Dissecting the black box of microbially mediated pyrite formation from FeS and H2S

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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 played a major role in the global iron and sulfur cycles, with direct impact on the redox state of the atmosphere. However, the mechanism of sedimentary pyrite formation and the way microorganisms contribute to this process is still being debated. This year, we published work on the first enrichment culture, which is capable to grow with FeS, H2S, and CO2 as sole substrates to produce FeS2 and CH4 (Thiel et al., 2019, PNAS). This proposal aims to elucidate the mechanism behind microbially mediated pyrite formation coupled to methanogenesis. Two hypotheses will be tested to unravel whether pyrite formation in enrichment J5 is directly involved in energy conservation or not. Hypothesis I (H-I) will address the question whether microorganisms involved in pyrite formation could potentially utilize the Wächtershäuser reaction, i.e. the direct formation of FeS2 and H2 from FeS and H2S for energy conservation. This would necessitate long-distance electron transport from the cell surface into the cytoplasmic membrane or cytoplasm, e.g. involving multiheme cytochrome c complexes. Hypothesis II (H-II) will test whether the energy metabolism of the non-methanogenic partner is restricted to a reversal of sulfur respiration (sulfide conversion to zero-valent sulfur and H2), with subsequent pyrite formation being mediated by the (possibly abiotic) reaction of the formed zero-valent sulfur with FeS. The two hypotheses will be tested in three complementary work packages (WP). In WP1, high quality draft genomes of enrichment J5 members will be obtained by metagenomics and annotated in respect to their potential energy metabolism including hallmark proteins indicative of H-I or H-II. Subsequent metatranscriptomics will follow expression of genes encoding such hallmark proteins. In WP2, individual community members in enrichment J5 will be identified by fluorescent in situ hybridization in combination with single-cell RAMAN microspectroscopy. The latter will serve the identification of RAMAN signals indicative of overexpressed multiheme cytochrome c redox complexes (H-I) or the formation of zero-valent sulfur within or associated with microbial cells (H-II). In WP3, enrichment J5 will be exposed to alternative growth conditions, which are postulated to require similar enzyme complexes as laid out in H-I and H-II. This will include the oxidation of elemental Fe under sulfate-reducing conditions (H-I) and the oxidation of hydrogen with elemental sulfur to H2S (H-II). Upon positive growth, expressed genes will be followed by metatranscriptomics. The proposed project will be important to establish enrichment J5 as a model for microbial pyrite formation, which has impact for our understanding of biogeochemical sulfur and iron cycling and origin-of-life-hypotheses.