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A hydrogen dependent geochemical analogue of primordial carbon and energy metabolism

By Martina Preiner, Kensuke Igarashi, Kamila B. Muchowska, Mingquan Yu, Sreejith J. Varma, Karl Kleinermanns, Masaru K. Nobu, Yoichi Kamagata, Harun Tüysüz, Joseph Moran, William F. Martin

Posted 27 Jun 2019
bioRxiv DOI: 10.1101/682955 (published DOI: 10.1038/s41559-020-1125-6)

Hydrogen gas, H2, is generated in alkaline hydrothermal vents from reactions of iron containing minerals with water during a geological process called serpentinization. It has been a source of electrons and energy since there was liquid water on the early Earth, and it fuelled early anaerobic ecosystems in the Earth's crust. H2 is the electron donor for the most ancient route of biological CO2 fixation, the acetyl-CoA (or Wood-Ljungdahl) pathway, which unlike any other autotrophic pathway simultaneously supplies three key requirements for life: reduced carbon in the form of acetyl groups, electrons in the form of reduced ferredoxin, and ion gradients for energy conservation in the form of ATP. The pathway is linear, not cyclic, it releases energy rather than requiring energy input, its enzymes are replete with primordial metal cofactors, it traces to the last universal common ancestor and abiotic, geochemical organic syntheses resembling segments of the pathway occur in hydrothermal vents today. Laboratory simulations of the acetyl-CoA pathway's reactions include the nonenzymatic synthesis of thioesters from CO and methylsulfide, the synthesis of acetate and pyruvate from CO2 using native iron or external electrochemical potentials as the electron source. However, a full abiotic analogue of the acetyl-CoA pathway from H2 and CO2 as it occurs in life has not been reported to date. Here we show that three hydrothermal minerals — awaruite (Ni3Fe), magnetite (Fe3O4) and greigite (Fe3S4) — catalyse the fixation of CO2 with H2 at 100 °C under alkaline aqueous conditions. The product spectrum includes formate (100 mM), acetate (100 μM), pyruvate (10 μM), methanol (100 μM), and methane. With these simple catalysts, the overall exergonic reaction of the acetyl-CoA pathway is facile, shedding light on both the geochemical origin of microbial metabolism and on the nature of abiotic formate and methane synthesis in modern hydrothermal vents.

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