Biosynthesis of Nanocrystal Akaganéite from FeCl2 Solution Oxidized

Environ. Sci. Technol. 2008, 42, 4165–4169

Biosynthesis of Nanocrystal Akagane´ ite from FeCl2 Solution Oxidized by Acidithiobacillus ferrooxidans Cells HUIXIN XIONG,† YUEHUA LIAO,† L I X I A N G Z H O U , * ,† Y I Q U N X U , ‡ A N D SHIMEI WANG† College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, P.R. China, and College of Environmental Sciences and Engineering, Yangzhou University, Yangzhou 225009, P.R. China

Received November 23, 2007. Revised manuscript received February 28, 2008. Accepted March 4, 2008.

Akagane´ite (β-FeOOH) is a major iron oxyhydroxide component in some soils, marine concretions, and acid mine drainage environments. Recently, synthetic β-FeOOH has been found to be a promising absorbent in the treatment of metalcontaminated water. It has been recognized in previous study that akagane´ite could be formed via FeCl2 chemical oxidation under specific conditions. Here we report a novel and simple method for akagane´ite bioformation from FeCl2 solution oxidized by Acidithiobacillus ferrooxidans LX5 cells at 28 °C. After acclimation in modified 9K medium containing 0.2 M chloride, Acidithiobacillus ferrooxidans cells had great potential for oxidization of Fe2+ as FeCl2 solution, and then resulted in the formation of precipitates. The resulting precipitates were identified by powder X-ray diffraction and transmission FT-IR analyses to be akagane´ite. Scanning electron microscopy imagesshowedtheakagane´itewasspindle-shaped,approximately 200 nm long with an axial ratio of about 5, and the spindles had a rough surface. X-ray energy-dispersive spectral analyses indicated the chemical formula of the crystalloid akagane´ite could be expressed as Fe8O8(OH)7.1(Cl)0.9 with Fe/Cl molar ratio of 8.93. The biogenetic akagane´ite had a specific surface area of about 100 m2 g-1 determined by BET method.

Introduction Iron oxyhydroxides (FeOOH), as a group, are commonly found in minerals, soils, and corrosion products of steels and organisms (1). Akagane´ite (namely β-FeOOH), one of the polymorphs of iron oxyhydroxides, is less common than either goethite (R-FeOOH) or lepidocrocite (γ-FeOOH) in nature (2). However, it has been recognized as a major iron oxyhydroxide component in some soils and hydrothermal systems (3, 4). It has also been identified in marine concretions (5, 6) and acid mine drainage environments (7). Akagane´ite has a tetragonal structure consisting of double chains of edge-shared octahedra that share corners with adjacent chains to form channels running parallel to the c-axis, which can be occupied by chloride ions and water * Corresponding author phone: +86-25-84395160; fax: +86-2584395343; e-mail: [email protected]. † Nanjing Agricultural University. ‡ Yangzhou University. 10.1021/es702933v CCC: $40.75

