Environ. Sci. Technol. 2008, 42, 6154–6159
Removal of Arsenic from Contaminated Soils by Microbial Reduction of Arsenate and Quinone S H I G E K I Y A M A M U R A , * ,† MIRAI WATANABE,† MASAYA KANZAKI,‡ SATOSHI SODA,‡ AND MICHIHIKO IKE‡ Water and Soil Environment Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan and Division of Sustainable Energy and Environmental Engineering, Graduate School of Engineering, Osaka University, 2-1 Yamada-oka, Suita, Osaka 565-0871, Japan
Received December 17, 2007. Revised manuscript received May 21, 2008. Accepted May 30, 2008.
We investigated bioremediation of As-contaminated soils by reductive dissolution of As using a dissimilatory As(V)-reducing bacterium (DARB), Bacillus selenatarsenatis SF-1. We also examined the effect of anthraquinone-2,6-disulfonate (AQDS), an extracellular electron-shuttling quinone, on the As extraction. When B. selenatarsenatis was incubated with As(V)-laden Al precipitates, no acceleration of As dissolution was observed in the presence of AQDS, even though the microbial reduction of AQDS occurred actively. In contrast, AQDS addition significantly enhanced the reductive dissolution of As and Fe in analogous experiments with As(V)-laden Fe(III) precipitates, whereas As dissolution did not occur in the absence of the As(V) reducer. These results indicate the dissolution of As was accelerated by indirect reduction of solid-phase Fe(III) following microbial AQDS reduction, although As(V) reduction is vital for As extraction. B. selenatarsenatis was able to extract As from two types of industrially contaminated soils through reduction of solid-phase As(V) and Fe(III). The copresence of AQDS with B. selenatarsenatis improved the removal efficiency of As from the contaminated soils, concomitantly releasing Fe(II), suggesting that simultaneous use of DARB and electron-shuttling compounds can be an effective strategy for remediation of As-contaminated soils.
Introduction Industrial activities such as mining, smelting, manufacturing, and wood preservation have led to the accumulation of arsenic (As) in soils (1, 2). As-contaminated sites have been found throughout the world (3, 4), particularly in Japan, where As has become one of the most prevalent soil contaminants. In most cases, soil replacement, containment, and solidification methods are utilized for the treatment of soils contaminated with metals and metalloids, including As (5, 6), but these techniques are often expensive and labor intensive. In addition, because of the risk of leaching of As, soils treated by these methods must be monitored. In Japan, the Soil Contamination Countermeasures Law enforced in 2003 * Corresponding author phone: +81-29-850-2168; fax: +81-29850-2576; e-mail:
[email protected]. † National Institute for Environmental Studies. ‡ Osaka University. 6154
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requires management of designated areas where soil standards are not met until remediation is completed. Thus, development of cost-effective alternatives for As remediation is acutely needed to reduce environmental risk. Our previous studies suggested that reductive dissolution of As by means of a dissimilatory arsenate-reducing bacterium (DARB) might be an effective alternative for remediation of As-contaminated soil (7, 8). In soil, As exists mainly in two inorganic forms, arsenate (As(V)) and arsenite (As(III)) (1, 9, 10). As(V), generally found to be the predominant As species in As-contaminated soils (11–13), is strongly adsorbed on soil minerals (e.g., Fe(III) and Al oxides and hydroxides), whereas As(III) is much less adsorptive and more mobile than As(V) (1, 10). We successfully extracted As from various As-laden solids, including model contaminated soils spiked with As(V), using the microbial reduction of As(V) to As(III) (8). However, the removal efficiency was insufficient for practical use; the soil concentration standard set by the Soil Contamination Countermeasures Law in Japan (150 mg/kg, 1 N HCl-extractable) could not be achieved only by the DARB. While simultaneous use of washing agents may improve the removal efficiency, soil washing with chemical agents often causes significant dissolution and loss of valuable soil minerals (14), which can prevent reuse of the soils after treatment. Thus, investigations into