Australian Centre for Water and Environmental Biotechnology, Faculty of Engineering, Architecture and Information Technology, The University of Queensland, St. Lucia, Queensland 4072, Australia.
Australian Centre for Water and Environmental Biotechnology, Faculty of Engineering, Architecture and Information Technology, The University of Queensland, St. Lucia, Queensland 4072, Australia.
Sci Total Environ. 2024 Feb 20;912:169576. doi: 10.1016/j.scitotenv.2023.169576. Epub 2023 Dec 23.
Anaerobic methanotrophic archaea (ANME) belonging to the family Methanoperedenaceae are crucial for the global carbon cycle and different biogeochemical processes, owing to their metabolic versatility to couple anaerobic oxidation of methane (AOM) with different electron acceptors. A universal feature of Methanoperedenaceae is the abundant genes encoded in their genomes associated with extracellular electron transfer (EET) pathways. Candidatus. 'Methanoperedens manganicus', an archaeon belonging to the family Methanoperedenaceae, was recently enriched in a bioreactor performing AOM coupled with Mn (IV) reduction. Using this EET-capable ANME, we tested the hypothesis in this study that ANME can catalyse the humic-dependent AOM for growth. A two-year incubation showed that AOM activity can be sustained by Ca. 'M. manganicus' consortium in a bioreactor fed only with humic acids and methane. An isotopic mass balance batch test confirmed that the observed AOM was coupled to the reduction of humic acids. The increase of relative abundance of Ca. 'M. manganicus', and the total archaea population in the microbial community suggested that Ca. 'M. manganicus' can grow on methane and humic acids. The observation of humic-dependent AOM led to a subsequent hypothesis that humic acids could be used as the electron shuttle to mediate the EET in dissimilatory Mn (IV) reduction by Ca. 'M. manganicus'. We tested this hypothesis by adding humic acids to a Ca. 'M. manganicus' dominated-culture, which showed that the AOM rate was doubled by the addition of humic acids. X-ray photoelectron spectroscopy (XPS) showed that quinone moieties were consumed when humic acids worked as electron acceptors while remaining stable when functioning as a shuttle for electron transfer. The results of our study suggest that humic acids may serve as electron shuttles to allow ANME to access more electron acceptors through long-range EET.
属于甲烷鬃菌科的厌氧甲烷营养古菌 (ANME) 对全球碳循环和不同的生物地球化学过程至关重要，这是由于它们代谢的多功能性，能够将甲烷的厌氧氧化 (AOM) 与不同的电子受体相耦合。甲烷鬃菌科的一个普遍特征是其基因组中大量编码与细胞外电子转移 (EET) 途径相关的基因。最近，一种属于甲烷鬃菌科的古菌，被命名为“Methanoperedens manganicus”，在一个进行 AOM 与 Mn(IV) 还原偶联的生物反应器中被富集。利用这种具有 EET 能力的 ANME，我们在本研究中测试了一个假设，即 ANME 可以催化依赖腐殖质的 AOM 以实现生长。为期两年的培养表明，在仅以腐殖酸和甲烷为底物的生物反应器中，Ca. 'M. manganicus' 共生物种可以维持 AOM 活性。一个同位素质量平衡批量测试证实，观察到的 AOM 与腐殖质的还原偶联。微生物群落中 Ca. 'M. manganicus' 的相对丰度增加和总古菌种群的增加表明，Ca. 'M. manganicus' 可以在甲烷和腐殖酸上生长。依赖腐殖质的 AOM 的观察导致了随后的一个假设，即腐殖酸可以作为电子穿梭体，通过 Ca. 'M. manganicus' 介导异化 Mn(IV) 还原中的 EET。我们通过向 Ca. 'M. manganicus' 主导的培养物中添加腐殖酸来测试这一假设，结果表明添加腐殖酸可使 AOM 速率提高一倍。X 射线光电子能谱 (XPS) 表明，当腐殖酸作为电子受体时，醌部分被消耗，而当腐殖酸作为电子转移的穿梭时则保持稳定。我们的研究结果表明，腐殖酸可能作为电子穿梭体，使 ANME 通过长程 EET 来获取更多的电子受体。
