Reductive dissolution of pyrite by methanogenic archaea

Abstract

The formation and fate of pyrite (FeS2) modulates global iron, sulfur, carbon, and oxygen biogeochemical cycles and has done so since early in Earth’s geological history. A longstanding paradigm is that FeS2 is stable at low temperature and is unavailable to microorganisms in the absence of oxygen and oxidative weathering. Here, we show that methanogens can catalyze the reductive dissolution of FeS2 at low temperature (≤38 °C) and utilize dissolution products to meet cellular iron and sulfur demands associated with the biosynthesis of simple and complex co-factors. Direct access to FeS2 is required to catalyze its reduction and/or to assimilate iron monosulfide that likely forms through coupled reductive dissolution and precipitation, consistent with close associations observed between cells and FeS2. These findings demonstrate that FeS2 is bioavailable to anaerobic methanogens and can be mobilized in low temperature anoxic environments. Given that methanogens evolved at least 3.46 Gya, these data indicate that the microbial contribution to the iron and sulfur cycles in ancient and contemporary anoxic environments may be more complex and robust than previously recognized, with impacts on the sources and sinks of iron and sulfur and other bio-essential and thiophilic elements such as nickel and cobalt.

Investigating Abiotic and Biotic Mechanisms of Pyrite Reduction

“…Recent studies have shown that methanogens can reductively dissolve FeS 2 ( Payne et al, 2021a , b ). Given that (1) methanogens can produce H 2 during methanogenesis ( Lupa et al, 2008 ; Kulkarni et al, 2018 ) combined with (2) prior studies that have demonstrated abiotic FeS 2 reduction by H 2 , albeit at high temperature (>90°C) and high H 2 partial pressure (>8 bar, equivalent to >7 mM aqueous H 2 ; Truche et al, 2010 ), it was necessary to first evaluate the potential for H 2 to abiotically reduce FeS 2 at lower temperature.…”

“…Recently, pure cultures of methanogenic archaea ( Methanosarcina barkeri strain MS and Methanococcus voltae strain A3) were shown to catalyze the reductive dissolution of FeS 2 when grown with methanol and acetate or with formate, respectively, when incubated at 38°C, with FeS 2 as the sole source of Fe and S for cell growth ( Payne et al, 2021b ). This same study showed that M. voltae required direct contact with FeS 2 to catalyze its reduction and/or to acquire Fe and S dissolution products to meet nutritional demands.…”

“…This same study showed that M. voltae required direct contact with FeS 2 to catalyze its reduction and/or to acquire Fe and S dissolution products to meet nutritional demands. The FeS 2 dissolution product Fe 1– x S has a relatively high solubility of ∼2 μM ( Davison, 1991 ) at the ionic strength and the circumneutral pH of the base salts medium used to cultivate M. voltae in the aforementioned study ( Payne et al, 2021b ). In the presence of a stoichiometric excess of HS – (>2 μM) and at circumneutral pH, the predominant form of Fe(II) in solution from Fe 1– x S dissolution is iron monosulfide aqueous (FeS aq ) clusters ( Luther and Rickard, 2005 ; Rickard and Luther, 2007 ).…”

“…In the presence of a stoichiometric excess of HS – (>2 μM) and at circumneutral pH, the predominant form of Fe(II) in solution from Fe 1– x S dissolution is iron monosulfide aqueous (FeS aq ) clusters ( Luther and Rickard, 2005 ; Rickard and Luther, 2007 ). Given that the measured concentration of HS – significantly exceeded 2 μM (reaching concentrations as high as 35 μM) in the methanogen cultures that were actively shown to be reducing FeS 2 , it was proposed that the cells assimilated soluble FeS aq clusters to meet biosynthetic demands ( Payne et al, 2021b ). These findings are significant since they point to the existence of a biological mechanism that can drive FeS 2 reductive dissolution and mobilization of Fe and S under anoxic and lower temperature (38°C) conditions that, until recently ( Payne et al, 2021b ), were thought to stabilize FeS 2 .…”

“…Given that the measured concentration of HS – significantly exceeded 2 μM (reaching concentrations as high as 35 μM) in the methanogen cultures that were actively shown to be reducing FeS 2 , it was proposed that the cells assimilated soluble FeS aq clusters to meet biosynthetic demands ( Payne et al, 2021b ). These findings are significant since they point to the existence of a biological mechanism that can drive FeS 2 reductive dissolution and mobilization of Fe and S under anoxic and lower temperature (38°C) conditions that, until recently ( Payne et al, 2021b ), were thought to stabilize FeS 2 . Further, this newly discovered process may provide an explanation for how methanogens meet their unusually high demand for Fe ( Ronnow and Gunnarsson, 1981 ; Major et al, 2004 ; Liu et al, 2010 , 2012 ; Johnson et al, 2021 ) in anoxic and sulfidic habitats, conditions that favor formation of FeS aq , Fe 1– x S, and FeS 2 phases ( Luther and Rickard, 2005 ; Rickard and Luther, 2007 ).…”