Exploring the link between ruminal methane production and physiological resilience in Japanese Black cattle during fattening

Background: Gastroenteric release of methane from livestock accounts for a substantial portion of anthropogenic greenhouse gas emissions worldwide. Here, we examined the characteristics of rumen microbiome and physiological resilience associated with methane production, a breed characterized by enhanced intramuscular fat deposition. Results: Methane emissions were measured during three phases: early (13 months), middle (20 months), and late (28 months), and the liver transcriptome, blood metabolites, hormones, rumen fermentation characteristics, and microbiota were analysed. Hydrogen-sinking microbes such as Anaerovorax and Succinivibrio were present at low levels, whereas the prevalence of hydrogen-producing microbes including Christensenellaceae , Clostridium methylpentosum , and Mogibacterium was high in cattle with high methane emissions. Functional profiling of rumen microbiota revealed decreased coenzyme M biosynthesis and an increased hydrogen sink from L-glutamate biosynthesis in low-emission cattle. In the liver, glutamate-derived ornithine and elevated ornithine transcarbamylase gene expression facilitated ammonia detoxification in low-emission cattle, whereas the glutamate transporter-encoding gene SLC1A1 was upregulated in high-emission cattle, thereby enhancing glutathione synthesis and reducing the oxidative stress induced by beta-hydroxybuteric acid. Conclusions: These ruminal and physiological changes reflect the resilience of these cattle to different rumen fermentation conditions, have potential as biomarkers for monitoring the methanogenic potential of Japanese Black cattle, and highlight the upstream oxoglutarate-to-glutamate biosynthesis pathway as a promising target for decreasing methane production by reducing hydrogen in the rumen.