Elsevier

Chemical Geology

Volume 212, Issues 3–4, 1 December 2004, Pages 255-268
Chemical Geology

Microbial reduction of iron(III) oxyhydroxides: effects of mineral solubility and availability

https://doi.org/10.1016/j.chemgeo.2004.08.015Get rights and content

Abstract

The rate of Fe(III) reductive dissolution by ascorbate has been shown by [Larsen, O. and Postma, D., 2001. Kinetics of reductive bulk dissolution of lepidocrocite, ferrihydrite and goethite. Geochim. Cosmochim. Acta, 65: 1367–1379.] to decrease in the order ferrihydrite>lepidocrocite>goethite>hematite. The abiotic rate of reductive dissolution thus correlates with the solubility of the iron oxyhydroxides. We investigated whether this also holds for the microbial reduction kinetics of Fe(III) iron oxyhydroxides. The solubilities of nanoparticulate hematite, lepidocrocite, ferrihydrite and amorphous Fe(III) oxyhydroxide were obtained from pe–pH titrations of oxyhydroxide/Fe2+(aq) suspensions, in pH range 4 to 7. The solubility of low surface area (LSA) hematite was estimated from redox potential measurements at pH 2. The same solid phases and soluble Fe(III)-citrate were then reduced by the iron reducing bacterium Shewanella putrefaciens using lactate as the electron donor. In all cases, the microbial Fe(III) reduction rates exhibited saturation behavior with respect to the initial Fe(III) concentration. The maximum specific rate of reduction (vmax, in μmol cell−1 h−1) correlated positively with the solubility of the Fe(III) oxyhydroxides, with the highest values of vmax for ferrihydrite and amorphous Fe(III) oxide, the lowest for LSA hematite. Hence, the solubility appears to be a rate-controlling parameter in both the abiotic and enzymatic reduction of Fe(III) oxyhydroxides.

Introduction

Iron oxyhydroxides are ubiquitous reactive constituents of soils, sediments and aquifers. They exhibit large surface areas, which bind trace metals, nutrients and organic molecules. Under suboxic conditions, Fe(III) solids are reductively dissolved via a number of alternative abiotic and microbial pathways (Lovley, 1987, Roden and Wetzel, 2002, Van Cappellen and Wang, 1996). In particular, they serve as terminal electron acceptors for the oxidation of organic matter by iron reducing bacteria. In addition to being an important oxidation pathway of organic matter degradation and generating soluble ferrous iron, microbial iron reduction can have a major impact on the persistence and mobility of metals, phosphate, radionuclides and organic contaminants (Anderson and Lovley, 1999, Roden and Edmonds, 1997). The metabolic activity of iron reducing bacteria may further enhance the natural or engineered bioremediation of contaminated sites (Lovley, 1995, McCormick et al., 2002).

The rate and extent of microbial reduction of Fe(III) oxyhydroxides are influenced by a variety of factors, including the microbial community structure and biomass, the type and abundance of Fe(III) oxyhydroxides, and the sorption affinity between the oxide phases and bacteria (Caccavo et al., 1992). In addition, the Fe(III) reduction rate may be inhibited by adsorption, on the Fe(III) solid (Roden et al., 2000) or cell surface (Urrutia et al., 1998), of Fe2+ formed as by-product of microbial Fe(III) reduction. While many of the rate-determining factors have been identified, in most cases mathematical relationships expressing their effects on the kinetics of microbial Fe(III) reduction are lacking.

Rates of microbial processes typically exhibit saturation behavior with respect to external substrates. That is, with increasing concentration of a given substrate, the rate levels off at a maximum value. The so-called Michaelis–Menten (or Monod) rate expression forms the basis for representing microbial reaction pathways in biogeochemical reactive transports models (McNab and Narasimhan, 1994, Van Cappellen et al., 1993). Whether the Michaelis–Menten expression describes the dependence of dissimilatory Fe(III) reduction kinetics on the availability of Fe(III) oxyhydroxides has not been experimentally demonstrated, however.