stimulating the Asspecific microbial reduction are desirable. A number of studies have shown that anthraquinone2,6-disulfonate (AQDS), a functional analog for quinone moieties in humic substances, shuttles electrons between microorganisms and insoluble Fe(III), leading to reductive dissolution of various Fe(III) minerals (15–17). The reduced product, anthrahydroquinone-2,6-disulfonate (AH2QDS), can act as a chemical reductant with concomitant regeneration of AQDS; AH2QDS has been reported to enhance the reduction of other metals and radionuclides including Cr(V), U(VI), and Tc(VII) (18, 19). Reductive dissolution of Fe(III) oxides can indirectly enhance As mobilization, in which the associated As is released into solution (20), as well as the direct reduction of associated As(V) (8, 21, 22). Thus, our working hypothesis is that the microbial reduction of electron-shuttling compounds like AQDS could stimulate DARB-mediated As dissolution from soils by enhancing the reduction of As(V), Fe(III), or both. To our knowledge, however, there has been no experimental evidence for this hypothesis. Our objectives in this study were to (1) demonstrate that microbial AQDS reduction could enhance As extraction by means of DARB and (2) determine the specific mechanisms controlling As extraction in this proposed strategy. In this study, we conducted extraction experiments on As(V)-laden Al precipitates in the presence and absence of AQDS to determine whether AQDS could stimulate As extraction using a well-characterized DARB, Bacillus selenatarsenatis SF-1 (7, 8, 23), by direct reduction of solid-phase As(V) and on As(V)-laden Fe(III) precipitates to determine whether enhancement of reductive dissolution of solid-phase Fe(III) by microbial AQDS reduction could indirectly stimulate As extraction. We also demonstrated microbial As extraction from two types of As-contaminated soils collected at a former factory site with and without AQDS.
Materials and Methods Media and Cultivation. Bacillus selenatarsenatis SF-1 is a facultative anaerobic bacterium isolated from sediment in an effluent drain in a glass-manufacturing plant (23). The basal salt medium containing 0.1% yeast extract (BSMY) has 10.1021/es703146f CCC: $40.75
2008 American Chemical Society
Published on Web 07/09/2008
been described previously (7). B. selenatarsenatis was cultivated in a pH 8.0 lactate medium (LM; 20 mM lactate in BSMY). Unless otherwise stated, incubations were performed in 20 mL of LM in 50-mL serum bottles sealed with butyl rubber stoppers and aluminum crimp seals. For anaerobic cultivation, the bottles’ headspace was purged with N2 gas. Cultures were incubated at 30 °C on a reciprocal shaker at 120 rpm. Bacillus jeotgali JCM 10885, the nearest phylogenetic relative of B. selenatarsenatis (23), was obtained from RIKEN BRC-JCM. B. jeotgali was cultivated under the same conditions as was B. selenatarsenatis. Soil Characterization and Digestion. Two types of Ascontaminated soils (soils L and H) were collected from a former factory site in Hyogo Prefecture, Japan. All soil samples were air dried and sieved (2-mm mesh) to remove pebbles and ground and mixed thoroughly prior to analysis. For analysis of elements in the soils, the soil samples were digested with mixtures of acids (HClO4/HNO3/HF) in stainless steel high-pressure bombs with Teflon double vessels (140 °C, 6 h), as described previously (24). To determine HClextractable As (the soil concentration standard set by the Soil Contamination Countermeasures Law in Japan), 1.5-g soil samples were extracted with 50 mL of 1 N HCl by reciprocal shaking for 2 h at room temperature. All digested and extracted samples were filtered (0.45 µm filter) prior to analysis. Characteristics of As-contaminated soils are summarized in the Supporting Information, Table S1. Microbial As Extractions. As(V)-laden Al and Fe(III) precipitates were prepared by adding 5 mM Al2(SO4)3 or 10 mM FeCl3 to 10 mL of 2 mM As(V) solution in 50-mL serum bottles as described previously (8); 10 mL of sterile LM was then added to each bottle. Each precipitate sample would contain 5 mM dissolved Al or Fe with 1 mM dissolved As if the Al, Fe(III), and As(V) contained in the precipitates were completely extracted. Powder X-ray diffraction (XRD) revealed both As(V)-laden Al and Fe(III) precipitates were