Hyperthermophilic iron reducers are common in hydrothermal chimneys found along the Endeavour Segment in the northeastern Pacific Ocean based on culture-dependent estimates. However, information on the availability of Fe(III) (oxyhydr) oxides within these chimneys, the types of Fe(III) (oxyhydr) oxides utilized by the organisms, rates and environmental constraints of hyperthermophilic iron reduction, and mineral end products is needed to determine their biogeochemical significance and are addressed in this study. Thin-section petrography on the interior of a hydrothermal chimney from the Dante edifice at Endeavour showed a thin coat of Fe(III) (oxyhydr) oxide associated with amorphous silica on the exposed outer surfaces of pyrrhotite, sphalerite, and chalcopyrite in pore spaces, along with anhydrite precipitation in the pores that is indicative of seawater ingress. The iron sulfide minerals were likely oxidized to Fe(III) (oxyhydr) oxide with increasing pH and Eh due to cooling and seawater exposure, providing reactants for bioreduction. Culture-dependent estimates of hyperthermophilic iron reducer abundances in this sample were 1740 and 10 cells per gram (dry weight) of material from the outer surface and the marcasite-sphalerite-rich interior, respectively. Two hyperthermophilic iron reducers, Hyperthermus sp. Ro04 and Pyrodictium sp. Su06, were isolated from other active hydrothermal chimneys on the Endeavour Segment. Strain Ro04 is a neutrophilic (pHopt 7–8) heterotroph, while strain Su06 is a mildly acidophilic (pHopt 5), hydrogenotrophic autotroph, both with optimal growth temperatures of 90–92 °C. Mössbauer spectroscopy of the iron oxides before and after growth demonstrated that both organisms form nanophase (<12 nm) magnetite [Fe3O4] from laboratory-synthesized ferrihydrite [Fe10O14(OH)2] with no detectable mineral intermediates. They produced up to 40 mm Fe2+ in a growth-dependent manner, while all abiotic and biotic controls produced <3 mm Fe2+. Hyperthermophilic iron reducers may have a growth advantage over other hyperthermophiles in hydrothermal systems that are mildly acidic where mineral weathering at increased temperatures occurs.
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