Abstract
The rumen barriers, constituted by the microbial, physical and immune barrier, prevent the transmission of pathogens and toxins to the host tissue in the maintenance of host-microbe homeostasis. Ruminal short-chain fatty acids (SCFAs), which are the important signaling molecules derived from the rumen microbiota, regulate a variety of physiological functions of the rumen. So far, how the ruminal SCFAs regulate the function of rumen barriers is unclear. By the combined methods of transcriptome sequencing, 16S rRNA gene sequencing, and metagenome shotgun sequencing, we have investigated the regulatory effects of ruminal SCFAs on the functions of rumen barriers, by determining the composition and functions of epimural microbiota and on the structure and immunity of the rumen epithelium in goats receiving a 10% (LC group), 35% (MC group), or 65% concentrate diet (HC group). We found that, when the dietary concentrate shifted from 10 to 35%, the increase of total SCFA is associated with the diversification of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus increase mostly. Meantime, the signals on pathways concerning the mechanical connections and growth homeostasis in the rumen epithelium were upregulated. Under these conditions, the responses of immune components in the rumen epithelium decrease. However, when the dietary concentrate shifted from 35 to 65%, the increase of acetate and reduction of pH decrease the diversity of epimural microbiota and the diversity of its gene pool. Within the microbial community, the relative abundance of genera Sphingobium, Acinetobacter, and Streptococcus significantly decrease. Concomitantly, the signals on pathways concerning the cell growth and tight junction disruption were upregulated, while the signals on pathways concerning paracellular permeability were downregulated. Under these conditions, the signals on the pathways relating to the immune components increase. Our data thus indicates that diet-SCFA axis maintains the host-microbe homeostasis via promoting the diversification of epimural microbiota and maintaining the integrity of rumen epithelium in healthy animals, while via enhancing the activities of immune barrier in animal with lower rumen pH.
Highlights
The rumen is the most important site for digestion in ruminant animals
If it is applied to the rumen epimural microbiota, the acid environment induced the decrease on energy-extraction ability of the epimural microbiota might be part of the reason for the sharp decline of the microbial diversity in the HC group, in comparison with that of MC group
The 16S rRNA sequencing data, metagenomic data and correspondence analysis (CCA) results all indicated the importance of genera Sphingobium, Acinetobacter, and Streptococcus in the short-chain fatty acids (SCFAs)-microbe-host axis
Summary
The rumen is the most important site for digestion in ruminant animals. On the one hand, it provides the space and nutrients for microbes to live within the rumen. The central strategy utilized by them to maintain such homeostatic relationships is to construct barriers and, to protect the ecological niche of the commensals, limit the colonization of pathogens, and clearance the invaded microbes in the intestinal epithelium (Belkaid and Hand, 2014). The integrity of physical barrier is fundamental to the animal health and productivity since it prevents the translocation of toxins and pathogens from the rumen into the blood; (3) the immune barrier, which is composed of the intestinal-associated immune cells and their secretion of cytokines. SCFAs have been reported to influence the function of the physical barrier, such as the integrity of rumen epithelium, renewal of epithelial cells and the expression of tight junction proteins (Gui and Shen, 2016; Greco et al, 2018). The study of the global effects of ruminal SCFAs on the function of rumen barriers is valuable in order to obtain a comprehensive view of the interactions between ruminal SCFAs and rumen barriers and, will provide potential regulation methods for animal health and growth
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