amorphous (Supporting Information, Figure S1). Three gram samples of contaminated soil were each placed in 100 mL serum bottles. The bottles were then autoclaved (121 °C, 1 h), and 60 mL of LM was added to each bottle. Each sample bottle was inoculated with an aliquot of aerobically grown cell suspension (3-5 × 107 cells/mL), and the mixtures were then incubated under anaerobic conditions. To investigate the effect of extracellular quinone on As dissolution, AQDS was added to each bottle to give a final concentration of 0.1 or 1 mM before inoculation. All experiments were duplicated, and an additional bottle was left uninoculated as a control in each experiment. The bottles were periodically removed from incubation for sampling. The mixtures of LM and solids were filtered (0.45 µm filter), and the filtrates were acidified immediately with 1 N HCl to stabilize Fe(II). However, when the HClextractable phase was analyzed, HCl was added prior to filtration. Analyses. Multielement analysis (including As analysis) of filtered soil digestions and extractions was carried out by inductively coupled plasma-atomic emission spectrometry (ICP-AES: ICAP-750, Nippon Jarrell-Ash, Japan). Aqueous and HCl-extractable Fe(II) were determined by means of the ferrozine assay, with ferrous ethylene diammonium sulfate as the Fe(II) standard (21, 25). As(V) concentration in the cultures was quantified by ion chromatography with a conductivity detector as described previously (7). Concentrations of AH2QDS were determined according to Cervantes et al. (26). The cell density of B. selenatarsenatis in cultures was expressed as optical density at 650 nm (OD650) measured using a spectrophotometer.
FIGURE 1. Reduction of AQDS (a) and As(V) (b) by B. selenatarsenatis in liquid cultures. Liquid cultures (LM) containing AQDS (1 mM) and/or As(V) (1 mM) were incubated with B. selenatarsenatis. Symbols represent the averages of duplicate experiments, and error bars show the range of data. Ranges smaller than the symbols are not displayed.
Results AQDS and As(V) Reduction by B. selenatarsenatis. Under anaerobic conditions, B. selenatarsenatis can reduce As(V), selenate, and nitrate as the terminal electron acceptors coupled with oxidation of an electron donor (7, 23). Selenate is reduced to elemental selenium via the intermediate selenite and nitrate to ammonia via nitrite, but As(III), the reduced product of As(V), is not further reduced by this bacterium. To determine whether B. selenatarsenatis is capable of reducing AQDS as well as other electron acceptors and its effect on capability of reducing As(V), we investigated preliminary experiments with liquid cultures containing AQDS and/or As(V). Production of AH2QDS, the reduced form of AQDS, obviously occurred in the liquid cultures containing AQDS, although the copresence of As(V) delayed the beginning of AQDS reduction (Figure 1a). In contrast, reduction of As(V) was slightly slowed by AQDS addition in the cultures containing As(V) (Figure 1b). Growth of B. selenatarsenatis was lower in the presence of AQDS when As(V) was added as the electron acceptor. Effect of AQDS on As Extraction from As(V)-Laden Precipitates. In extraction experiments with As(V)-laden Al precipitates, AQDS had no noticeable effect on As dissolution by B. selenatarsenatis (Figure 2a). AH2QDS was produced in the presence of B. selenatarsenatis (Figure 2b), indicating that biological reduction of AQDS actively occurred in the extraction experiments. No significant As dissolution or AQDS reduction was observed in the abiotic controls, and dissolved Al was not detected in any of the experiments. In extraction experiments with As(V)-laden Fe(III) precipitates, dissolved As accumulated rapidly when the precipitates were incubated with B. selenatarsenatis, whereas aqueous As levels remained nearly unchanged in the abiotic control experiments regardless of AQDS addition (Figure 3a). The rate and extent of As extraction were clearly enhanced VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. (a) Reductive dissolution of As from As(V)-laden Al precipitates, and (b) production of AH2QDS by means of microbial AQDS reduction. Liquid cultures (LM) containing solid-phase As(V) (1 mM) and Al (5 mM) were incubated with B. selenatarsenatis, AQDS (1 mM), or both. Symbols represent the averages of