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.

Identification of the Potential Role of the Rumen Microbiome in Milk Protein and Fat Synthesis in Dairy Cows Using Metagenomic Sequencing

“…The three most abundant phyla were Bacteroidetes, Firmicutes, and Proteobacteria. Notably, these results are consistent with previous discoveries [ 50 , 51 , 52 ]. Besides, we also found that Neocallimastigomycota is the major anaerobic fungus, which is similar to the report by Zhang et al [ 51 ].…”

“…This difference between the studies could be due to the distinct feeding management and environment of the dairy farm where the samples were collected. Consistent with the previous report by Xue et al [ 52 ], we also found that Prevotella is the most abundant genus in the rumen of lactating cows with high milk protein.…”

Identification of the Potential Role of the Rumen Microbiome in Milk Protein and Fat Synthesis in Dairy Cows Using Metagenomic Sequencing

“…The three most abundant phyla were Bacteroidetes, Firmicutes, and Proteobacteria. Notably, these results are consistent with previous discoveries [ 50 , 51 , 52 ]. Besides, we also found that Neocallimastigomycota is the major anaerobic fungus, which is similar to the report by Zhang et al [ 51 ].…”

“…This difference between the studies could be due to the distinct feeding management and environment of the dairy farm where the samples were collected. Consistent with the previous report by Xue et al [ 52 ], we also found that Prevotella is the most abundant genus in the rumen of lactating cows with high milk protein.…”

Rumen microbes affect the somatic cell counts of dairy cows by modulating glutathione metabolism

“…Some important ruminal cellulolytic species, such as Ruminococcus albicans, Fibrobacterium succinate, and Prevotella , can also secrete pectin-lysing enzymes ( 39 ), which could explain why the TVFAs significantly decreased with decreasing Prevotella abundance in the H-SCC group. Xue et al ( 40 ) demonstrated that the abundance of Prevotella was significantly negatively correlated with the milk fat rate and was related to the biosynthetic functions of branched-chain amino acids, ruminal amino acids, and serum amino acids, providing sufficient precursor materials for the synthesis of immunoglobulins, which was in agreement with our results. Furthermore, it has been reported that the genera, Lactococcus , Fibrobacterium , and Bacteroidetes, can degrade pectin, and their abundance in the rumen is related to the pectin content in the feed ( 41 ).…”

Metagenomic and Metabolomic Insights Into the Mechanism Underlying the Disparity in Milk Yield of Holstein Cows

“…It is important to note that the CBMs (CBM56 and CBM62) were only enriched in the LP group. This is in line with the reports of Xue et al (2020) and Wu et al (2021) who recorded a higher number of genes encoding CBMs in low-producing cows. The CBMs are non-catalytic components within the CAZymes that target polysaccharides having D -galactose or L -arabinopyranose residues ( Drula et al, 2022 ), hence suggesting a higher capacity of the cows with low milk yield in degrading complex polysaccharides.…”

Identification of the Potential Role of the Rumen Microbiome in Milk Protein and Fat Synthesis in Dairy Cows Using Metagenomic Sequencing

“…The three most abundant phyla were Bacteroidetes, Firmicutes, and Proteobacteria. Notably, these results are consistent with previous discoveries [ 50 , 51 , 52 ]. Besides, we also found that Neocallimastigomycota is the major anaerobic fungus, which is similar to the report by Zhang et al [ 51 ].…”

“…This difference between the studies could be due to the distinct feeding management and environment of the dairy farm where the samples were collected. Consistent with the previous report by Xue et al [ 52 ], we also found that Prevotella is the most abundant genus in the rumen of lactating cows with high milk protein.…”

Rumen microbes affect the somatic cell counts of dairy cows by modulating glutathione metabolism

“…Some important ruminal cellulolytic species, such as Ruminococcus albicans, Fibrobacterium succinate, and Prevotella , can also secrete pectin-lysing enzymes ( 39 ), which could explain why the TVFAs significantly decreased with decreasing Prevotella abundance in the H-SCC group. Xue et al ( 40 ) demonstrated that the abundance of Prevotella was significantly negatively correlated with the milk fat rate and was related to the biosynthetic functions of branched-chain amino acids, ruminal amino acids, and serum amino acids, providing sufficient precursor materials for the synthesis of immunoglobulins, which was in agreement with our results. Furthermore, it has been reported that the genera, Lactococcus , Fibrobacterium , and Bacteroidetes, can degrade pectin, and their abundance in the rumen is related to the pectin content in the feed ( 41 ).…”

Metagenomic and Metabolomic Insights Into the Mechanism Underlying the Disparity in Milk Yield of Holstein Cows

“…It is important to note that the CBMs (CBM56 and CBM62) were only enriched in the LP group. This is in line with the reports of Xue et al (2020) and Wu et al (2021) who recorded a higher number of genes encoding CBMs in low-producing cows. The CBMs are non-catalytic components within the CAZymes that target polysaccharides having D -galactose or L -arabinopyranose residues ( Drula et al, 2022 ), hence suggesting a higher capacity of the cows with low milk yield in degrading complex polysaccharides.…”

Identification of the Potential Role of the Rumen Microbiome in Milk Protein and Fat Synthesis in Dairy Cows Using Metagenomic Sequencing

“…The three most abundant phyla were Bacteroidetes, Firmicutes, and Proteobacteria. Notably, these results are consistent with previous discoveries [ 50 , 51 , 52 ]. Besides, we also found that Neocallimastigomycota is the major anaerobic fungus, which is similar to the report by Zhang et al [ 51 ].…”

“…This difference between the studies could be due to the distinct feeding management and environment of the dairy farm where the samples were collected. Consistent with the previous report by Xue et al [ 52 ], we also found that Prevotella is the most abundant genus in the rumen of lactating cows with high milk protein.…”

Rumen microbes affect the somatic cell counts of dairy cows by modulating glutathione metabolism

“…Some important ruminal cellulolytic species, such as Ruminococcus albicans, Fibrobacterium succinate, and Prevotella , can also secrete pectin-lysing enzymes ( 39 ), which could explain why the TVFAs significantly decreased with decreasing Prevotella abundance in the H-SCC group. Xue et al ( 40 ) demonstrated that the abundance of Prevotella was significantly negatively correlated with the milk fat rate and was related to the biosynthetic functions of branched-chain amino acids, ruminal amino acids, and serum amino acids, providing sufficient precursor materials for the synthesis of immunoglobulins, which was in agreement with our results. Furthermore, it has been reported that the genera, Lactococcus , Fibrobacterium , and Bacteroidetes, can degrade pectin, and their abundance in the rumen is related to the pectin content in the feed ( 41 ).…”

Metagenomic and Metabolomic Insights Into the Mechanism Underlying the Disparity in Milk Yield of Holstein Cows

“…It is important to note that the CBMs (CBM56 and CBM62) were only enriched in the LP group. This is in line with the reports of Xue et al (2020) and Wu et al (2021) who recorded a higher number of genes encoding CBMs in low-producing cows. The CBMs are non-catalytic components within the CAZymes that target polysaccharides having D -galactose or L -arabinopyranose residues ( Drula et al, 2022 ), hence suggesting a higher capacity of the cows with low milk yield in degrading complex polysaccharides.…”