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

Abstract

Methanogens are CH4-producing, H2-oxidizing (i.e. hydrogenotrophic) archaea. Numerous studies have associated methanogens with obesity, but these results have been inconsistent. One link to host metabolism may be methanogens ability to consume H2, thus reducing H2 partial pressure and thermodynamically enhancing fermentation of sugars to short-chain fatty acids (SCFA) 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, and the association of methanogens with human metabolizable energy (ME). Using results from a randomized crossover feeding study with well-characterized human participants and novel continuous methane measurements, we analyzed hydrogenotroph abundance and activity, fecal and serum SCFAs, and host ME between high and low CH4 producers. Methanogens were detected in about one-half of participants, and most were high CH4 producers. We found no evidence that methanogens consumption of H2 to produce CH4 affected other hydrogenotrophs. High CH4 producers had greater serum propionate and host ME irrespective of diet, as well as greater gene and transcript abundance of a key enzyme of the H2-consuming, propionate-producing succinate pathway. Finally, a network analysis revealed positive relationships between Methanobrevibacter smithii (the most prevalent methanogen in the human colon) 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 methanogens in a microbial consortium were linked to host metabolizable energy through enhanced SCFA production and host SCFA absorption.