Disruption of ruminal homeostasis by malnutrition involved in systemic ruminal microbiota-host interactions in a pregnant sheep model

Abstract

Background Undernutrition is a prevalent and spontaneous condition in animal production which always affects microbiota-host interaction in gastrointestinal tract. However, how undernutrition affects crosstalk homeostasis is largely unknown. Here, we discover how undernutrition affects microbial profiles and subsequently how microbial metabolism affects the signal transduction and tissue renewal in ruminal epithelium, clarifying the detrimental effect of undernutrition on ruminal homeostasis in a pregnant sheep model. Results Sixteen pregnant ewes (115 days of gestation) were randomly and equally assigned to the control (CON) and severe feed restriction (SFR) groups. Ewes on SFR treatment were restricted to a 30% level of ad libitum feed intake while the controls were fed normally. After 15 days, all ewes were slaughtered to collect ruminal digesta for 16S rRNA gene and metagenomic sequencing and ruminal epithelium for transcriptome sequencing. Results showed that SFR diminished the levels of ruminal volatile fatty acids and microbial proteins and repressed the length, width, and surface area of ruminal papillae. The 16S rRNA gene analysis indicated that SFR altered the relative abundance of ruminal bacterial community, showing decreased bacteria about saccharide degradation (Saccharofermentans and Ruminococcus) and propionate genesis (Succiniclasticum) but increased butyrate producers (Pseudobutyrivibrio and Papillibacter). Metagenome analysis displayed that genes related to amino acid metabolism, acetate genesis, and succinate-pathway propionate production were downregulated upon SFR, while genes involved in butyrate and methane genesis and acrylate-pathway propionate production were upregulated. Transcriptome and real-time PCR analysis of ruminal epithelium showed that downregulated collagen synthesis upon SFR lowered extracellular matrix-receptor interaction, inactivated JAK3-STAT2 signaling pathway, and inhibited DNA replication and cell cycle. Conclusions Generally, undernutrition altered rumen bacterial community and function profile to decrease ruminal energy retention, promoted epithelial glucose and fatty acid catabolism to elevate energy supply, and inhibited the proliferation of ruminal epithelial cells. These findings provide the first insight into the systemic microbiota-host interactions that are involved in disrupting the ruminal homeostasis under a malnutrition pattern.

Growth performance, digestibility, blood metabolites, ruminal fermentation, and bacterial communities in response to the inclusion of gallic acid in the starter feed of preweaning dairy calves

“…The relative abundance of Saccharofermentans was positively related to feed intake, indicating that the increase was possibly caused by substrate sufficiency. The higher abundance of Saccharofermentans, which was possibly caused by increased fermentable substrates, implied the enhanced ability of ruminal saccharide metabolism (Xue et al, 2020). Christensenellaceae R-7 can use saccharides to produce butyrate.…”

Changes in Rumen Microbiota Affect Metabolites, Immune Responses and Antioxidant Enzyme Activities of Sheep under Cold Stimulation

“…Additionally, feed intake also affects the microbiota. For pregnant ewes, restricted feeding can change the bacteria in the rumen, for example, to those involved in the degradation of carbohydrates and the production of short-chain fatty acids (SCFAs) [ 10 ]. Ultimately, the external environmental temperature has an impact on the microbiota.…”

The rumen microbiome of yak co-evolves with its host probably adding the adaptation to its harsh environments

“…Because the yak rumen had a higher propionate molar proportion (Table 1), we compared the relative abundance of bacterial species that either produce or utilize succinate, a fermentation intermediate of propionate production via the succinate pathway [25]. Of the 12 succinate-producing bacterial species, Prevotella brevis, P. bryantii, P. albensis, Fibrobacter succinogenes, Succinimonas amylolytica, and Mitsuokella jalaludinii were enriched (P < 0.05) in the yak rumen compared to the rumen microbiota of cattle or dzo (Fig.…”

“…This in turn reduces the amount of energy wasted via methane production from hydrogen. Two fermentation pathways are mainly responsible for the propionate production in the rumen: the acrylate pathway and succinic acid pathway [25], with the former using lactate as the input substrate and acryloyl-CoA as an intermediate, while the latter using oxaloacetate as the starting substrate and succinate as an intermediate. In this study, the increased relative abundance of succinateproducing and utilizing bacterial species seen in yak might be attributable to the higher propionate proportion detected in that species.…”