Environmental Microbiology Laboratory, Environmental Engineering Institute, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne, Lausanne, 1015, Switzerland.
Department of Biological Sciences, University of Calgary, Calgary, AB, T2N 1N4, Canada.
ISME J. 2022 Jun;16(6):1583-1593. doi: 10.1038/s41396-022-01207-w. Epub 2022 Feb 16.
Microbial life is widespread in the terrestrial subsurface and present down to several kilometers depth, but the energy sources that fuel metabolism in deep oligotrophic and anoxic environments remain unclear. In the deep crystalline bedrock of the Fennoscandian Shield at Olkiluoto, Finland, opposing gradients of abiotic methane and ancient seawater-derived sulfate create a terrestrial sulfate-methane transition zone (SMTZ). We used chemical and isotopic data coupled to genome-resolved metaproteogenomics to demonstrate active life and, for the first time, provide direct evidence of active anaerobic oxidation of methane (AOM) in a deep terrestrial bedrock. Proteins from Methanoperedens (formerly ANME-2d) are readily identifiable despite the low abundance (≤1%) of this genus and confirm the occurrence of AOM. This finding is supported by C-depleted dissolved inorganic carbon. Proteins from Desulfocapsaceae and Desulfurivibrionaceae, in addition to S-enriched sulfate, suggest that these organisms use inorganic sulfur compounds as both electron donor and acceptor. Zerovalent sulfur in the groundwater may derive from abiotic rock interactions, or from a non-obligate syntrophy with Methanoperedens, potentially linking methane and sulfur cycles in Olkiluoto groundwater. Finally, putative episymbionts from the candidate phyla radiation (CPR) and DPANN archaea represented a significant diversity in the groundwater (26/84 genomes) with roles in sulfur and carbon cycling. Our results highlight AOM and sulfur disproportionation as active metabolisms and show that methane and sulfur fuel microbial activity in the deep terrestrial subsurface.
微生物生命广泛存在于陆地地下深处，可达到数千米的深度，但在深层贫营养和缺氧环境中驱动代谢的能源仍不清楚。在芬兰奥卢基洛托的芬诺斯堪的亚盾状杂岩的深部结晶基底中，非生物甲烷和古老海水来源的硫酸盐的逆向梯度创造了一个陆地硫酸盐-甲烷过渡带（SMTZ）。我们使用化学和同位素数据以及基因组解析的宏蛋白质组学，证明了生命的活跃性，并首次提供了在深层陆地基岩中进行活跃的厌氧甲烷氧化（AOM）的直接证据。尽管该属的丰度较低（≤1％），但仍可以轻易识别出 Methanoperedens（以前称为 ANME-2d）的蛋白质，并证实了 AOM 的发生。这一发现得到了 C 耗尽的溶解无机碳的支持。来自脱硫球菌科和脱硫弧菌科的蛋白质以及富含 S 的硫酸盐表明，这些生物体将无机硫化合物同时用作电子供体和受体。地下水中的零价硫可能源自非生物岩石相互作用，或者与 Methanoperedens 之间的非专性共生关系，这可能将奥卢基洛托地下水的甲烷和硫循环联系起来。最后，候选门辐射（CPR）和 DPANN 古菌的假定共生菌在地下水中具有显著的多样性（84 个基因组中有 26 个），在硫和碳循环中具有作用。我们的研究结果强调了 AOM 和硫歧化作用是活跃的代谢途径，并表明甲烷和硫为深层陆地地下的微生物活动提供了燃料。