duplicate experiments, and error bars show the range of data. Ranges smaller than the symbols are not displayed. by AQDS in the inoculation experiments. After 7 d of incubation in the presence of both B. selenatarsenatis and AQDS, the accumulated aqueous As accounted for 65% of the initial solid-phase As, an amount nearly twice that observed with only B. selenatarsenatis (35%). Aqueous Fe, detected almost entirely as Fe(II), also accumulated concomitantly with As dissolution; 48% and 10% of the initial solid-phase Fe was solubilized with and without AQDS, respectively (Figure 3b). Fe(II) production proceeded more rapidly in AQDS-amended incubations throughout the experiments (Figure 3b and 3c). Most Fe(III) in the HClextractable phase was reduced to Fe(II) after 7 d in the presence of AQDS, whereas only about 30% of Fe(III) was converted to Fe(II) in the absence of AQDS (Figure 3c). Neither accumulation of aqueous Fe nor reduction of Fe(III) to Fe(II) was observed in the abiotic experiments (data not shown). We also conducted similar experiments on As(V)-laden precipitates using B. jeotgali, which cannot reduce As(V) (23), to investigate the role of microbial AQDS and As(V) reduction in As extraction. In experiments with As(V)-laden Al precipitates, no As dissolution was observed even when B. jeotgali was incubated with AQDS, although B. jeotgali was found to be able to reduce AQDS (data not shown). Similarly, in experiments on As(V)-laden Fe(III) precipitates, As dissolution did not occur in the presence of B. jeotgali, and addition of AQDS did not accelerate As dissolution (Figure 4). However, reductive dissolution of Fe(III) was observed in the presence of B. jeotgali, and it was greatly accelerated by AQDS addition, as observed with B. selenatarsenatis. Stimulation of Microbial As Extraction from Contaminated Soils Using AQDS. B. selenatarsenatis and AQDS were incubated with As-contaminated soils (soil L, 250 mg-As/kg; soil H, 2400 mg-As/kg) to test whether the electron-shuttling compound could enhance the microbial reductive dissolution of As from soils. For both soils, the concentration of aqueous As clearly increased after 7 d in the presence of B. selenatarsenatis, whereas no remarkable extraction was observed in abiotic control experiments (Figure 5). The copresence of AQDS greatly enhanced As extraction with B. selenatarsenatis, whereas As dissolution was not significant in the presence 6156
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FIGURE 3. Reductive dissolution of As and Fe from As(V)-laden Fe(III) precipitates. The data represent concentrations of (a) dissolved As, (b) Fe, and (c) HCl-extractable Fe. Liquid cultures (LM) containing solid-phase As(V) (1 mM) and Fe(III) (5 mM) were incubated with B. selenatarsenatis, AQDS (0.1 mM), or both.
FIGURE 4. Reductive dissolution of Fe from As(V)-laden Fe(III) precipitates in the absence of microbial As(V) reduction. Liquid cultures (LM) containing solid-phase As(V) (1 mM) and Fe(III) (5 mM) were incubated with B. jeotgali, AQDS (0.1 mM), or both. of AQDS alone. In the inoculation experiments, the As removal efficiencies, calculated from the percentage of the total amount of As dissolved to the initial amount in soils, increased to 56% and 40% in soils L and H, respectively, in the presence of AQDS, whereas the removal efficiencies were 32% and 19%, respectively, without AQDS. Dissolution of Fe was observed when B. selenatarsenatis existed, and the extent of Fe dissolution was much greater in the presence of AQDS (Figure 6). In all extraction tests, most of the dissolved Fe
controls, the loss did not exceed 7% of the initial Fe. The decrease/increase of the other minerals did not vary greatly compared with abiotic control experiments.
Discussion
FIGURE 5. Reductive dissolution of As from contaminated soils. The data represent dissolved As concentrations in (a) soil L and (b) soil H slurries after 7-d extraction experiments. Soil slurries containing liquid LM were incubated with B. selenatarsenatis, AQDS (1 mM), or both. The amount of As contained in soil L and soil H, if completely extracted, would be equal to 0.17 and 1.6 mM dissolved As, respectively. Values represent the averages of duplicate experiments, and error bars show the range of data. For characteristics of contaminated soils, see Table S1.
