The impact of rumen and hindgut microbiomes on the persistent productivity of long-lived dairy cows.

BACKGROUND

In high-producing dairy systems, the average productive lifespan of cows is around 2.5-4 years. Persistent productivity and longevity are key determinants of dairy cow production performance and herd profitability. Although gastrointestinal microbiota influences dairy cow productivity, the mechanisms by which host-microbiome interactions support sustained productivity in long-lived dairy cows remain unclear. Therefore, this study integrated the metagenomics and metabolomics of the rumen and rectum, along with serum and milk metabolomics, to elucidate the potential impact of the rumen and rectum microbiota on the productivity of long-lived dairy cows.

RESULTS

Serum alanine aminotransferase (ALT), alkaline phosphatase (ALP), total cholesterol (TC), and high-density and low-density lipoprotein cholesterol (HDL-C and LDL-C) levels in long-lived dairy cows were positively correlated with milk yield (MY) and elevated in long-lived high-yielding (LH) dairy cows, whereas insulin (INS) and glucagon (GCG) were negatively correlated with MY and higher in long-lived low-yielding (LL) dairy cows. Rumen propionate level was elevated in LH group and positively correlated with MY. The rumen microbiome, in LH cows upregulated pathways involved in amino acid, cofactor, and vitamin metabolism. LH cows' rumen and rectum microbial networks had cohesion and vulnerability levels similar to those of LL cows and exhibited dependence on key nodes. The rumen and rectum MY-associated purine metabolites, guanosine and D-ribose-1-phosphate, mediated 65.56% and 67.55% of the significant positive effects of Acidaminococcaceae bacterium and Parabacteroides sp. on MY, respectively. Furthermore, the specific lipid metabolism-associated rumen microbiota module enhanced serum eicosapentaenoic acid (EPA) levels by modulating rumen α-linolenic acid metabolism, thereby promoting the synthesis of Pe(20:5/0:0) in milk, which positively contributed to MY.

CONCLUSIONS

This study revealed the potential contributions of the rumen and rectum microbiota to the productivity of long-lived dairy cows via purine metabolites, as well as the potential role of the rumen microbial network module in influencing productivity through α-linolenic acid metabolism, providing new insights for nutritional management strategies aimed at improving the persistent production capacity of dairy cows. Video Abstract.