Published on Web 04/18/2008

 2008 American Chemical Society

molecules (8, 9). This tunnel structure makes akagane´ite an especially interesting material in the areas of catalysis, electrode materials, and ion exchange (10, 11). The application of akagane´ite for hydroprocessing of coal has been reported due to its high catalytic activity (10). Akagane´ite is also widely used in the fields of pigment, magnetic powders, and adsorbent production (1, 12). Recently, akagane´ite has been found to have great potential for the treatment of metalor metalloid-contaminated water. For example, akagane´ite can specifically adsorb arsenate from aqueous solutions with a maximum load capacity of 120-150 mg As(V) per g of akagane´ite (13). Surfactant-modified akagane´ite has also been investigated and proved to be very effective for removal of more toxic As(III) ions with an adsorbent capacity of about 84 mg As(III) g-1 (14). Furthermore, bead cellulose loaded with β-FeOOH is considered to have high removal efficiency for arsenic from groundwater with adsorption capacity for arsenite and arsenate of 99.6 and 33.2 mg g-1, respectively (15). It is well-known that groundwater contaminated by arsenic poses great health risk to millions of persons worldwide (16, 17) and iron hydroxides are gaining considerable interest in recent years due to their high affinity with inorganic arsenic species (18, 19). Moreover, akagane´ite has also been shown to be an effective material for hexavalent chromium ions removal with a sorption capacity approximately 80 mg Cr(VI) g-1 (20). Therefore, the synthesis of akagane´ite has been extensively investigated owing to its wide application. Akagane´ite chemical synthesis methods studied mainly include forced hydrolysis of FeCl3 at low pH with heating to 60-100 °C or neutralization of FeCl3 solution at room temperature by slow addition of various precipitating agents such as ammonium carbonate, ammonia, sodium hydroxide, or urea, etc., yet requiring subsequent dialysis in cellulose membrane against distilled water for several days (21-26). Moreover, it was reported that when solution pH ranged from 3 to 4.5, akagane´ite was the only solid phase occurred in FeCl2 solution oxidized by air at 25 °C with addition of sodium hydroxide (27, 28). However, it is well documented that Acidithiobacillus ferrooxidans (A. ferrooxidans), an acidophilic chemolithotroph and gram-negative bacterium (0.5-0.6 µm wide by 1.02.0 µm long) (29, 30), can obtain energy for growth and maintenance from the oxidation of ferrous iron or reduced sulfur compounds (31). A. ferrooxidans is able to grow at a pH value between 1 and 6 (32), whereas with the optimal pH for ferrous iron oxidation at about 3.0 (30). The formation of acid mine drainage (AMD) is closely linked to oxidation of pyrite accelerated by A. ferrooxidans at low pH (33). Karathanasis and Thompson (7) observed the occurrence of akagane´ite in a constructed acid mine drainage wetland, implying the presence of A. ferrooxidans facilitated the formation of akagane´ite. However, little information is available on the biological formation of akagane´ite facilitated by A. ferrooxidans in chloride medium such as FeCl3 or FeCl2 since inhibition effects of chloride on ferrous iron oxidation as well as the growth of A. ferrooxidans have been reported in previous studies (34, 35). It is noticeable that some acidic chloride-rich media exist extensively such as some industrial wastewater and some types of sewage sludge. In recent years, we found that iron hydroxysulfate was often observed in acidic sulfate- and chloride-rich bioleached sludge involving A. ferrooxidans (36, 37). In light of the above findings, we presumed that the formation of akagane´ite might be achieved through oxidation of ferrous iron by A. ferrooxidans in chloride-rich environments under ambient conditions. VOL. 42, NO. 11, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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Therefore, the objectives of this work are to (1) investigate whether ferrous iron in acidic FeCl2 solution is able to be oxidized facilitated by A. ferrooxidans cells, consequently resulting in the formation of akagane´ite-like precipitate, and (2) characterize the resulted akagane´ite-like precipitate by X-ray diffraction (XRD), transmission FT-IR, and scanning electron microscopy (SEM) with X-ray energy-dispersive spectral analyses (EDS). The expected outcome from the present study will contribute to the understanding of akagane´ite formation facilitated by A. ferrooxidans in acidic natural or artificial environments under ambient conditions, and also will provide a new approach for preparation of akagane´ite, as a nanocrystal material used as potentially efficient adsorbent for the removal of toxic elements such as arsenic or chromium from contaminated water.