FIGURE 6. Dissolved total Fe (T-Fe) and Fe(II) concentrations in (a) soil L and (b) soil H slurries after 7-d extraction experiments. For experimental conditions, see Figure 5. was in the Fe(II) form. There were no changes of pH in soil slurries (nearly 8.0) during the extraction experiments. To evaluate the effect of microbial As extraction on the soil mineral components, we also monitored the changes in soil composition during the extraction experiments (Supporting Information, Table S2). With B. selenatarsenatis and AQDS, 140 and 970 mg/kg of As were removed from contaminated soils L and H, respectively; these amounts were about twice the amounts removed with only B. selenatarsenatis. Although the Fe concentration in the soils decreased slightly in the inoculation experiments compared to abiotic
Roles of AQDS and As(V) Reduction in the Microbial As Extraction. B. selenatarsenatis was able to reduce AQDS to AH2QDS under an anaerobic condition. Since AQDS reduction was inhibited by the copresence of As(V) and began after As(V) reduction was almost complete in liquid cultures, AQDS seems to act as an electron acceptor for anaerobic respiration as well as As(V), selenate, and nitrate. However, when As(V) was added as an electron acceptor, cell growth of B. selenatarsenatis was lower in the copresence of AQDS, and thus, there was no conclusive evidence that B. selenatarsenatis can utilize AQDS as a terminal electron acceptor. A previous study revealed that solid-phase As(V) reduction mediated by B. selenatarsenatis results in the dissolution of As(III) into solution (8). Although extensive production of AH2QDS was observed as a result of microbial AQDS reduction by B. selenatarsenatis, the rate and extent of As dissolution was unchanged compared with the case without added AQDS when Al precipitates were used. Thus, AH2QDS neither catalyzed the reduction of solid-phase As(V) nor enhanced the microbial reductive dissolution of As from the inert solid-phase adsorbent. The results from similar experiments using B. jeotgali also supported this conclusion because As dissolution from Al precipitates hardly occurred in the absence of microbial As(V) reduction even when AH2QDS was actively produced. The results of this study illustrate that B. selenatarsenatis was able to reduce solid-phase Fe(III) as well as As(V) and thus extracted As from amorphous Fe(III) precipitates as a consequence of both As(V) and Fe(III) reduction. As and Fe dissolved simultaneously into solution in all incubations with B. selenatarsenatis, and addition of AQDS greatly enhanced the reductive dissolution of both elements. A similar phenomenon, acceleration of As removal coupled with an increase in dissolved Fe(II), was observed when the Ascontaminated soils were incubated with AQDS and B. selenatarsenatis. These results clearly indicate that microbial AQDS reduction indirectly accelerated the As extraction: the reduction and consequent dissolution of solid-phase Fe(III) released Fe(II) and associated As into solution. On the other hand, B. jeotgali lacking in As(V) reduction ability could not extract As from Fe(III) precipitate, although B. jeotgali could reduce Fe(III), and solid-phase Fe(III) reduction into soluble Fe(II) was clearly stimulated in the copresence of AQDS. Islam et al. (27) reported that microbial reduction of soluble and insoluble Fe(III) resulted in formation of various Fe(II)-bearing minerals, e.g., vivianite and magnetite, accompanied by removal of a considerable amount of As(V) from solution. Also in this study, more than one-half of the Fe(II) produced was still in the solid phase, retaining most As added (Supporting Information, Figure S2), indicating that biogenic Fe(II)-bearing minerals prevented As(V) dissolution. In another study of Islam et al. (28), when As-rich sediments were incubated with acetate under an anaerobic condition, accumulation of Fe(II) did not accompany release of As(V) and As mobilization occurred with an increase in the dissolved As(III) concentration. Therefore, the reductive dissolution of Fe(III) does not seem to be enough to cause significant As extraction from As(V)laden Fe(III) minerals, and As(V) reduction is necessary for effective As removal. From all experimental results, the mechanisms of As extraction from solid phase or soils using DARB and AQDS might be elucidated as depicted in Figure 7. DARB can extract solid-phase As via As(V) reduction into less adsorptive As(III). However, a considerable portion of As remains in the solid VOL. 42, NO. 16, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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termination of the experiments (data not shown), greater removal is likely possible through improvement of the extraction conditions. Moreover, although we utilized AQDS as an electron-shuttling redox mediator for stimulating the microbial As