The mechanisms of iron isotope fractionation produced during dissimilatory Fe(III) reduction by Shewanella putrefaciens and Geobacter sulfurreducens

Abstract

Microbial dissimilatory iron reduction (DIR) is widespread in anaerobic sediments and is a key producer of aqueous Fe(II) in suboxic sediments that contain reactive ferric oxides. Previous studies have shown that DIR produces some of the largest natural fractionations of stable Fe isotopes, although the mechanism of this isotopic fractionation is not yet well understood. Here we compare Fe isotope fractionations produced by similar cultures of Geobacter sulfurreducens strain PCA and Shewanella putrefaciens strain CN32 during reduction of hematite and goethite. Both species produce aqueous Fe(II) that is depleted in the heavy Fe isotopes, as expressed by a decrease in 56 Fe/54 Fe ratios or δ 56 Fe values. The low δ 56 Fe values for aqueous Fe(II) produced by DIR reflect isotopic exchange among three Fe inventories: aqueous Fe(II) (Fe(II)aq), sorbed Fe(II) (Fe(II)sorb), and a reactive Fe(III) component on the ferric oxide surface (Fe(III)reac). The fractionation in 56 Fe/54 Fe ratios between Fe(II)aq and Fe(III)reac was –2.95‰, and this remained constant over the timescales of the experiments (280 d). The Fe(II)aq – Fe(III)reac fractionation was independent of the ferric Fe substrate (hematite or goethite) and bacterial species, indicating a common mechanism for Fe isotope fractionation during DIR. Moreover, the Fe(II)aq – Fe(III)reac fractionation in 56 Fe/54 Fe ratios during DIR is identical within error of the equilibrium Fe(II)aq – ferric oxide fractionation in abiological systems at room temperatures. This suggests that the role of bacteria in producing Fe isotope fractionations during DIR lies in catalyzing coupled atom and electron exchange between Fe(II)aq and Fe(III)reac so that equilibrium Fe isotope partitioning occurs. Although Fe isotope fractionation between Fe(II)aq and Fe(III)reac remained constant, the absolute δ 56 Fe values for Fe(II)aq varied as a function of the relative proportions of Fe(II)aq, Fe(II)sorb, and Fe(III)reac during reduction. The temporal variations in these proportions were unique to hematite or goethite but independent of bacterial species. In the case of hematite reduction, the small measured Fe(II)aq – Fe(II)sorb fractionation of −0.30‰ in 56 Fe/54 Fe ratios, combined with the small proportion of Fe(II)sorb, produced insignificant (<0.05‰) isotopic effects due to sorption of Fe(II). Sorption of Fe(II) produced small, but significant effects during reduction of goethite, reflecting the higher proportion of Fe(II)sorb and larger measured Fe(II)aq – Fe(II)sorb fractionation of –0.87‰ in 56 Fe/54 Fe ratios for goethite. The isotopic effects of sorption on the δ 56 Fe values for Fe(II)aq were largest during the initial stages of reduction when Fe(II)sorb was the major ferrous Fe species during goethite reduction, on the order of 0.3 to 0.4‰. With continued reduction, however, the isotopic effects of sorption decreased to <0.2‰. These results provide insight into the mechanisms that produce Fe isotope fractionation during DIR, and form the basis for interpretation of Fe isotope variations in modern and ancient natural systems where DIR may have driven Fe cycling.