Abstract

Whether dietary non-fiber carbohydrate (NFC), a rapid fermentable substance, affects immune homeostasis of rumen through the modulation of interactions of ruminal microbiota and epithelial toll-like receptors (TLRs) remains unclear. A combination of 16S rRNA amplicon sequencing and quantitative PCRs was applied to study the synergetic responses of ruminal microbiota and epithelial TLRs to the dietary NFC switch from 15 to 31% in the goat model. The results showed that the 31% NFC diet caused the radical increases on the richness and diversity of rumen microbiota. The phylum Verrucomicrobia was most significantly expanded, whereas opportunistic pathogens, namely Rikenella, Anaeroplasma, and Olsenella, were significantly decreased. In rumen epithelium, the significantly increased expressions of TLR1, 6, 10 were associated with the significantly decreased expressions of pro-inflammatory cytokines interleukin-1beta (IL-1ß), IL-6, and anti-inflammatory cytokine IL-10. Constrained correlation analysis indicated that the increased abundance of commensal bacteria in Verrucomicrobia subdivision 5 contributed to the upregulation of TLR10 expression. Finally, the significantly increased concentrations of rumen short-chain fatty acids (SCFAs), coupled with the significantly upregulated expressions of epithelial genes related to SCFA absorption were observed in goats fed with 31% NFC diet. Thus, the NFC-induced expansion of rumen microbiota promoted epithelium tolerance by enhancement of the intensity of TLR10 signaling. The newly established equilibrium benefited to the transport of ruminal energy substances into the blood.

Highlights

  • The rumen is the most important site for digestion and absorption in ruminant animals

  • A total of 22 prokaryotic phyla were identified by comparing with the ribosomal database project (RDP) databases at a 97% similarity threshold, and 15 phyla were common to both groups (Figure 1)

  • WS3 was only detected in the LNFC group, whereas Elusimicrobia, Armatimonadetes, Gemmatimonadetes, Cyanobacteria, Nitrospira, and Planctomycetes were only detected in the MNFC group

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Summary

Introduction

The rumen is the most important site for digestion and absorption in ruminant animals. To maintain a harmonious symbiosis with these exogenous antigens, the host has to be tolerant of commensals. Tolerance is defined as a state in which the immune system of the host rendered non-reactive toward commensals (van Baarlen et al, 2009). The commensals in the tolerance state contribute to the energy absorption of the host by modulating the expression of host genes that participate in breakdown and absorption of energy substrates/diverse and fundamental physiological functions (Hooper and Gordon, 2001). The gastrointestinal (GI) microbiota has a crucial function in building and maintaining gut tolerance. A dysbiosis of GI microbiota predisposes the host to various kinds of immune and metabolic diseases (Ohland and Jobin, 2015)

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