Elsevier

Chemical Geology

Volume 283, Issues 3–4, 22 April 2011, Pages 242-250
Chemical Geology

Microbial reduction of chlorite and uranium followed by air oxidation

https://doi.org/10.1016/j.chemgeo.2011.01.021Get rights and content

Abstract

To evaluate the stability of biogenic nanoparticulate U(IV) in the presence of an Fe(II)-rich iron-bearing phyllosilicate, we examined the reduction of structural Fe(III) in chlorite CCa-2 and uranium(VI) by Shewanella oneidensis MR-1, and the reoxidation of these minerals (after pasteurization) via the introduction of oxygen. Bioreduction experiments were conducted with combinations of chlorite, U(VI), and anthraquinone-2,6-disulfonate (AQDS). Abiotic experiments were conducted to quantify the reduction of U(VI) by chemically-reduced chlorite-associated Fe(II), the oxidation of nanoparticulate U(IV) by unaltered structural Fe(III) in chlorite, and the sorption of U(VI) to chlorite, to elucidate interactions between U(VI)/U(IV) and Fe(II)/Fe(III)-chlorite. Solids were characterized by X-ray diffraction, scanning electron microscopy, and X-ray absorption spectroscopy to confirm Fe and U reduction and reoxidation. U(VI) enhanced the reduction of structural Fe(III) in chlorite and nanoparticulate U(IV) was oxidized by structural Fe(III) in chlorite, demonstrating that U served as an effective electron shuttle from S. oneidensis MR-1 to chlorite-Fe(III). Abiotic reduction of U(VI) by chlorite-associated Fe(II) was very slow compared to biological U(VI) reduction. The rate of nanoparticulate U(IV) oxidation by dissolved oxygen increased in the presence of chlorite-associated Fe(II), but the extent of U(IV) oxidation decreased as compared to no-chlorite controls. In identical experiments conducted with bioreduced suspensions of nanoparticulate U(IV) and nontronite (another iron-bearing phyllosilicate), the rate of U(IV) oxidation by dissolved oxygen increased in the presence of nontronite-associated Fe(II). In summary, we found that structural Fe(III) in chlorite delayed the onset of U(VI) loss from solution, while chlorite-associated Fe(II) enhanced the oxidation rate of U(IV) by dissolved oxygen, indicating that chlorite-associated Fe(II) could not protect nanoparticulate U(IV) from oxygen intrusion but instead increased the oxidation rate of U(IV).

Research highlights

► Chlorite-Fe(III) delayed U(VI) reduction, while chlorite-Fe(II) enhanced U(IV) oxidation. ► U(VI) reduced chlorite-Fe(III) while U(IV) oxidized chlorite-Fe(II). ► Chlorite-Fe(II) could not protect U(IV) from oxygen intrusion. ► Abiotic reduction of U(VI) by chlorite-Fe(II) was slow compared to U(VI) bioreduction. ► U(IV) oxidation by dissolved oxygen also increased in the presence of nontronite-Fe(II).

Introduction

Uranium contamination of sediment and groundwater is a problem at many U.S. Department of Energy (DOE) sites and uranium ore-processing sites where soluble U(VI) has migrated into groundwater. In aerobic groundwater, U(VI) carbonate complexes are often the predominant uranium species. These anionic or neutral U species tend to sorb weakly to solid phases and, therefore, can be relatively mobile in the environment (Akcay, 1998, Arnold et al., 1998). Under anoxic conditions U(VI) can be reduced to sparingly soluble U(IV) minerals and precipitated from groundwater (Lovley and Phillips, 1992). Bacterially mediated reduction of U(VI) to uraninite may be exploited for in situ remediation of uranium-contaminated sites (Lovley et al., 1991, Fredrickson et al., 2000, Brooks et al., 2003).

The stimulation of indigenous dissimilatory metal-reducing bacteria (DMRB) for uranium remediation is an area of active research at several DOE field sites. Assessment of the efficacy of any one strategy (e.g., ethanol addition) is typically based on changes in aqueous geochemistry measured in monitoring wells. Interpretation of these results is often challenging due to the complex suite of redox reactions potentially operative in these subsurface environments. For example, while the addition of an electron donor will promote reducing conditions, the availability of multiple electron acceptors (e.g., nitrate, Mn(III/IV) oxides, Fe(III) oxides, or sulfate) may enhance or impede U(VI) reduction. In a related manner, the concentration and flux of electron donor addition can also impact U(VI) reduction and U(IV) reoxidation (Tokunaga et al., 2008).

