Pyrite formation from FeS and H2S is mediated by a novel type of microbial energy metabolism
AbstractThe exergonic reaction of FeS with H2S to form FeS2(pyrite) and H2was postulated to have operated as an early form of energy metabolism on primordial Earth. Since the Archean, sedimentary pyrite formation played a major role in the global iron and sulfur cycles, with direct impact on the redox chemistry of the atmosphere. To date, pyrite formation was considered a purely geochemical reaction. Here, we present microbial enrichment cultures, which grew with FeS, H2S, and CO2as their sole substrates to produce FeS2and CH4. Cultures grew over periods of three to eight months to cell densities of up to 2–9×106cells mL−1. Transformation of FeS with H2S to FeS2was followed by57Fe Mössbauer spectroscopy and showed a clear biological temperature profile with maximum activity at 28°C and decreasing activities towards 4°C and 60°C. CH4was formed concomitantly with FeS2and exhibited the same temperature dependence. Addition of either penicillin or 2-bromoethanesulfonate inhibited both FeS2and CH4production, indicating a syntrophic coupling of pyrite formation to methanogenesis. This hypothesis was supported by a 16S rRNA gene-based phylogenetic analysis, which identified at least one archaeal and five bacterial species. The archaeon was closely related to the hydrogenotrophic methanogenMethanospirillum stamsiiwhile the bacteria were most closely related to sulfate-reducingDeltaproteobacteria, as well as unculturedFirmicutesandActinobacteria. We identified a novel type of microbial metabolism able to conserve energy from FeS transformation to FeS2, which may serve as a model for a postulated primordial iron-sulfur world.Significance statementPyrite is the most abundant iron-sulfur mineral in sediments. Over geological times, its burial controlled oxygen levels in the atmosphere and sulfate concentrations in seawater. Its formation in sediments is so far considered a purely geochemical process that is at most indirectly supported by microbial activity. We show that lithotrophic microorganisms can directly transform FeS and H2S to FeS2and use this exergonic reaction as a novel form of energy metabolism that is syntrophically coupled to methanogenesis. Our results provide insights into a syntrophic relationship that could sustain part of the deep biosphere and lend support to the iron-sulfur-world theory that postulated FeS transformation to FeS2as a key energy-delivering reaction for life to emerge.