Dirks Blake, Davis Taylor L, Carnero Elvis A, Corbin Karen D, Smith Steven R, Rittmann Bruce E, Krajmalnik-Brown Rosa
Biodesign Center for Health through Microbiomes, Arizona State University, Tempe, AZ 85287, United States.
Biodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, AZ 85287, United States.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf103.
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.
产甲烷菌是一类能够产生甲烷、氧化氢气（即氢营养型）的古菌。众多研究将产甲烷菌与肥胖联系起来，但这些结果并不一致。与新陈代谢的一个关联可能是产甲烷菌的氢气氧化能力，从而降低氢气分压，并在热力学上增强糖发酵为宿主可吸收的短链脂肪酸（SCFAs）的过程。由于将产甲烷作用与人类新陈代谢联系起来的研究有限，我们进行这项探索性分析的目的是研究产甲烷菌与其他氢营养菌之间的关系，以及产甲烷菌与人类可代谢能量（ME）的关联。利用一项随机交叉喂养研究的结果，该研究包括西式饮食和高纤维饮食、特征明确的人类参与者以及连续的甲烷测量，我们分析了高甲烷产生者和低甲烷产生者之间的氢营养菌丰度和活性、粪便和血清中的短链脂肪酸以及宿主的可代谢能量。我们在大约一半的参与者中检测到了产甲烷菌。我们没有发现证据表明产甲烷菌消耗氢气产生甲烷会影响其他氢营养菌。高甲烷产生者血清中的丙酸含量更高，并且在消耗氢气、产生丙酸的琥珀酸途径中一种关键酶的基因和转录本丰度也更高。在高纤维饮食中，高甲烷产生者的可代谢能量也比低甲烷产生者更高。网络分析揭示了甲烷产生速率与能够降解纤维并发酵纤维降解产物的细菌之间存在正相关关系，从而形成了一条营养链，以便从未消化的底物中提取额外的能量。我们的结果表明，微生物群落中的产甲烷作用通过增强微生物产生短链脂肪酸并随后被宿主吸收，与宿主的可代谢能量相关联。
