Linkages between Epithelial Microbiota and Host Transcriptome in the Ileum during High-Grain Challenges: Implications for Gut Homeostasis in Goats

A high-grain (HG) diet can result in ruminal subacute acidosis, which is detrimental to gut health and can lead to decreased productivity. This study investigated the ileal epithelial microbiota and its relationship with host epithelial function in goats fed a HG diet (concentrate/hay, 90:10) and a control diet (concentrate/hay, 55:45), aiming to elucidate the mechanisms involved in ileal adaptation to subacute acidosis. The HG challenge increased the ileal volatile fatty acid concentration (p = 0.030) and altered the ileal epithelial microbiota by increasing (FDR < 0.05) relative abundances of active carbohydrate and protein degraders Synergistetes, Prevotella, Fibrobacter, Clostridium, Treponema, and unclassified Ruminococcaceae by 20.1-, 6.3-, 16.8-, 8.5-, 19.9-, and 7.1-fold, respectively. However, the HG diet tended to reduce (FDR < 0.10) the relative abundance of Candidatus Arthromitus (38.8 ± 36.1 versus 2.1 ± 3.1). Microbial functional potentials inferred using PICRUSt indicated that the HG challenge elevated abundances of pathways associated with metabolism of amino acid, glycan, cofactors, and vitamins, whereras it decreased pathways associated with signal transduction, xenobiotic biodegradation, and metabolism. Additionally, in the ileal epithelium of HG goats, transcriptome analysis identified the increment (FDR < 0.10) of candidate genes involved in metabolism of carbohydrates, lipids, proteins, vitamins, and the proinflammatory cytokine pathway, while downregulating genes encoding antimicrobials and complements (FDR < 0.05). Collectively, the HG challenge shifted the structure and functional potentials of the ileal microbial community and affected the host responses in the ileum of goats toward increased metabolic activities of macro- and micronutrients, together with an increased risk of gut inflammation.