The gastrointestinal microbiome in dairy cattle is constrained by the deterministic driver of the region and the modified effect of diet

Abstract

Background Dairy cattle (Bos taurus), especially Holstein cows, which are the highest-producing dairy animals and are widely bred to provide milk products to humans, rely critically on their associated gastrointestinal tract (GIT) microbiota to digest plant feed. However, the region-specific taxonomic composition and function of the GIT microbiome in dairy cattle and the mechanistic basis for the diet-induced effects remain to be elucidated. Results We collected 120 digesta samples from 10 GIT regions of 12 Holstein cows fed forage- and grain-based diets and characterized their GIT microbiome via functional shotgun metagenomics and the resolution of metagenome-assembled genomes. Our results demonstrated that the GIT microbiome was mainly partitioned into three distinct clusters, four-chambered stomach, small intestine, and large intestine. Moreover, we found that the four-chambered stomach microbiome with the highest diversity had a strong ability to degrade recalcitrant polysaccharide substrates, underpinned by the prevalence of potential cellulosome-­producing and plant-derived polysaccharide utilization loci-encoding consortia. In contrast, the post-gastric intestinal microbiome orchestrated alternative fermentation pathways to adapt to nutrient availability and energy acquisition. Diet shifts selectively modified the metabolic cascades of the microbiome in specific GIT regions, evidenced by the loss of fiber-degrading taxa and increased hydrogen sinks in propionate after grain introduction. Conclusions Our findings provide new insights into GIT microbial organization and function in dairy cattle by GIT regions and diet regimes, which offers clues for improving animal production and health in the future.

Bacteroidia and Clostridia genomes collectively encode for a progressive cascade of marine polysaccharide degradation along the hindgut of the herbivorous fishKyphosus sydneyanus

“…For example, Alistipes increased in relative abundance in rumen metagenomes of Holstein cows fed on a high-forage (HF) diet, and also displayed higher abundances of glycoside hydrolases (GHs) and carbohydrate binding modules (CBMs) [58]. The predominance of Alistipes within the large intestine of ruminants has also been attributed to the utilization of host glycan, based on high numbers of CAZy families GH109, GH20 and GH92 encoded by these organisms [59]. While the role of Alistipes in various hosts remains under-explored, studies collectively suggest that species within this genus perform differing host-dependent roles related to substrate degradation [54].…”

Spatial heterogeneity of viral communities across the gastrointestinal tracts of ruminants

“…Microbial DNA was extracted from each sample using the repeated beading method as described by Yan et al 55 . The integrity of the DNA was verified using electrophoresis on a 0.8% agarose gel and the DNA concentrations and quality were evaluated using a Nanodrop ND-1000 (Thermo Scientific) 43 .…”

Spatial heterogeneity of viral communities across the gastrointestinal tracts of ruminants

“…3B; Supplementary Data 11: Table S14). The host MAGs have a diverse repertoire of genes involved in polysaccharide degradation, yielding 147 families of glycoside hydrolases (GHs), enabling them to hydrolyze common dietary components like cellulose, hemicellulose, and starch [6,43,44]. For example, many MAGs classi ed to the genera of Kiritimatiellae and Clostridia have numerous GHs, potentially enabling them to adapt to the dietary environment in the GIT regions.…”

“…Microbial DNA was extracted from each sample using the repeated beading method as described by Yan et al [56]. The integrity of the DNA was veri ed using electrophoresis on a 0.8% agarose gel and the DNA concentrations and quality were evaluated using a Nanodrop ND-1000 (Thermo Scienti c) [44].…”