Department of Marine Sciences, University of Georgia, Athens, Georgia, USA
Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA.
mBio. 2021 May 11;12(3):e03620-20. doi: 10.1128/mBio.03620-20.
About 382 Tg yr of methane rising through the seafloor is oxidized anaerobically (W. S. Reeburgh, Chem Rev 107:486-513, 2007, https://doi.org/10.1021/cr050362v), preventing it from reaching the atmosphere, where it acts as a strong greenhouse gas. Microbial consortia composed of anaerobic methanotrophic archaea and sulfate-reducing bacteria couple the oxidation of methane to the reduction of sulfate under anaerobic conditions via a syntrophic process. Recent experimental studies and modeling efforts indicate that direct interspecies electron transfer (DIET) is involved in this syntrophy. Here, we explore a fluorescent hybridization-nanoscale secondary ion mass spectrometry data set of large, segregated anaerobic oxidation of methane (AOM) consortia that reveal a decline in metabolic activity away from the archaeal-bacterial interface and use a process-based model to identify the physiological controls on rates of AOM. Simulations reproducing the observational data reveal that ohmic resistance and activation loss are the two main factors causing the declining metabolic activity, where activation loss dominated at a distance of <8 μm. These voltage losses limit the maximum spatial distance between syntrophic partners with model simulations, indicating that sulfate-reducing bacterial cells can remain metabolically active up to ∼30 μm away from the archaeal-bacterial interface. Model simulations further predict that a hybrid metabolism that combines DIET with a small contribution of diffusive exchange of electron donors can offer energetic advantages for syntrophic consortia. Anaerobic oxidation of methane is a globally important, microbially mediated process reducing the emission of methane, a potent greenhouse gas. In this study, we investigate the mechanism of how a microbial consortium consisting of archaea and bacteria carries out this process and how these organisms interact with each other through the sharing of electrons. We present a process-based model validated by novel experimental measurements of the metabolic activity of individual, phylogenetically identified cells in very large (>20-μm-diameter) microbial aggregates. Model simulations indicate that extracellular electron transfer between archaeal and bacterial cells within a consortium is limited by potential losses and suggest that a flexible use of electron donors can provide energetic advantages for syntrophic consortia.
大约有 382 太克/年的甲烷通过海底释放到大气中，这会导致温室效应。但其中有一部分会被微生物在无氧条件下氧化，从而避免甲烷进入大气。这些微生物是由厌氧甲烷氧化菌和硫酸盐还原菌组成的共生体，它们通过一种共生关系将甲烷的氧化与硫酸盐的还原结合起来。最近的实验研究和建模工作表明，直接种间电子转移（DIET）参与了这种共生关系。在这里，我们探索了一个关于大型厌氧甲烷氧化（AOM）共生体的荧光杂交-纳米二次离子质谱数据集，该数据集揭示了代谢活性从古菌-细菌界面向外的下降，并使用基于过程的模型来确定 AOM 速率的生理控制因素。模拟再现观测数据的结果表明，欧姆电阻和激活损失是导致代谢活性下降的两个主要因素，其中激活损失在距离<8μm 的地方占主导地位。这些电压损失限制了共生体之间的最大空间距离，模型模拟表明，硫酸盐还原菌细胞在距离古菌-细菌界面约 30μm 的范围内仍能保持代谢活性。模型模拟还进一步预测，一种混合代谢，即结合 DIET 和电子供体的小部分扩散交换，可以为共生体提供能量优势。厌氧甲烷氧化是一种全球重要的微生物介导过程，可减少甲烷这种强效温室气体的排放。在这项研究中，我们研究了由古菌和细菌组成的微生物共生体如何进行这一过程，以及这些生物体如何通过电子的共享相互作用。我们提出了一个基于过程的模型，该模型通过对非常大（>20μm 直径）微生物聚集体中单个、系统发育鉴定细胞的代谢活性的新的实验测量进行验证。模型模拟表明，共生体中细菌和古菌细胞之间的细胞外电子转移受到潜在损失的限制，并表明灵活使用电子供体可以为共生体提供能量优势。
