Methanogenesis associated with altered microbial production of short-chain fatty acids and human-host metabolizable energy

Abstract

Methanogens are methane-producing, hydrogen-oxidizing (i.e. hydrogenotrophic) archaea. Numerous studies have associated methanogens with obesity, but these results have been inconsistent. One link to metabolism may be methanogens' hydrogen-oxidizing ability, thus reducing hydrogen partial pressure and thermodynamically enhancing fermentation of sugars to short-chain fatty acids (SCFAs) that the host can absorb. Because research linking methanogenesis to human metabolism is limited, our goal with this exploratory analysis was to investigate relationships between methanogens and other hydrogenotrophs, along with the association of methanogens with human metabolizable energy (ME). Using results from a randomized crossover feeding study including a western diet and a high-fiber diet, well-characterized human participants, and continuous methane measurements, we analyzed hydrogenotroph abundance and activity, fecal and serum SCFAs, and host ME between high and low methane producers. We detected methanogens in about one-half of participants. We found no evidence that methanogens' consumption of hydrogen to produce methane affected other hydrogenotrophs. High methane producers had greater serum propionate and greater gene and transcript abundance of a key enzyme of the hydrogen-consuming, propionate-producing succinate pathway. High methane producers also had greater ME than low producers on the high-fiber diet. A network analysis revealed positive relationships between the methane-production rate and bacteria capable of degrading fiber and fermenting fiber-degradation products, thus forming a trophic chain to extract additional energy from undigested substrates. Our results show that methanogenesis in a microbial consortium was linked to host ME through enhanced microbial production, and subsequent host absorption, of SCFAs.