Materials and Methods Microorganisms and Inoculum. Acidithiobacillus ferrooxidans LX5 (CGMCC No. 0727) obtained from China General Microbiological Culture Collection Center (CGMCC) was cultured in modified 9K medium (38). The medium was adjusted to pH ∼2.5 with 9 N H2SO4 and autoclaved at 121 °C for 15 min. Five percent (v/v) of the cultures of A. ferrooxidans was inoculated into the medium and incubated at 28 °C for 3-4 days with continuous aeration. Acclimation of A. ferrooxidans by Chloride. Chloride ion was reported to inhibit ferrous iron oxidation by A. ferrooxidans due to its negative impact on the microorganism growth (34, 35). Also, our preliminary experiments did show that the oxidation rate of ferrous iron (as 0.1 M FeCl2) by chlorideacclimated A. ferrooxidans was about 2-3 times faster than that by nonacclimated bacteria. Thus, acclimation of A. ferrooxidans by chloride was conducted in this study with an aim to enable A. ferrooxidans to adapt well to the chloriderich medium. To obtain an optimum concentration of chloride for cultivation of the microorganism, different contents of NaCl in the range from 0 to 0.3 M were added to 500-mL flasks containing 250 mL of modified 9K medium with 5% (v/v) inoculums of A. ferrooxidans cultures. The initial pH of the medium was adjusted to 2.84 with 9 N H2SO4. All flasks were shaken at 180 rpm and 28 °C in a horizontal shaker. The water content lost in the flasks due to evaporation during the trial was replenished with distilled water by weight method. During incubation, 5 mL of suspension was withdrawn from each flask at a given interval and centrifuged at 12 000 rpm for 15 min. The supernatants were filtered through a Whatman No. 4 filter paper and acidified to pH 2 with 6 N HCl, then stored at 4 °C prior to Fe determination by a colorimetric procedure using 1,10-phenanthroline as described in Standard Methods (39). After 5 days for acclimation, cell numbers in cultures were determined by a double-layer plate method as described by Wang and Zhou (40). The concentration of chloride in the culture with maximum cell density was then selected for bacterial acclimation. Finally, the acclimation of bacteria was performed in the medium with such chloride concentration through continuous culture for 3-4 generations in order to reduce the length of the lag phase for the bacterial grown in the medium containing the above-mentioned chloride concentration. Preparation of the Chloride-Acclimated A. ferrooxidans Cells Suspension. Chloride-acclimated A. ferrooxidans cells were harvested at the end of exponential phase of growth (about 40-48 h after inoculation). The cultures were first filtered through a Whatman No. 4 filter paper to remove precipitated iron. Subsequently, the filtrate was passed through a 0.22-µm Millipore membrane to separate the cells. Cells were washed twice with dilute H2SO4 solution (pH 2.5) followed by rinsing with distilled water, and then resuspended in distilled water. A. ferrooxidans cell numbers in suspension were determined by a double-layer plate method (40) prior 4166

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to synthesis experiments. The cell density of the chlorideacclimated A. ferrooxidans resuspended in distilled water was about 7.8 × 108 cells mL-1. Formation of Precipitates. The formation of precipitates was performed in triplicate with 270 mL of solution, each containing 0.1 M FeCl2 and approximately 5.0 × 107 cells mL-1 of chloride-acclimated A. ferrooxidans in a 500-mL flask. The flasks were shaken at 180 rpm and 28 °C in a horizontal shaker. A control without addition of A. ferrooxidans cells was also conducted in this study. Water content lost from the flasks due to evaporation during the trial was replenished with distilled water by weight method. During the formation of precipitates, 5 mL of the solution was taken out of flasks periodically for Fe determination by the method described above. Meanwhile, ORP and pH of solutions were monitored using a pHS-3C model digital pH-meter. The suspended yellow precipitate formed in 2-3 days was observed. After 4 days, the precipitates were collected from the flasks by centrifuging at 12 000 rpm at 4 °C and thoroughly washed with distilled water until no Cl- existed, and then dried in air at room temperature and identified by following the methods described below. Methods for Characterization of Precipitates. The phases of products were determined by powder X-ray diffraction (XRD) using a D8 ADVANCE model diffractometer with a Cu target (40 kV and 200 mA). Powder diffraction patterns were obtained by scanning speed of 6 deg min-1 and scanning angles in 10-80 deg. The characteristic reflection peaks (d values) were matched with JCPDS data files, and the crystalline phases were identified. The FT-IR spectra were taken on a Nicolet 500 Fourier transform spectrometer at a resolution of 4 cm-1 using a KBr beamsplitter, a DTGS detector with KBr window, and a sample shuttle for the transmittance measurements. The background was taken on a disk made from 400 mg KBr. The morphology and elemental composition were examined by a Hitachi S-4800 field emission-scanning electron microscope (SEM) equipped with an energy dispersive spectral analyzer (EDS), operated at 15.0 kV accelerating voltage. EDS analysis of mineral sample has typically been applied to quantitative identification of major elements with rough estimates of composition based on relative peak intensities. Analytical data were obtained on the SEM using a standardless Link Analytical eXL energy dispersive analysis system with a ZAF4-FLS deconvolution/recalculation package. Specific surface area of the precipitate was measured by multipoint BET method using a Micrometrics ASAP 2010 surface area analyzer and N2 as the adsorbate.

