Fe0-dependent carbon dioxide reduction to methane via diverse electron transfer pathway in methanogenic community

Abstract

Summary: In natural and engineered environments, iron biocorrosion is an energy reservoir for growth of methanogens. However, how archaea accept electrons from metallic iron remains enigmatic. Here, we report that a Methanothrix-dominated methanogenic community from anaerobic granular sludge can reduce carbon dioxide (CO2) to methane (CH4) via electron uptake from zero-valent iron (ZVI). Through the batch experiments, a maximum CH4 yield of 40.8 ± 0.6 μeequiv/day and an electron recovery from ZVI oxidation to CH4 generation of 69.7% ± 6.1% are observed. Metagenome analysis and inhibition experiments indicate that electrons released by corrosive bacteria are utilized by Methanothrix for accomplishing CO2-to-CH4 conversion via potential intracellular and extracellular electron transfer. The results of activity tests of four electron donors (i.e., ZVI, stainless steel, H2, and acetate) suggest that the ZVI-dependent methanogenesis dominate the overall CH4 generation compared with hydrogenotrophic and acetoclastic methanogenesis, which provides a new insight into autotrophic metabolism of methanogens. Science for society: In natural and engineered environments, biocorrosion of iron is a critical energy reservoir for methanogens. With the increasing utilization of Fe0-containing materials in engineering field, Fe0-dependent methanogenesis is becoming a very important agent for CH4 generation. Generally, methanogens can consume H2 abiotically produced from the Fe0 corrosion. The direct electron uptake from Fe0 by methanogens might also be possible. Although the reliance of microbes on Fe0 has been recognized and known since the 19th century, the mechanisms are still widely debated and, in some cases, poorly understood. Hence, a comprehensive study of Fe0-dependent methanogenesis is expected to uncover the processes of metal corrosion, CH4 generation, and global carbon cycling.

Keywords

• biocorrosion
• extracellular electron transfer
• syntrophic methanogenesis
• zero-valent iron