Examining Pathways of Iron and Sulfur Acquisition, Trafficking, Deployment, and Storage in Mineral-Grown Methanogen Cells

Payne, Devon; Shepard, Eric M.; Spietz, Rachel L.; Steward, Katherine F.; Brumfield, S. K. Z.; Young, Mark; Bothner, Brian; Broderick, William E.; Broderick, Joan B.; Boyd, Eric S.

doi:10.1128/jb.00146-21

Cited by 16 publications

(42 citation statements)

References 85 publications

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“…This observation is consistent with the detection of Fe 1– x S as the primary product of abiotic FeS 2 reduction, albeit at high temperature [>90°C; ( Truche et al, 2010 )]. These calculations confirm that abiotic reduction of FeS 2 to HS – and Fe 1– x S, but not FeS, by H 2 is thermodynamically feasible under the conditions of prior experiments ( Payne et al, 2021a , b ).…”

Section: Resultssupporting

confidence: 64%

“…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.…”

Section: Resultsmentioning

confidence: 99%

“…Abiotic experiments were conducted using synthetic FeS 2 (2 mM in FeS 2 formula unit) nanoparticles in reactors incubated at 38°C in low salinity, carbonate-buffered medium (2 g L –1 NaHCO 3 ) at pH 7.0, similar to the conditions under which biological FeS 2 reduction has been demonstrated ( Payne et al, 2021a , b ) and for which the thermodynamic parameters above were calculated. In reactors with a 100% H 2 headspace (1.98 × 10 –3 M aqueous H 2 ), rapid abiotic reduction of FeS 2 was observed, as determined by the production of total sulfide (sum of aqueous HS – and gaseous H 2 S) according to Eq.…”

Section: Resultsmentioning

confidence: 99%

“…Based on thermodynamic data ( Luther and Rickard, 2005 ; Rickard and Luther, 2007 ), aqueous solutions with HS – in excess of Fe(II) favors hydrated FeS aq clusters as the predominant form of Fe(II) in solution. Experiments have shown that the methanogen M. voltae , when grown with FeS 2 as the sole source of Fe and S, simultaneously exhibited evidence indicative of Fe limitation [i.e., up-expression of the Fe(II) transporter FeoB and the metal regulator DtxR] but at the same time hyperaccumulated Fe as a thioferrate-like mineral ( Payne et al, 2021a ). To explain this paradox, it was suggested that cells incorrectly sensed Fe(II) limitation during growth due to assimilation of Fe(II) complexed with sulfide (i.e., FeS aq ).…”

Section: Resultsmentioning

confidence: 99%

“…To explain this paradox, it was suggested that cells incorrectly sensed Fe(II) limitation during growth due to assimilation of Fe(II) complexed with sulfide (i.e., FeS aq ). In this model, excess Fe(II) that was assimilated as hydrated FeS aq clusters (cells require more S than Fe) was then sequestered as thioferrate-like nanoparticles to limit toxicity ( Payne et al, 2021a ). FeS aq is predicted to be uncharged at the circumneutral pH of the culture medium used to cultivate M. voltae and M. barkeri ( Jordan et al, 2019a , b ).…”

Section: Resultsmentioning

confidence: 99%

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Investigating Abiotic and Biotic Mechanisms of Pyrite Reduction

et al. 2022

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Pyrite (FeS2) has a very low solubility and therefore has historically been considered a sink for iron (Fe) and sulfur (S) and unavailable to biology in the absence of oxygen and oxidative weathering. Anaerobic methanogens were recently shown to reduce FeS2 and assimilate Fe and S reduction products to meet nutrient demands. However, the mechanism of FeS2 mineral reduction and the forms of Fe and S assimilated by methanogens remained unclear. Thermodynamic calculations described herein indicate that H2 at aqueous concentrations as low as 10–10 M favors the reduction of FeS2, with sulfide (HS–) and pyrrhotite (Fe1–xS) as products; abiotic laboratory experiments confirmed the reduction of FeS2 with dissolved H2 concentrations greater than 1.98 × 10–4 M H2. Growth studies of Methanosarcina barkeri provided with FeS2 as the sole source of Fe and S resulted in H2 production but at concentrations too low to drive abiotic FeS2 reduction, based on abiotic laboratory experimental data. A strain of M. barkeri with deletions in all [NiFe]-hydrogenases maintained the ability to reduce FeS2 during growth, providing further evidence that extracellular electron transport (EET) to FeS2 does not involve H2 or [NiFe]-hydrogenases. Physical contact between cells and FeS2 was required for mineral reduction but was not required to obtain Fe and S from dissolution products. The addition of a synthetic electron shuttle, anthraquinone-2,6-disulfonate, allowed for biological reduction of FeS2 when physical contact between cells and FeS2 was prohibited, indicating that exogenous electron shuttles can mediate FeS2 reduction. Transcriptomics experiments revealed upregulation of several cytoplasmic oxidoreductases during growth of M. barkeri on FeS2, which may indicate involvement in provisioning low potential electrons for EET to FeS2. Collectively, the data presented herein indicate that reduction of insoluble FeS2 by M. barkeri occurred via electron transfer from the cell surface to the mineral surface resulting in the generation of soluble HS– and mineral-associated Fe1–xS. Solubilized Fe(II), but not HS–, from mineral-associated Fe1–xS reacts with aqueous HS– yielding aqueous iron sulfur clusters (FeSaq) that likely serve as the Fe and S source for methanogen growth and activity. FeSaq nucleation and subsequent precipitation on the surface of cells may result in accelerated EET to FeS2, resulting in positive feedback between cell activity and FeS2 reduction.

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Section: Resultssupporting

confidence: 64%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Investigating Abiotic and Biotic Mechanisms of Pyrite Reduction

et al. 2022

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Development of molecular cluster models to probe pyrite surface reactivity

Kour,

Taborosi,

Boyd

et al. 2023

J Comput Chem

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The recent discovery that anaerobic methanogens can reductively dissolve pyrite and utilize dissolution products as a source of iron and sulfur to meet their biosynthetic demands for these elements prompted the development of atomic‐scale nanoparticle models, as maquettes of reactive surface sites, for describing the fundamental redox steps that take place at the mineral surface during reduction. The given report describes our computational approach for modeling n(FeS2) nanoparticles originated from mineral bulk structure. These maquettes contain a comprehensive set of coordinatively unsaturated Fe(II) sites that are connected via a range of persulfide (S22−) ligation. In addition to the specific maquettes with n = 8, 18, and 32 FeS2 units, we established guidelines for obtaining low‐energy structures by considering the pattern of ionic, covalent, and magnetic interactions among the metal and ligand sites. The developed models serve as computational nano‐reactors that can be used to describe the reductive dissolution mechanism of pyrite to better understand the reactive sites on the mineral, where microbial extracellular electron‐transfer reactions can occur.

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