Genomic and ecological specialization of Methanobrevibacter species shape human methane emission and overall gut ecosystem function

Abstract Methane is a unique archaeal metabolite that links gut microbial ecology to host physiology. Although intestinal methane production varies by several orders of magnitude between individuals and has been associated with gastrointestinal transit and disease states, the ecological and functional determinants underlying this variation remain poorly understood. Here, we integrate breath methane phenotyping with shotgun metagenomics, metatranscriptomics, comparative genomics, cultivation and stable-isotope tracing in 80 deeply characterized individuals to determine the species-level and functional basis of human gut methanogenesis. Breath methane levels strongly reflected archaeal abundance but could not fully explain methane emission; species-resolved profiling revealed that methane emission represents distinct archaeome states rather than differences in methanogen quantity alone. High methane emitters were dominated by Methanobrevibacter smithii and M. intestini, whereas low emitters harbored a previously uncharacterized Methanobrevibacter lineage (M. sp900766745), for which we propose the name Candidatus Methanobrevibacter hominipaucus sp. nov. Comparative genomics revealed that M. sp900766745 represents a metabolically streamlined lineage lacking several methyl-compound utilization pathways and displaying reduced substrate acquisition capacity. Communities of low-emission individuals exhibited reduced microbial transcriptional activity and accumulated incompletely processed dietary metabolites, indicating lower fermentative turnover and altered hydrogen flux.