Abstract
The exergonic reaction of FeS with H2S to form FeS2 (pyrite) and H2 was postulated to have operated as an early form of energy metabolism on primordial Earth. Since the Archean, sedimentary pyrite formation has played a major role in the global iron and sulfur cycles, with direct impact on the redox chemistry of the atmosphere. However, the mechanism of sedimentary pyrite formation is still being debated. We present microbial enrichment cultures which grew with FeS, H2S, and CO2 as their sole substrates to produce FeS2 and CH4 Cultures grew over periods of 3 to 8 mo to cell densities of up to 2 to 9 × 106 cells per mL-1 Transformation of FeS with H2S to FeS2 was followed by 57Fe Mössbauer spectroscopy and showed a clear biological temperature profile with maximum activity at 28 °C and decreasing activities toward 4 °C and 60 °C. CH4 was formed concomitantly with FeS2 and exhibited the same temperature dependence. Addition of either penicillin or 2-bromoethanesulfonate inhibited both FeS2 and CH4 production, indicating a coupling of overall 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 methanogen Methanospirillum stamsii, while the bacteria were most closely related to sulfate-reducing Deltaproteobacteria, as well as uncultured Firmicutes and Actinobacteria. Our results show that pyrite formation can be mediated at ambient temperature through a microbially catalyzed redox process, which may serve as a model for a postulated primordial iron-sulfur world.
Highlights
The exergonic reaction of FeS with H2S to form FeS2 and H2 was postulated to have operated as an early form of energy metabolism on primordial Earth
Coupling of pyrite formation to methanogenesis has been proposed by Jørgensen and coworkers [17] to be part of a cryptic sulfur cycle in deep marine sediments where it could support the enigmatic life forms of the deep biosphere. Coupling of this reaction to the synthesis of organic matter is the basis of the “iron−sulfur world” theory proposed by Wächtershäuser, by which pyrite formation is viewed as the central process that led to the transition from Fe–S surface-catalyzed synthesis of organic molecules to actual life on primordial Earth [18,19,20]
We show that lithotrophic microorganisms can mediate the transformation of FeS and H2S to FeS2 at ambient temperature if metabolically coupled to methane-producing archaea
Summary
The exergonic reaction of FeS with H2S to form FeS2 (pyrite) and H2 was postulated to have operated as an early form of energy metabolism on primordial Earth. Burial of pyrite was tightly intertwined with organic matter preservation in reduced sediments [2] These massive reservoirs of reduced sulfur and carbon are counterbalanced by the photosynthetically produced oxygen in Earth’s atmosphere [2]. Coupling of pyrite formation to methanogenesis has been proposed by Jørgensen and coworkers [17] to be part of a cryptic sulfur cycle in deep marine sediments where it could support the enigmatic life forms of the deep biosphere Coupling of this reaction to the synthesis of organic matter is the basis of the “iron−sulfur world” theory proposed by Wächtershäuser, by which pyrite formation is viewed as the central process that led to the transition from Fe–S surface-catalyzed synthesis of organic molecules to actual life on primordial Earth [18,19,20]. Our results provide insights into a metabolic relationship that could sustain part of the deep biosphere and lend support to the iron−sulfur-world theory that postulated FeS transformation to FeS2 as a key energy-delivering reaction for life to emerge
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