While considerable research has been conducted on uranium interactions with iron (oxyhydr)oxides (e.g., Jeon et al., 2005, Ginder-Vogel et al., 2006), much less research has focused on uranium interactions with iron-bearing clay minerals (Stucki et al., 2007). Iron-bearing clay minerals are widely distributed in soils and sediments (Stucki et al., 2007) and often account for about half of the Fe mass in soils and sediments (Favre et al., 2006). Specifically, at the Old Rifle and Oak Ridge DOE field sites, the mass of iron associated with clay minerals is higher than the mass of iron associated with oxide minerals (Stucki et al., 2007, Komlos et al., 2008). In addition, chlorite is a common clay mineral at the DOE Hanford site (Schmeide et al., 2000, Baik et al., 2004, McKinley et al., 2007).

Compared to iron oxides which dissolve during reduction, the majority of reduced Fe(II) in iron-bearing clays is retained in the clay structure (Kostka et al., 1999, Dong et al., 2009). Fe(II) sorbed to mineral surfaces may be a more facile reductant compared to structural Fe(II) in clay minerals (Hofstetter et al., 2003, Hofstetter et al., 2006), however, structural Fe(II) will not be flushed from a biostimulated reduction zone by advection. Thus, structural Fe(II) in clay minerals may be an important long-term reactant in maintaining anoxic conditions. The stability of U(IV) is, ultimately, the key criterion for determining success of any reductive immobilization strategy. The intrusion of oxidants such as oxygen or nitrate may be countered by a large reservoir of solid-phase reductants such as Fe(II)-bearing clay minerals.

In a recent, related study we measured the concomitant bioreduction of structural Fe(III) in the clay mineral nontronite and U(VI) by Shewanella oneidensis MR-1 (Zhang et al., 2009). From those experiments we found that uranium served as an effective electron shuttle to enhance the reduction of structural Fe(III) in nontronite but that delayed the onset of U(VI) loss from solution. In this current study, we not only report on the bioreduction of structural Fe(III) in the clay mineral chlorite CCa-2 and U(VI) but also measure the stability of bioreduced U(IV) in the presence of chlorite-associated Fe(II) and nontronite-associated Fe(II) upon oxygen intrusion. These two iron-bearing phyllosilicates were selected because they represent mineralogical end-members with respect to Fe(III) and Fe(II) content. Nontronite NAu-2 contains 4.2 mmol Fe/g with the majority of the structural iron as Fe(III) (Jaisi et al., 2007), while chlorite CCa-2 contains 3.4 mmol Fe/g with the majority of the structural iron as Fe(II). The objectives of this research were to study the interactions between U(VI) and the iron-rich ripidolite chlorite CCa-2 during their concomitant biological reduction, and then to further investigate the stability of bioreduced U(IV) and chlorite-associated Fe(II) in the presence of dissolved oxygen.

Section snippets

Cell cultivation

S. oneidensis MR-1 was cultured in a chemically defined minimal medium as described previously (Burgos et al., 2008). Cells were harvested by centrifugation (15 min and 20 °C at 3,500 g), washed three times with anoxic 30 mM NaHCO3 (pH 6.8, prepared under an 80:20% N2:CO2 atm) and resuspended in the same buffer.

Mineral preparation

CCa-2, an iron-bearing ripidolite chlorite from Flagstaff Hill (El Dorado County, CA, USA), was purchased in two separate batches from the Source Clays Repository (West Lafayette, IN). One

Results

The speciation of Fe in these experiments is difficult to assign because of the multiple possible forms of Fe(II) in chlorite. In its unaltered, initial form, all of the Fe(III) in chlorite is structural Fe(III) located in the octahedral sheet of the TOT layer (Brandt et al., 2003). In its unaltered, initial form, the Fe(II) in chlorite is distributed in both the tetrahedral and octahedral sheets of the TOT layer and in the brucite-like sheet attached to the TOT layer. After chemical or

Discussion

In these experiments with multiple TEAs, i.e., structural Fe(III) in chlorite, U(VI), and AQDS, the apparent utilization of TEAs is complicated by valence cycling of the TEAs themselves. For example, we have recently shown that U valence cycling increased the rate and extent of bioreduction of structural Fe(III) in nontronite (Zhang et al., 2009). In those experiments, substantial concentrations of biogenic Fe(II) evolved before any U(VI) was removed from solution even though U(VI) reduction

Acknowledgements

This research was supported by the Subsurface Biogeochemical Research (SBR) Program, Office of Science (BER), U.S. Department of Energy (DOE) grant no. DE-SC0005333 to The Pennsylvania State University, and by the National Science Foundation under grant no. CHE-0431328. ANL contributions were supported, in part, by the ANL Subsurface Science Scientific Focus Area project, which is part of the SBR Program of BER, U.S. DOE under contract DE-AC02-06CH11357. Use of the MRCAT/EnviroCAT sector at the

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