State Key Laboratory of Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Tongji University, Shanghai, 200092, China.
State Key Laboratory of Pollution Control and Resource Reuse, School of Environmental Science and Engineering, Tongji University, Shanghai, 200092, China.
Water Res. 2024 Sep 15;262:122102. doi: 10.1016/j.watres.2024.122102. Epub 2024 Jul 14.
Anaerobic digestion (AD) is a promising technology to realize the conversion from organic matters to methane, which is highly mediated by syntrophic microbial community via mutualistic interactions. However, small energy available in methanogenic conversion usually limits the metabolic activity. To adapt such energy-limited environment, efficient energy conservation is critical to support active physiological functions of anaerobic consortia for methanogenic metabolism. In this study, the contribution of extracellular proton transfer (EPT) enhancement to achieving energy-conserving methanogenesis in AD was explored. Proton-conductive medium (PCM) was applied to construct efficient proton transport pathway, and a large number of protons from extracellular water were found available to upregulate methanogenesis in AD, as indicated by the increase in the content of H (D) in methane molecules (over 40.7%), among which CO-reduction-to-CH was effectively enhanced. The increases of adenosine triphosphate (ATP) concentration (+54.1%) and gene expression activities related to ATPase (+100.0%) and proton pump (+580.1%) revealed that enhanced EPT by PCM promoted transmembrane proton motive force generation to facilitate ATP synthesis. Based on genome-centric metatranscriptomic analyses, MAG14, MAG63 and MAG61 with high energy conservation activity displayed most pronounced positive response to the EPT enhancement. In these core MAGs, the metabolic pathway reconstruction and the key genes activity identification further proved that EPT enhancement-driven efficient ATP synthesis stimulated the cross-feeding of carbon and proton/electron to facilitate microbial mutualism, thereby resulting in the high energy-conserving methanogenesis. Overall, our work provides new insights into how EPT enhancement drives high energy-conserving methanogenesis, expanding our understanding of the ecological role of EPT in AD.
厌氧消化（AD）是一种将有机物转化为甲烷的有前途的技术，该过程高度依赖于通过共生微生物群落的相互作用进行协同转化。然而，产甲烷转化中可用的能量较小，通常会限制代谢活性。为了适应这种能量有限的环境，高效的能量保存对于支持厌氧群落进行产甲烷代谢的活跃生理功能至关重要。在本研究中，探索了通过增强细胞外质子转移（EPT）来实现节能型产甲烷的方法。质子传导介质（PCM）被应用于构建高效的质子传输途径，并且从细胞外水中发现了大量质子可用于增强 AD 中的产甲烷作用，这表现为甲烷分子中 H（D）的含量增加（超过 40.7%），其中 CO 还原为 CH 的作用得到了有效增强。三磷酸腺苷（ATP）浓度的增加（增加 54.1%）以及与 ATP 酶（增加 100.0%）和质子泵（增加 580.1%）相关的基因表达活性的增加表明，PCM 增强的 EPT 促进了跨膜质子动力的产生，从而促进了 ATP 的合成。基于基于基因组的宏转录组分析，具有高能量保存活性的 MAG14、MAG63 和 MAG61 对 EPT 增强表现出最显著的正响应。在这些核心 MAG 中，代谢途径重建和关键基因活性鉴定进一步证明了 EPT 增强驱动的高效 ATP 合成刺激了碳和质子/电子的交叉喂养，从而促进了微生物共生，从而实现了高能量保存的产甲烷作用。总的来说，我们的工作提供了关于 EPT 增强如何驱动高效节能型产甲烷的新见解，扩展了我们对 EPT 在 AD 中的生态作用的理解。
