Microbiome–host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model

BACKGROUND: Ruminant gastrointestinal tract homeostasis deploys interactive microbiome–host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiological compensatory actor. RESULTS: In this study, 20 sheep were randomly divided into four groups: a hay-fed control (CON) group and a high-grain (HG) diet group for 7, 14, or 28 days. Then, we examined 16S rRNA gene sequences and transcriptome sequences to outline the microbiome–host co-oscillation patterns in remodeling of colonic homeostasis in a sheep model during adaptation to a HG diet. Our data revealed that with durations of an HG diet, the higher starch levels directly affected the colonic lumen environment (lower pH and higher fermentation parameters), which in turn filtered lumen-specific functional taxonomic groups (HG-sensitive and HG-tolerant taxa). The colonic epithelium then gave rise to a new niche that triggered endoplasmic reticulum stress to activate unfolded protein response, if the duration of endoplasmic reticulum stress was overlong, this process would regulate cell apoptosis (Caspase-3, Caspase-8, and TNFRSF21) to achieve a functional transformation. CONCLUSIONS: Our results provide a holistic view of the colonic microbial assemblages and epithelium functional profile co-oscillation patterns in remodeling of colonic homeostasis during adaptation to an HG diet in a sheep model. These findings also provide a proof of concept that the microbe–host collaboration is vital for maintaining hindgut homeostasis to adapt to dietary dichotomies.