The kinetics of abiotic reductive dissolution of Fe(III) iron oxyhydroxides by organic reductants have been extensively studied (Kuma et al., 1993, Larsen and Postma, 2001, Postma, 1993). In particular, Larsen and Postma (2001) have shown that the Fe(III) reduction rate by ascorbate, normalized to the mineral surface area, decreases in the order ferrihydrite 2-lines>ferrihydrite 6-lines>lepidocrocite>goethite>hematite. The observed reaction rate order sequence is suggestive of a linear free energy relationship between the solubility of an iron oxyhydroxyde and its rate of reductive dissolution by ascorbate.

In this paper, we investigate the dependence of the rate of dissimilatory Fe(III) reduction on the concentration of various Fe(III) oxyhydroxides, as well as on the bacterial density. The goal is to determine if the reduction rate follows the Michaelis–Menten expression with respect to the Fe(III) substrate concentration. The results obtained with the solid Fe(III) phases are compared to the microbial reduction kinetics of dissolved Fe(III)-citrate. We further investigate the relationship between the microbial reduction kinetics and the solubility of the Fe(III) oxyhydroxides. The microbial Fe(III) reduction experiments are performed using the facultative anaerobic Gram-negative bacterium Shewanella putrefaciens as model iron reducing bacterium, and lactate as electron donor.

Section snippets

Fe(III) oxyhydroxides

Hematite nanoparticles were prepared by adding 100 mL of a 0.1 M Fe(NO3)3 solution to 1 L of boiled and vigorously stirred water, and allowing the suspension to cool down at room temperature, according to the method described by Schwertmann and Cornell (1991). Nanoparticles of 6-lines ferrihydrite were synthesized by dissolving 20 g of Fe(NO3)3 in 2 L of demineralized water at 75 °C under rapid stirring (Schwertmann and Cornell, 1991). The solution was maintained at 75 °C for 10 min and then

Fe(III) oxyhydroxide solubilities

Duplicate titrations for each oxyhydroxide, except LSA hematite, yielded 7 to 11 individual (pe*, pH) points (Fig. 1), which were fitted by linear least square regression. The slopes of the pe* versus pH trends were close, but not equal, to the theoretical value of −3 (Eq. (4)); the values varied from −2.65 for lepidocrocite to −2.85 for nanohematite. Comparison of dissolved and total Fe2+ concentrations indicated that up to 25% of the Fe2+ was adsorbed by the mineral surfaces, with the highest

Fe(III) oxyhydroxide solubilities

Solubility products of Fe(III) oxyhydroxides reported in the literature often vary over several orders of magnitude (Table 1). Differences in solubility of a given Fe(III) oxyhydroxide may arise from variations in specific surface area, crystallinity and impurity content. They may also reflect difficulties associated with the experimental determination of Fe(III) oxyhydroxide solubilities. Because one of the objectives of this study is to determine the relationship between microbial Fe(III)

Conclusions

The Michaelis–Menten expression for enzyme-catalyzed reactions describes the dependence of the rates of dissimilatory reduction by S. putrefaciens of five Fe(III) oxyhydroxides and soluble Fe(III)-citrate on the Fe(III) substrate concentration. For the mineral phases, the maximum reduction rate per cell, vmax, is positively correlated with the effective solubility product of the oxyhydroxide, *Kso=aFe3+aH+n, which accounts for deviations from the end-member mineral compositions via the

Acknowledgements

This study is part of TRIAS project 835.80.004, co-funded by the Centre for Soil Quality Management and Knowledge Transfer (SKB), Delft Cluster (DC) and the Council for the Earth and Life Sciences (ALW) of the Netherlands Organisation for Scientific Research (NWO). The authors thank Dr. D. Perret and Dr. J. Haas for their constructive reviews. [LW]

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