Bechtold Emily K, Ellenbogen Jared B, Xin Danhui, Pacheco Maricia, Toner Brandy M, Chin Yu-Ping, Arnold William A, Bansal Sheel, Wilkins Michael J
Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523, United States.
Department of Civil, Construction, and Environmental Engineering, University of Delaware, Newark, DE 19716, United States.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf196.
Wetlands are a major source of methane emissions and contribute to the observed increase in atmospheric methane over the last 20 years. Methane production in wetlands is the final step of carbon decomposition performed by anaerobic archaea. Although hydrogen/carbon dioxide and acetate are the substrates most often attributed to methanogenesis, other substrates-such as methylated compounds-may additionally play important roles in driving methane production in wetland systems. Here we conducted mesocosm experiments combined with genome-resolved metatranscriptomics to investigate the impact of diverse methanogenic substrate amendment on methanogenesis in two high methane-emitting wetlands with distinct geochemistry, termed P7 and P8. Methanol amendment resulted in high methane production at both sites, whereas acetate and formate amendment only stimulated methanogenesis in P7 mesocosms, where aqueous sulfide concentrations were lower. In P7 sediments, formate amendment fueled acetogenic microbes that produced acetate, which was subsequently utilized by acetoclastic methanogens. In contrast to expression profiles in P7 mesocosms, active methylotrophic methanogen genomes from P8 showed increased expression of genes related to membrane remodeling and DNA damage repair, indicative of stress tolerance mechanisms to counter sulfide toxicity. Methylotrophic methanogenesis generates higher free energy yields than acetoclastic methanogenesis, which likely enables allocation of more energy toward stress responses. These findings contribute to the growing body of literature highlighting methylotrophic methanogenesis as an important methane production pathway in wetlands. By using less competitive substrates like methanol that provide greater energy yields, methylotrophic methanogens may invest in physiological strategies that provide competitive advantages across a range of environmental stresses.
湿地是甲烷排放的主要来源，也是过去20年中观测到的大气甲烷增加的原因之一。湿地中的甲烷生成是厌氧古菌进行碳分解的最后一步。虽然氢气/二氧化碳和乙酸盐是最常被认为与甲烷生成有关的底物，但其他底物，如甲基化化合物，可能在推动湿地系统中的甲烷生成方面也发挥着重要作用。在这里，我们进行了中宇宙实验，并结合基因组解析宏转录组学，以研究不同产甲烷底物添加对两个具有不同地球化学特征、高甲烷排放的湿地（称为P7和P8）中甲烷生成的影响。添加甲醇在两个地点都导致了高甲烷产量，而添加乙酸盐和甲酸盐仅在P7中宇宙中刺激了甲烷生成，那里的水相硫化物浓度较低。在P7沉积物中，添加甲酸盐为产生乙酸盐的产乙酸微生物提供了燃料，随后乙酸盐被乙酸裂解产甲烷菌利用。与P7中宇宙中的表达谱相反，来自P8的活跃甲基营养型产甲烷菌基因组显示与膜重塑和DNA损伤修复相关的基因表达增加，这表明存在应对硫化物毒性的应激耐受机制。甲基营养型甲烷生成比乙酸裂解型甲烷生成产生更高的自由能产量，这可能使更多能量能够分配用于应激反应。这些发现有助于增加的文献强调甲基营养型甲烷生成是湿地中重要的甲烷生成途径。通过使用像甲醇这样竞争较小、能量产量更高的底物，甲基营养型产甲烷菌可能会采用在一系列环境应激中提供竞争优势的生理策略。
