Coupling methanogenesis with iron reduction by acetotrophic Methanosarcina mazei zm-15

Application of ferric iron is conventionally considered to inhibit methanogenesis in anoxic environments. Here we show that Methanosarcina mazei zm-15, a strain isolated from the natural wetland of Tibetan plateau, is capable of Fe(III) reduction, which significantly promotes its growth and methanogenesis. We grew Ms. mazei zm-15 in a medium containing acetate supplemented with Fe(III) in ferric citrate or ferrihydrite and to some cultures anthraquinone-2,6-disulfonate (AQDS) was applied as an electron shuttle. The reduction of Fe(III) species occurred immediately. Ferric citrate was more readily reduced than ferrihydrite. The X-ray diffraction spectra analysis showed the formation of magnetite from ferrihydrite and amorphous reduced products from ferrihydrite plus AQDS. The analysis of protein contents revealed that Fe(III) reduction contributed 36%-46% of the cell growth. The growth yield, estimated as protein increment per acetate consumed for Fe(III) reduction, increased by 20- to 30-fold compared with methanogenesis, which is in consistence with the difference in free energy available by Fe(III) reduction relative to methanogenesis. We propose that the outer-surface multiheme c-type cytochrome predicted from Ms. mazei zm-15 genome serves as the terminal reductase with the energy-converting hydrogenase and F₄₂₀ H₂ dehydrogenase involved in electron transport chain for Fe(III) reduction. The findings shed a light to better understand the ecophysiology of Methanosarcina in anaerobic environments.