Multi-omics reveals that the rumen microbiome and its metabolome together with the host metabolome contribute to individualized dairy cow performance

Abstract

Background: Recently, we reported that some dairy cows could produce high amounts of milk with high amounts of protein (defined as milk protein yield [MPY]) when a population was raised under the same nutritional and management condition, a potential new trait that can be used to increase high-quality milk production. It is unknown to what extent the rumen microbiome and its metabolites, as well as the host metabolism, contribute to MPY. Here, analysis of rumen metagenomics and metabolomics, together with serum metabolomics was performed to identify potential regulatory mechanisms of MPY at both the rumen microbiome and host levels. Results: Metagenomics analysis revealed that several Prevotella species were significantly more abundant in the rumen of high-MPY cows, contributing to improved functions related to branched-chain amino acid biosynthesis. In addition, the rumen microbiome of high-MPY cows had lower relative abundances of organisms with methanogen and methanogenesis functions, suggesting that these cows may produce less methane. Metabolomics analysis revealed that the relative concentrations of rumen microbial metabolites (mainly amino acids, carboxylic acids, and fatty acids) and the absolute concentrations of volatile fatty acids were higher in the high-MPY cows. By associating the rumen microbiome with the rumen metabolome, we found that specific microbial taxa (mainly Prevotella species) were positively correlated with ruminal microbial metabolites, including the amino acids and carbohydrates involved in glutathione, phenylalanine, starch, sucrose, and galactose metabolism. To detect the interactions between the rumen microbiome and host metabolism, we associated the rumen microbiome with the host serum metabolome and found that Prevotella species may affect the host's metabolism of amino acids (including glycine, serine, threonine, alanine, aspartate, glutamate, cysteine, and methionine). Further analysis using the linear mixed effect model estimated contributions to the variation in MPY based on different omics and revealed that the rumen microbial composition, functions, and metabolites, and the serum metabolites contributed 17.81, 21.56, 29.76, and 26.78%, respectively, to the host MPY.

A Combined Metabolomic and Metagenomic Approach to Discriminate Raw Milk for the Production of Hard Cheese

“…Overall, due to the important role of metabolism across all biological processes, metabolomics-based studies have been increasingly used to understand the physiological processes associated with economically important traits in the dairy industry, such as milk production in dairy cattle (as affected by the feeding systems) and cheese manufacturing [ 2 , 3 , 4 ]. Additionally, several metabolomic research efforts have been mainly devoted to a better understanding of the impact of diet on rumen health in dairy cows [ 5 , 6 ].…”

Ruminal Degradation of Rumen-Protected Glucose Influences the Ruminal Microbiota and Metabolites in Early-Lactation Dairy Cows

“…Therefore, the role of the rumen microbiome in host health goes far beyond the local role of the rumen. Previous studies have revealed the interaction between the diversity or unique niche of functional categories and metabolic factors that control microbial metabolism and related nutrient formation pathways ( 12 , 13 ). Accumulating evidence indicated that rumen metabolic disorders related to changes in the rumen microbiota composition are important risk factors for disease development ( 14 , 15 ).…”

The Role of Innate Immune Response and Microbiome in Resilience of Dairy Cattle to Disease: The Mastitis Model

“…Recent studies using an omics-based structure have suggested that differences in rumen microbiota are associated with cattle production and health traits, such as feed efficiency [ 130 , 131 ], methane (CH 4 ) yield [ 132 ], milk composition [ 133 ], and ruminal acidosis [ 134 ]. Manipulating rumen microbiota may improve cattle productivity and health and reduce CH 4 emissions.…”