Rumen microbiota modulates metabolic stress in high-yield dairy cows: insights from early to peak lactation

Early lactation (EL) in high-yield dairy cows represents a critical lactation phase marked by significant metabolic stress, which often provokes health disorders and production losses. The rumen microbiome is instrumental in regulating host health and metabolism. However, its contribution to metabolic stress experienced by EL cows has been largely unexplored.

Metabolic stress was prominently observed during EL in the form of elevated oxidative stress (OS), inflammation, and lipolysis. This stress gradually decreased with the progression of lactation from day in milk (DIM) 21 to 90. To identify the underlying mechanisms, this study analyzed EL cows (DIM 32) and peak lactation (PL, DIM 72) using an integrative approach including rumen metagenomics, rumen metabolomics, host metabolomics, and their interactions. Metagenomic analysis revealed a higher abundance of methanogenic archaea (Methanobrevibacter and Methanosphaera) in EL cows, driving increased methane production and subsequent energy loss. This energy waste likely worsened the negative energy balance and caused excessive lipolysis in EL cows. In contrast, the rumen microbiota of PL cows was enriched with Prevotella species and anti-inflammatory bacterial genera (Bacteroides, Parabacteroides, and Alistipes), which are associated with the alleviation of host metabolic stress. Functional analysis of the rumen microbiota uncovered increased tryptophan biosynthesis in EL cows, driving kynurenine production. Conversely, PL cows exhibited a greater abundance of enzymes involved in tryptophan metabolism, thus facilitating the production of indole-3-acetic acid (IAA). Metabolomics analysis also identified the tryptophan metabolism pathway as a shared link between the rumen and serum. Specifically, the kynurenine pathway, associated with OS and inflammation, was upregulated in EL cows, while the indole pathway, particularly the production of IAA, was markedly elevated in PL cows, which attenuated OS and inflammation.

The study results indicate that the rumen microbiota is pivotal in mitigating metabolic stress in EL cows by modulating tryptophan metabolism. Specifically, the transition from EL to PL was characterized by an enhanced tryptophan-indole pathway and a suppressed tryptophan-kynurenine pathway. The results offer meaningful insights into the microbial mechanisms underlying metabolic stress and identify potential strategies for improving cow health and productivity during lactation. Video Abstract.