Iron Sulfides Produced by Thermococcales: An Iron Detoxification Mechanism

Thermococcales, sulfur-reducing archaea inhabiting the hottest parts of hydrothermal vents, have evolved to thrive in environments rich in iron and sulfide species. In this study, using experimental analogues of sulfur-rich hydrothermal chimneys, we confirm previous suggestions that the precipitation of iron sulfide minerals promoted by Thermococcales contributes to a population-wide adaptation to reactive species induced by the presence of high levels of iron. In parallel with mineral phases identification, cellular metabolic activity was monitored during mineralization, revealing a mechanism in which a subpopulation of cells does not survive mineralization and becomes encrusted in pyrite, while the remaining living cells exhibit a gene expression profile focused on DNA repair and metal excess associated detoxification. Compared to abiotic conditions, Thermococcales induce a faster precipitation of dissolved iron, immobilising excess metal. Our results clarify the role of mineralizing cells in this survival mechanism, suggesting that this biomineralization process allows resilience to extreme chemical stress. Upon drastic levels of toxic dissolved iron, thanks to a population of mineralizing cells, the surviving Thermococcales are thus more likely to endure those still harsh environments. This complex mechanism is likely a key factor in the adaptation of microorganisms to the hottest environments of hydrothermal vents.