Precipitation of greigite and pyrite induced by Thermococcales: an advantage to live in Fe‐ and S‐rich environments?

Abstract

Summary Thermococcales, a major order of archaea inhabiting the iron‐ and sulfur‐rich anaerobic parts of hydrothermal deep‐sea vents, have been shown to rapidly produce abundant quantities of pyrite FeS2 in iron–sulfur‐rich fluids at 85°C, suggesting that they may contribute to the formation of ‘low temperature’ FeS2 in their ecosystem. We show that this process operates in Thermococcus kodakarensis only when zero‐valent sulfur is directly available as intracellular sulfur vesicles. Whether in the presence or absence of zero‐valent sulfur, significant amounts of Fe3S4 greigite nanocrystals are formed extracellularly. We also show that mineralization of iron sulfides induces massive cell mortality but that concomitantly with the formation of greigite and/or pyrite, a new generation of cells can grow. This phenomenon is observed for Fe concentrations of 5 mM but not higher suggesting that above a threshold in the iron pulse all cells are lysed. We hypothesize that iron sulfides precipitation on former cell materials might induce the release of nutrients in the mineralization medium further used by a fraction of surviving non‐mineralized cells allowing production of new alive cells. This suggests that biologically induced mineralization of iron‐sulfides could be part of a survival strategy employed by Thermococcales to cope with mineralizing high‐temperature hydrothermal environments.

Production of carbon-containing pyrite spherules induced by hyperthermophilic Thermococcales: a biosignature?

“…Upon addition of ferrous sulfate (FeSO 4 ) in the medium, abundant black precipitates were immediately generated both in abiotic controls (S(0)+Na 2 S+FeSO 4 ) and in experiments conducted in the presence of cells ( Figure 1 ). In presence of T. kodakarensis , the deep dark aspect of the precipitates faded after 192 h of mineralization ( Figure 1 ), consistently with the observations reported in Gorlas et al (2022) . The abiotic controls retained their initial appearance over the entire duration of the experiments, no fading of the deep dark aspect of the precipitates occurred ( Supplementary Figure 1 ).…”

“…The formation of a black precipitate immediately after the addition in the medium of iron as Fe 2+ ( Figure 1 ) is caused by the precipitation of amorphous or poorly crystalline nanophases such as FeS nano-mackinawite [unambiguously detected by Rietveld refinement ( Table 2 ) and XANES ( Figure 2 and Table 1 )] and iron phosphates ( Figure 4B ; Gorlas et al, 2018 , 2022 ), the two phases forming a three-dimensional matrix observed by electron microscopy. A similar amorphous matrix is observed in the abiotic control [S(0) + Na 2 S + FeSO 4 ] at 96 h ( Supplementary Figure 3 ), identified as FeS nano-mackinawite by Rietveld refinement ( Table 2 ).…”

“…While the precipitation of pyrite increases with increasing duration of mineralization ( Figures 6A–C ), the initial production of greigite, a sulfide containing 2 Fe(III) for 1 Fe(II), seems to be intimately related to that of Fe (II/III) phosphates in the present system: the proportion of greigite first decreases while barbosalite-like phosphates precipitate, before it increases once barbosalite-like are no longer present ( Figures 6A, D ). A number of studies have reported the microbial production of greigite either intracellularly (by magnetotactic bacteria for instance) or extracellularly (e.g., Mann et al, 1990 ; Bertel et al, 2012 ; Gorlas et al, 2018 , 2022 ; Picard et al, 2018 , 2019 ). Some authors proposed that the production of greigite requires a precursor already containing some Fe (III) ( Etique et al, 2018 ; Picard et al, 2018 ; Berg et al, 2020 ; Duverger et al, 2020 ; Gorlas et al, 2022 ).…”

Sulfidogenesis at low pH and its application for treatment of metalliferous wastewaters

“…An increased importance of the polysulfide pathway over the sulfide pathway for pyrite formation in the presence of microorganisms was supported by the observation that S 8 0 was required for pyrite formation in incubations with the thermophilic S 8 0 -reducing species Thermococcus kodakarensis (Gorlas et al, 2022). Although that study suggested a key role for intracellular S 8 0 vesicles produced by the T. kodakarensis cells (Gorlas et al, 2022), additional abiotic controls with higher amounts of Na 2 S, more closely mimicking the conditions created by actively S 8 0 -reducing microorganisms, were not performed.…”

“…(2 mM total sulfide) (Gorlas et al, 2022), which can be expected to have precipitated immediately as FeS, making H 2 S unavailable for subsequent pyrite formation. Abiotic controls with excess of H 2 S, would have helped to assess whether the S 8 0 vesicles indeed have a so far undefined beneficial property to induce pyrite formation, or whether pyrite formation in the microbial cultures is enabled by the higher H 2 S concentrations, regardless of the form of S 8 0 in the medium (bulk or biologically produced vesicles).…”