extraction, use of other quinone compounds and naturally occurring mediators that can reversibly form oxidized and reduced statesssuch as juglone, vitamins, and vanillic acid (31–33)smight also lead to improvements in removal efficiency and cost effectiveness. FIGURE 7. Proposed mechanism for the extraction of As from contaminated soil by means of microbial reduction of As(V) and AQDS. DARB: dissimilatory As(V)-reducing bacteria. AQDS: anthraquinone-2,6-disulfonate. AH2QDS: anthrahydroquinone-2,6disulfonate (reduced form of AQDS). phase owing to strong binding to Fe(III). AH2QDS resulting from microbial AQDS reduction can accelerate solid-phase Fe(III) reduction to form soluble Fe(II); this can enhance the release or accessibility of As(V) bound to Fe(III) minerals. The solubilized or surface As(V) is more available for DARB than is the case in the solid-phase, and reduction of As(V) to As(III) prevents As resorption onto soil minerals, allowing more effective As removal from soils. In addition, Campbell et al. (29) indicated that microbial reduction of As(V) to As(III) in an amorphous Fe(III) oxyhydroxide also increases the rate of microbial Fe(III) reduction. Thus, we see As(V) reduction as being vital in this microbial As extraction technique. Enhancement of Fe(III) reduction in the presence of microbial As(V) reduction accelerated As mobilization from both Fe(III) precipitates and contaminated soils in our experiments. However, in column experiments with ferrihydrite-coated sand conducted by Kocar et al. (30), reductive transformation of Fe(III) minerals could adversely promote As sequestration irrespective of its speciation. Although experimental conditions can be quite different, e.g., our study was conducted in batch experiments, long-term incubation might lead to formation of Fe minerals associated with sequestration of As. Thus, it may also be important to control Fe biotransformation by conditioning the incubation period and treatment systems to maintain effective As extraction. As Removal from Contaminated Soil. In this study, we found that a DARB, B. selenatarsenatis, extracted As from soils collected at a former factory site. Although there have been previous reports of DARB-mediated As dissolution from As-rich sediments and minerals under natural or seminatural conditions (21, 22, 28), our results have broad implications for removal of As from soils from contaminated industrial sites. The copresence of an extracellular electron-shuttling compound greatly improved the removal efficiency of As; after 7 d of incubation, As levels in soil L decreased to 110 mg/kg, which is below the soil concentration standard set by the Soil Contamination Countermeasures Law in Japan. The only other major changes in soil composition were an increase in P and a decrease in Ca concentrations, but they were comparable to the case for abiotic controls. Thus, nearly selective removal of As could be achieved; excess loss of soil minerals did not occur even in the presence of AQDS, implying the microbial extraction technique has no destabilizing effect on the soil element balance and the soils are reusable after As removal is complete. These findings suggest that microbial As extraction utilizing DARB in the copresence of the electron-shuttling quinones like AQDS can be an effective technique for the bioremediation of As-contaminated soils. In this study, the combination of B. selenatarsenatis and AQDS was able to remove nearly 1000 mg/kg of As from soil H, which contained a high initial amount of As, although the residual As level (about 1400 mg/kg) was still well above the Japanese legal standard. Because we did not optimize the AQDS concentration and the dissolution of As continued even after 6158
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Acknowledgments This work was supported by a Grant-in-Aid for Young Scientists (B) (no. 18710069) from the Ministry of Education, Culture, Sports, Science and Technology of Japan and the Environmental Technology Development Fund (Feasibility Study 2005) of the Ministry of the Environment of Japan. The authors thank Dr. M. Nishikawa and Ms. M. Okawa for their assistance with ICP-AES analyses and Dr. H. Seyama and Dr. M. K. Koshikawa for XRD data collection and analysis. Constructive comments by three anonymous reviewers, with input from the Associate Editor, further helped to improve this paper.
Supporting Information Available Characteristics of As-contaminated soils (Table S1), changes in concentrations of As and soil components after extraction experiments (Table S2), XRD for As(V)-laden Al and Fe(III) precipitates (Figure S1), and the time course of HClextractable As and Fe concentrations in Fe(III) precipitates incubated with B. jeotgali (Figure S2). This material is available free of charge via the Internet at http://pubs.acs.org.
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