Simulated early Earth geochemistry fuels a hydrogen-dependent primordial metabolism.

Molecular hydrogen is the electron donor for the ancient exergonic reductive acetyl-coenzyme A pathway (acetyl-CoA pathway), which is used by hydrogenotrophic methanogenic archaea. How the presence of iron-sulfides influenced the acetyl-CoA pathway under primordial early Earth geochemistry is still poorly understood. Here we show that the iron-sulfides mackinawite (FeS) and greigite (FeS), which formed in chemical garden experiments simulating geochemical conditions of the early Archaean eon (4.0-3.6 billion years ago), produce abiotic H in sufficient quantities to support hydrogenotrophic growth of the hyperthermophilic methanogen Methanocaldococcus jannaschii. Abiotic H from iron-sulfide formation promoted CO fixation and methanogenesis and induced overexpression of genes encoding the acetyl-CoA pathway. We demonstrate that H from iron-sulfide precipitation under simulated early Earth hydrothermal geochemistry fuels a H-dependent primordial metabolism.