Low rumen degradable starch reduces diarrhea and colonic inflammation by influencing the whole gastrointestinal microbiota and metabolite flow in dairy goats

Abstract

Postruminal intestinal inflammation and hindgut acidosis caused by increased dietary starch supply and thereby increased quantities of ruminal degradable starch (RDS) in ruminants have been widely studied. Although the roles of the microbiota in mediating hindgut health that are focused on the hindgut have been widely studied, the absence of whole gastrointestinal insight may influence the depth of research. We integrated the microbiome, metabolome, and host transcriptome changes in the rumen, jejunum, ileum, and colon to investigate the contributions of foregut changes to hindgut gene expression driven by gastrointestinal microbiota and metabolite flow. Forty goats were randomly assigned to receive either a low rumen degradable starch diet (LRDS, RDS=13.85%, n=20) or a high rumen degradable starch diet (HRDS, RDS=20.74%, n=20). Compared with the high RDS (HRDS) group, the low RDS (LRDS) group significantly decreased the diarrheal rate. Based on the mean values of the fecal scores, 6 represented goats of LRDS group (fecal scores=4.58±0.120) and 6 represented goats of HRDS group (fecal scores=3.53±0.343) were selected for sampling and subsequent analysis. LRDS had significantly decreased the colonic pathologic scores. Transcriptomic analysis revealed that LRDS reduced jejunal, ileal, and colonic inflammatory responses. An increase in beneficial commensals and a decreased abundance of pathogenic genera in the small intestine and hindgut were found in goats fed the LRDS diet using 16S rRNA gene sequencing. To identify microbial transmission as well as the transmission of microbial metabolites, 8 genera were identified as core genera according to their calculated niche width. Metabolomics analysis revealed that a total of 554 metabolites were identified among different gastrointestinal sites. Then, metabolites were incorporated into 3 modules: metabolites increased in the current site (ICS), unchanged inflow metabolites in the current site (UICS), and metabolites decreased in the current site (DCS). The results indicated that the UICS metabolites contributed more than 10% to host gene expression in the jejunum, ileum, and colon. When we further focused on the effects of colonic UICS metabolites on the colonic immune-related differentially expressed genes, the results indicated that 1-palmitoylglycerol and deoxycholic acid contributed 60.74% and 11.5% to the colonic immune-related differentially expressed genes, respectively. Our findings provide a preliminary framework of microbial effects that includes the microbiota and their metabolite changes, especially reduced 1-palmitoylglycerol and deoxycholic acid, in the former gastrointestinal tract that could be involved in the alleviation of colonic inflammation in goats fed LRDS diets.