Age-related shifts of dissolved hydrogen and its impact on rumen fermentation dynamics and microbial communities in goats (Capra hircus)

Abstract

Abstract The rumen is a complex anaerobic fermentation ecosystem in which microbial communities undergo dynamic changes during host development, influencing fermentation efficiency, hydrogen utilization, and methane (CH₄) production. However, how rumen maturation reshapes hydrogen redistribution and the associated microbial interactions remains poorly understood. This study compared rumen fermentation characteristics, microbial communities (bacteria, archaea, fungi, and protozoa), and Gibbs free energy profiles between 0.5-year-old and 2-year-old goats to elucidate age-related changes in hydrogen metabolism. Adult goats exhibited significantly higher concentrations of dissolved methane (dCH₄), dissolved hydrogen (dH₂), and total short-chain fatty acids (SCFAs), including acetate, propionate, and butyrate, than young goats ( P < 0.05). Thermodynamic analyses indicated that glucose fermentation and methanogenesis were energetically feasible under rumen conditions (ΔG < 0), while age-related differences in Gibbs free energy (ΔG) suggested altered hydrogen partitioning during rumen maturation. The mature rumen was characterized by enrichment of carbohydrate-fermenting microorganisms, particularly Segatella , Anaeroplasma , and the anaerobic fungus Cyllamyces , which were positively associated with glucose conversion pathways, metabolic hydrogen, and SCFA production. In contrast, younger goats showed enrichment of amino acid metabolism pathways together with microbial taxa associated with early rumen development, including Christensenellaceae_R-7_group and Caecomyces . The archaeal community also shifted with age, with significantly higher abundances of Methanosphaera and Methanosarcina in adult goats, consistent with enhanced hydrogen utilization through methanogenic pathways. Functional predictions further revealed enrichment of carbohydrate and energy metabolism in adult goats, whereas amino acid metabolism predominated in young goats. These findings demonstrate that rumen maturation is accompanied by coordinated changes in microbial community structure, metabolic hydrogen redistribution, and thermodynamic characteristics, resulting in a transition from amino acid-oriented metabolism in young goats to a more specialized carbohydrate-fermenting ecosystem in adults. This integrated analysis identifies key microbial groups involved in hydrogen turnover and may provide new insights into the microbial mechanisms underlying rumen maturation, offering potential targets for improving feed efficiency and mitigating methane emissions in ruminants.