Mineral Defects Enhance Bioavailability of Goethite toward Microbial Fe(III) Reduction

Abstract

Surface defects have been shown to facilitate electron transfer between Fe(II) and goethite (α-FeOOH) in abiotic systems. It is unclear, however, whether defects also facilitate microbial goethite reduction in anoxic environments where electron transfer between cells and Fe(III) minerals is the limiting factor. Here, we used stable Fe isotopes to differentiate microbial reduction of goethite synthesized by hydrolysis from reduction of goethite that was further hydrothermally treated to remove surface defects. The goethites were reduced by Geobacter sulfurreducens in the presence of an external electron shuttle, and we used ICP-MS to distinguish Fe(II) produced from the reduction of the two types of goethite. When reduced separately, goethite with more defects has an initial rate of Fe(III) reduction about 2-fold higher than goethite containing fewer defects. However, when reduced together, the initial rate of reduction is 6-fold higher for goethite with more defects. Our results suggest that there is a suppression of the reduction of goethite with fewer defects in favor of the reduction of minerals with more defects. In the environment, minerals are likely to contain defects and our data demonstrates that even small changes at the surface of iron minerals may change their bioavailability and determine which minerals will be reduced.

Iron Speciation and Physiological Analysis Indicate that Synechococcus sp. PCC 7002 Reduces Amorphous and Crystalline Iron Forms in Synthetic Seawater Medium

“…While a high relative PSII/PSI ratio was seen in both cultures, the Synechococcus grown on FeO(OH) had a significantly higher relative PSII/PSI ratio compared to that grown on FeCl 3 (p-value: <0.0001), thus indicating that the stress increased when the available iron was in a more crystalline form. This confirmed the hypothesis that FeO(OH), like other crystalline iron (oxyhydr)oxides, has a lower bioavailability than amorphous iron forms such as FeCl 3 [43]. Cultures grown on both FeCl 3 and FeO(OH) exhibited markedly higher relative PSII/IsiA ratios than the culture grown under iron-replete conditions, which was a clear indication of iron stress in both cultures under low iron concentrations The iron concentration used in this experiment was comparable to naturally occurring iron concentrations in coastal areas [29]; therefore, these results indicate that Synechococcus may experience iron stress under naturally occurring iron concentrations.…”

“…These iron sources were chosen to investigate the difference in response from Synechococcus to an amorphous, more bioavailable form and a crystalline, less bioavailable form of iron, respectively. Hydrolysis species of iron, such as those produced when FeCl 3 is dissolved in water, are considered more available for complexation by EDTA than poorly soluble oxyhydroxides such as FeO(OH) [30,43]. As the growth medium contains EDTA, these hydrolysis species are kept in solution and thus more available for uptake than in the absence of EDTA or other chelator.…”

“…The dFe fraction is considered to be the iron fraction that is most available for biotic uptake and is thus a better measure for initial available iron concentration than TFe. The amorphous FeCl 3 solubilizes better and forms complexes with EDTA more easily than FeO(OH) [30,43], thus explaining the higher initial concentrations of the total dissolved iron in the FeCl 3 control (8.99 ± 2.6 nM)) compared to the FeO(OH) control (3.37 ± 0.2 nM). The fact that there were no significant changes in the total dissolved iron concentration in the abiotic FeO(OH) control between the start and end of the experiment could point to the sampled fraction mostly consisting of FeEDTA, or iron complexed to EDTA, most likely the only truly soluble iron species in the solution.…”

Biological Reduction of Ferrihydrite with Silica Addition: Rates and Controlling Mechanisms

“…82,83 For example, faster electron transfer to freshly prepared versus hydrothermally annealed goethite (α-FeOOH) was attributed to more surface defects in the former; this was observed under abiotic conditions with Fe(II) as the electron donor 83 and under biotic conditions with Geobacter sulfurreducens facilitating electron transfer. 84 Faster electron transfer to a {110} goethite surface containing defects (versus the defect-free analogue) was also demonstrated by molecular modeling. 85 Surface defects were not directly measured in this work.…”

“…One possible reason for faster electron transfer rates in Si-substituted Fh was the presence of surface defects, often indicated by Fe lattice substitution or bond distortion via X-ray adsorption spectroscopy and/or changes in the Neél temperature. , For example, faster electron transfer to freshly prepared versus hydrothermally annealed goethite (α-FeOOH) was attributed to more surface defects in the former; this was observed under abiotic conditions with Fe­(II) as the electron donor and under biotic conditions with Geobacter sulfurreducens facilitating electron transfer . Faster electron transfer to a {110} goethite surface containing defects (versus the defect-free analogue) was also demonstrated by molecular modeling .…”