Results and Discussion Effect of Chloride on Activity of A. ferrooxidans in Cultivation. The effect of different concentrations of chloride in modified 9K medium on the efficiency of ferrous iron oxidation by A. ferrooxidans during cultivation is shown in Figure 1. It was noted that the presence of 0.1 or 0.2 M chloride had no substantial influence on biooxidation of ferrous iron to ferric iron, except that a little inhibition of ferrous iron oxidation occurred in the culture containing 0.2 M Clcompared to the control without addition of NaCl. However, a marked inhibition to ferrous iron biooxidation in medium was observed in the presence of 0.25 and 0.3 M Cl-. Meanwhile, enumeration of viable bacteria showed that there were ∼108, ∼106, and ∼104 cells mL-1 in the cultures containing chloride of 0-0.2, 0.25, and 0.3 M, respectively. Obviously, acclimation in 0.2 M chloride not only enabled A. ferrooxidans to be capable of oxidizing ferrous iron but also received the maximum cell density. Accordingly, for FeCl2 biooxidation experiment, 0.2 M chloride was selected for acclimation of bacteria.

FIGURE 3. XRD patterns of the precipitate from FeCl2 biooxidation by A. ferrooxidans. Numerical values for XRD peaks are in Ångstrom units for interatomic spacings.

FIGURE 1. Ferrous iron oxidation during A. ferrooxidans cultivation in modified 9K medium containing different concentrations of sodium chloride.

FIGURE 4. FT-IR spectra of the precipitate from FeCl2 biooxidation by A. ferrooxidans.

FIGURE 2. Fe2+ concentration, oxidation rate of Fe2+, pH, and ORP changes against reaction time during formation of the precipitates: (a) Fe2+ concentration (dashed curves) and percent Fe2+oxidation (solid curves); (b) pH (dashed curve) and ORP (solid curve). (Symbols: (∆) reaction with cells; (O) control.) Changes of pH, ORP, and Fe2+ Concentration in Solution during the Formation of Precipitates. After addition of the chloride-acclimated A. ferrooxidans, the FeCl2 solution

