1

Effects of tea polysaccharides on hepatic inflammation and immune stress in beef cattle under heat stress. (A). Gene Ontology (GO) functional enrichment analysis of the top 10 differentially expressed genes (DEGs) in the liver of the control and tea polysaccharide groups. (B). Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway enrichment analysis of the top 10 DEGs in the livers of the control and tea polysaccharide groups. (C) The top 10 GO enrichment circles of DEGs in the liver of the control and tea polysaccharide groups. (D) The map showing the relative expression levels of genes involved in inflammation in the liver of cattle. *p < 0.05, **p < 0.01 and ***p < 0.001, n = 4.

FIGURE 2

Effects of tea polysaccharides on microbiota composition of beef cattle under heat stress. (A) Stachyose increased the alpha diversity of the gut microbiota in beef cattle. Venn diagram showing the number of the same microbiota and unique microbiota between the control and tea polysaccharide groups (OTU level). (B–G) The observed species (B), ACE index (C), Chao1 index (D), PD-tree index (E), Simpson index (F) and Shannon index (G) were used to describe the alpha diversity of bacterial assemblages in beef cattle between groups. n = 4.

FIGURE 3

Bacterial community composition similarity. Tea polysaccharides improved the effects of heat stress on the bacterial community. (A) Principal coordinate analysis (PCoA) plots. (B) Nonmetric multidimensional scaling (NMDS) plots. (C) Principal component analysis (PCA) based on Bray−Curtis dissimilarity. (D) Cladogram visualizing the output of the LEfSe algorithm, which identifies taxonomically consistent differences between groups. The yellow dots represent nonsignificant bacteria in the groups; other colored dots are significant bacteria in the group labeled with the same color. (E) Histogram showing the LDA scores computed for features (genus level) that were differentially abundant between different treatments. The higher the LDA score is, the more significant the bacteria are.

FIGURE 4

Changes in the taxonomic composition of the cecum microbiota communities at the phylum and genus levels (A–C) Changes in the relative abundance of bacteria at the phylum and genus levels. (B) The Firmicutes-to-Bacteroidetes ratio of the groups. (D) Bacteria with significant changes in abundance (genus level). (E) Species abundance heatmap between the microbiota and samples of the groups at the genus level. *p < 0.05, n = 4.

FIGURE 5

Influence of tea polysaccharides on the serum metabolomic signatures of beef cattle. (A) Plots of orthogonal partial least squares-discriminant analysis (OPLS-DA). (B) Partial least squares discriminant analysis (PLS-DA) scaling plots. (C) Volcano plot showing changes in the relative abundance of metabolites in the groups. (D) Heatmap of differentially abundant metabolites of the groups. (E) KEGG pathway enrichment analysis of differentially abundant metabolites in the serum of the control and tea polysaccharide groups. N = 5.

FIGURE 6

Association analysis of intestinal microbiota and serum metabolites in tea polysaccharide-fed beef cattle. (A) Spearman correlation analysis was conducted between the groups; red represents a positive correlation, and blue represents a negative correlation. *p < 0.05, **p < 0.01 and ***p < 0.001.