Ruminal microbiome-host crosstalk stimulates the development of the ruminal epithelium in a lamb model

Abstract

Background The development of the rumen is an important physiological challenge for young ruminants. Previous studies have shown that starter feeding can effectively facilitate the growth and development of the rumen in ruminants. However, the mechanism through which starter feeding stimulates the development of the rumen is not clear. Here, we performed an integrated analysis in ruminal microbiota and a host transcriptomic profile in a lamb model with the intervention of starter feed to understand the ruminal microbiome-host crosstalk in stimulating the development of the ruminal epithelium. Results Decreased ruminal pH and increased acetate and butyrate concentrations in the rumen, followed by increasing rumen organ index, were observed in lambs supplemented with starter. Using metagenome sequencing in combination with 16S rRNA and 18S rRNA gene amplicon sequencing, the results showed the abundance of acetate-producing Mitsuokella spp., lactate-producing Sharpea spp., lactate-utilizing Megasphaera spp., and Entodinium spp. was enriched in rumen microbial communities in the starter-feed group. The abundances of genes involved in sugar degradation were decreased in starter-feed lambs, but the GH13 encoding α-amylase was obviously increased. Rumen epithelial transcriptome analysis revealed that seven differentially expressed genes, including MAPK1 , PIK3CB , TNFSF10 , ITGA6 , SNAI2 , SAV1 , and DLG , related to the cell growth module were upregulated, and BAD ’s promotion of cell death was downregulated. Correlation analysis revealed that the increase in the concentrations of acetate and butyrate significantly correlated with the expression of these genes, which indicates acetate and butyrate likely acted as important drivers in the ruminal microbiome-host crosstalk. Conclusions The present study comprehensively describes the symbiotic relationship between the rumen microbiota and the host in lambs after starter feeding. Our data demonstrates that the microbiome-driven generation of acetate and butyrate mediated the growth-related genes’ regulation of the growth-associated signalling pathway in the ruminal epithelium. These co-development networks regulated many physiological processes in the epithelium, including papillae morphology and rumen epithelial growth. Electronic supplementary material The online version of this article (10.1186/s40168-019-0701-y) contains supplementary material, which is available to authorized users.

The Signature Microbiota Driving Rumen Function Shifts in Goat Kids Introduced Solid Diet Regimes

“…The species affiliated with Prevotella (OTU2, OTU3, OTU6 and OTU13) in top 30 increased in solid supplementary regimes. Other studies also reported that the abundances of the genus Prevotella that was predominent in starter-fed lambs positively correlated with acetate, propionate and urea nitrogen concentration (3, 8, 11). This genus is good at utilization of proteins and carbohydrates (either fiber- or non-fiber-carbohydrate) (26).…”

“…For example, the low abundances of OTU87, OTU83, OTU93 and OTU539 were identified as the important predictor for regimes, which indicated that low abundance bacteria may also paly critical roles in function drifts. Therefore, previous literature (3, 10) only focused on the genera with significantly different abundances may not provide the best conclusion. RandomForest regression is useful and robust method for correlation applications because of its ability of automatically producing accuracy estimation and measuring the variable importance.…”

“…The early life diet, especially introduction of solid diet, is an important driver in shaping long-term and adult gut microbiome profiles due to the novel alteration of diet components and macronutrient levels as well as gut anatomical development (1). Goat with rapid physiological changes (non-rumination, transition and rumination) could be proposed as an appropriate animal model for studying the gut microbial ecosystems development by early diet intervention and providing a means for prevention of metabolic diseases (2, 3). Young ruminants receiving only milk or fluid diet (milk replacer) have limited metabolic activity in the rumen epithelium and minimal absorption of volatile fatty acids (VFA) (4).…”

“…Compared with breast milk-fed lambs, the community structure and composition of rumen microbiota of started-fed lambs tends to mature easily and quickly (8). Lin and their colleagues (3) analyzed rumen microbiota in lambs fed starter vs breast-milk. They found that acetate and butyrate increased in starter-feeding lambs, as well as increases of 5 genera including Mitsuokella , Sharpea , Megasphaera , Dialiste , and unclassified Bifidobacteriaceae .…”

Mining Novel Specific Rumen Bacteria to Enhance the Bioactive Function of Mulberry Leaf in Promoting Host Antioxidant Activity and Immunomodulatory

“…Rumen is a main position for the degradation of dietary nutrients in ruminants. The rumen microbiome is emerging as a cross bridge interacted with dietary utilization, host metabolism and phenotype changes, as shown by the association between rumen microbiome and the host metabolism [14][15][16].…”