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

Gastroenteric release of methane from livestock accounts for a substantial portion of anthropogenic greenhouse gas emissions worldwide. In this study, we investigated the rumen microbiome and physiological characteristics associated with methane production in Japanese Black cattle (n = 21). Methane emissions were measured during three fattening phases—early (13 months), middle (20 months), and late (28 months). Using a mixed-effects model to consolidate period-specific measurements, animals were classified into high- and low-methane emitting groups based on residual methane emission (RME). Methane emissions in the high-methane (HME; n = 6) and low-methane (LME; n = 6) groups were 261.6 and 216.5 L/day at T1, 276.9 and 201.7 L/day at T2, and 282.9 and 221.1 L/day at T3, respectively. Overall estimated methane emissions were 273.8 L/day in the HME group and 214.4 L/day in the LME group. Hepatic transcriptome profiles, blood metabolites and hormones, rumen fermentation parameters, and rumen microbiota were subsequently analyzed to identify physiological and microbial features associated with methane emission potential. 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 HME. Functional profiling of rumen microbiota revealed decreased coenzyme M biosynthesis and an increased hydrogen sink from L-glutamate biosynthesis in LME. In the liver, glutamate-derived ornithine and elevated ornithine transcarbamylase gene expression increased ammonia detoxification in LME, whereas the glutamate transporter-encoding gene SLC1A1 was upregulated in HME. These ruminal and physiological changes have potential as biomarkers for monitoring the methanogenic potential of Japanese Black cattle and highlight that the upstream oxoglutarate-to-glutamate biosynthesis pathway is associated with methane production by reducing hydrogen in the rumen.