gradually turned to turbid suspension that was weakly yellow, and then precipitates formed. During formation of precipitates, Fe2+ concentration, pH, and ORP varied drastically with the increase of reaction time (see Figure 2). As shown in Figure 2a, Fe2+ concentration in solutions decreased rapidly from 5.6 to 3.0 g L-1 in the first 24 h due to oxidation of ferrous iron by A. ferrooxidans. Fe2+ concentration in solution was maintained at 3.0 g L-1 after 24 h. In contrast, Fe2+ concentration in the control hardly decreased throughout the experiment, indicating that the chemical oxidation of ferrous iron was negligible in this study. According to Figure 2b, a continuous pH decrease from 3.2 to 1.5 and a corresponding ORP increase from 459 to 616 mV were observed in the first 24 h, and then they maintained at constant values. The rapid decrease of pH in solution was due to the net effect of the oxidation of ferrous iron and subsequent hydrolysis of the resulted ferric iron (41). When pH in solution decreased to about 1.5, the activity of A. ferrooxidans was strongly inhibited (30). Therefore, the concentration of ferrous iron in solution was constant at about 3.0 g L-1 after reaction for 24 h. Correspondingly, pH value in solution did not decrease greatly any more. Characterization of Precipitate. Whole-angle X-ray diffraction pattern of the produced precipitates is exhibited in Figure 3. The strong and sharp whole-angle diffraction peaks indicate that the precipitate had a fine crystallinity. It was identified as akagane´ite according to the JCPDS card no. 34-1266 (42), as difference was hardly observed between XRD patterns of the precipitate in present study and the standard akagane´ite pattern (42) except that the intensity of (211) peak at the d value of 2.55 Å was higher than that of (310) peak at the d value of 3.34 Å, which is contrary to standard patterns of akagane´ite. Actually, similar results have been reported by Cornell and Schwertmann (43), who ascribed this difference to the presence of rod-shaped akagane´ite crystals. VOL. 42, NO. 11, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 5. SEM images and ED spectra of the precipitate from FeCl2 biooxidation by A. ferrooxidans. However, akagane´ite in this work was presented in the shape of spindle-like crystals. Infrared (IR) spectroscopy of the precipitate (Figure 4) exhibited a split band with maxima at 3400 and 3340 cm-1 attributed to OH-stretching region in the akagane´ite, and some successive bands of H2O-bending located at 1652, 1538, and 1453 cm-1 (12, 23). The bands at 846 and 668 cm-1 were the vibration modes of the two O-H · · · Cl hydrogen bonds present, which were characteristic of chloride-containing akagane´ite (43). In addition, an intense band at 421 cm-1 was attributed to a symmetric Fe-O-Fe stretching vibration (44). In conclusion, IR spectra of the precipitate were in good agreement with literature data. Therefore, IR spectra further testified the biological product being akagane´ite. Furthermore, the SEM image in Figure 5 showed that the biogenetic akagane´ite were spindle-type particles approximately 200 nm long with an axial ratio of about 5 and the spindles had a rough surface. Similar results were also reported by Kan et al. (22) and Ishikawa et al. (45) when FeCl3 solution was aged at boiling point and at 50 °C, respectively. However, the spindle-like morphology differed markedly from that previously described for chemically synthetic akagane´ite of needle-like, somatoids shaped, or rod shaped (12, 43). Results of EDS analysis revealed that 5.75 wt% of Cl and 80.99 wt% of Fe were incorporated into the product of akagane´ite resulting in a Fe/Cl molar ratio of 8.93. Therefore, the chemical formula of akagane´ite could be expressed as Fe8O8(OH)7.1Cl0.9. The chloride content of akagane´ite in this work was consistent with the range between 1% and 7% as described by Cornell and Schwertmann (43). In addition, the akagane´ite had a specific surface area of about 100 m2 g-1 (determined by multipoint BET method), which was lower compared to literature values (12, 20, 24), maybe resulting from the aggregation of the biogenetic particles. Obviously, biosynthesis of pure akagane´ite proposed in the present work can be achieved through oxidation of FeCl2 by chloride-acclimated A. ferrooxidans under ambient conditions (namely ∼28 °C and 1 atm) without any control of pH in the reaction system. It is worthwhile to point out that, in akagane´ite (Fe8O8(OH)7.1Cl0.9), the tunnel was partly occupied by 5.75 wt% of Cl which appeared to be essential for its structural stability according to Schwertmann and Cornell (46). Indeed, in another experiment, we found that the analogous compound with SO4 occupying the tunnel position instead of Cl was typically identified as biogenic schwertmannite, a poorly crystalline oxyhydroxysulfate under similar experiment conditions (data not shown). In another word, A. ferrooxidans was able to result in the formation of typical schwertmannite 4168

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or akagane´ite in the ferrous solution containing sulfate or chloride only, respectively. Furthermore, in the complex ferrous solution containing both sulfate and chloride (FeSO4 + FeCl2), sulfate inhibited drastically the formation of biogenic akagane´ite, resulting in only schwertmannite occurrence even in the ferrous solution with Cl-/SO42- mole ratio being as high as 10 (data not shown). Similar results were also reported by Ishikawa et al. (25) for chemical synthesis of akagane´ite, in which the addition of SO42- and HPO42- in Fe(II)-oxidation and Fe(III)-hydrolysis interfered greatly with the particle growth and crystallization of β-FeOOH. Therefore, it appears that chloride present in solution was essential to the formation of biogenic akagane´ite by A. ferrooxidans.

Acknowledgments This research was supported jointly by National Natural Science Foundation of China (20677028) and the 863 program of China (2006AA06Z314). We appreciate Dr. W. D. Zhou at Yangzhou University, China, for his excellent technical assistance in XRD, FT-IR, and SEM-EDS analyses. We also thank Associate Editor David A. Dzombak and four anonymous reviewers for their valuable comments on this manuscript.

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