Effects of Chloride Acclimation on Iron Oxyhydroxides and Cell

Dec 3, 2010 - for bioleaching and desulfurization of coal). In this study, we observed the morphology and elemental composition of cells in stationary...
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Environ. Sci. Technol. 2011, 45, 235–240

Effects of Chloride Acclimation on Iron Oxyhydroxides and Cell Morphology during Cultivation of Acidithiobacillus ferrooxidans HUIXIN XIONG AND RONG GUO* School of Chemistry and Chemical Engineering, Yangzhou University, Yangzhou, 225002, PR China

Received January 1, 2010. Revised manuscript received November 14, 2010. Accepted November 22, 2010.

Iron oxyhydroxides as the efficient scavengers for heavy metals have been extensively investigated in iron-rich acid sulfate waters in the presence of Acidithiobacillus ferrooxidans (A. ferrooxidans, an especially important chemolithoautotroph for bioleaching and desulfurization of coal). In this study, we observed the morphology and elemental composition of cells in stationary phase and examined the dynamic variation of iron oxyhydroxides produced in cultures of A. ferrooxidans incubated in modified 9K medium initially including 0.15 M of ferrous iron, in the absence/presence of 0.2 M of chloride (NaCl/ FeCl2). Results showed that chloride acclimation had little effect on cellular morphology and elemental uptake that was mainly related to culture medium. Furthermore, schwertmannite with the typical morphology of aggregated spheres covered by some “pincushions” was precipitated first in bacterial cultures in the favorable pH range of 2.9 ( 0.1 to 2.6 ( 0.1. Some of schwertmannite could be transformed to lozenge-shaped jarosite, due to a successively decreasing of pH values. However, the jarosite transformation represented a lag period of 5 and 4 days in the chloride-rich cultures with sulfate at a low level, compared to the cultures with sulfate at a high level, which could be attributed to the influence of sulfate requirement and chloride acclimation.

Introduction Acidithiobacillus ferrooxidans, an acidophilic chemolithoautotroph, can use ferrous iron, reduced sulfur species, or metal sulfides as energy sources (1, 2). These abilities make this bacterium an especially interesting microorganism in specific areas of applications such as the extraction or recovery of metals from sulfuric ores and sludge, the desulfurization of coal, and removal of hydrogen sulfide from gaseous effluents (3). In the above processes, especially bioleaching of pyriterich ores, bacterial pyrite oxidation leads to production of the iron- and sulfate-rich acid mine drainage (AMD). The mixing of AMD with other types of water results in deposition of abundant iron oxyhydroxides in natural environments (4-7). It has been demonstrated that iron oxyhydroxides can effectively scavenge heavy metals by adsorption, coprecipitation, and structural incorporation/substitution. The capacity of iron oxyhydroxides for scavenging metals is strongly correlated with their morphology, size, and crystallinity (5-8). * Corresponding author phone/fax: +86-514-8797 5219; e-mail: [email protected]. 10.1021/es1019146

 2011 American Chemical Society

Published on Web 12/03/2010

Schwertmannite, a ubiquitous mineral present in iron oxyhydroxides, is the first Fe(III) mineral phase to precipitate in iron-rich acid sulfate waters with the favorable pH range of 2.5-4.5, while the lower and higher pH values facilitate the formation of jarosite and goethite/ferrihydrite, respectively (9-11). Schwertmannite as an iron oxyhydroxysulfate has an especial tunnel structure occupied by SO42-, which favors incorporation of toxic oxyanions (12-14). This mineral has a variable chemical formula Fe8O8(OH)8-2x(SO4)x · nH2O (1 e x e 1.86) with a Fe/S mole ratio range of 4.3-8 and a distinct “pincushion” morphology (12-14). In addition, during cultivation of A. ferrooxidans, schwertmannite is easily transformed to jarosite (another iron oxyhydroxysulfate, MFe3(SO4)2(OH)6, where M could be Na+, K+, NH4+, or H3O+) in the pH range of 1.5-2.5 (15, 16). However, it has been demonstrated that the jarosite transformation could be retarded due to occurrence of some anions in bacterial growth medium (11, 17). A. ferrooxidans is well-known for its sensitivity to various substances such as inorganic anions, organic compounds, and heavy metals present in bacterial growth medium (18, 19). It has been confirmed that sulfate is required during bacterially catalyzed ferrous oxidation, while chloride or nitrate can inhibit ferrous biooxidation as well as bacterial growth (19, 20). Gu and Wong (19) found that the presence of 0.1 M chloride started to have an inhibitory effect on ferrous oxidation, whereas nitrate with the same concentration completely restrained bacterial growth. It was also documented that acclimation in 0.2 M of chloride not only enabled A. ferrooxidans to be capable of oxidizing ferrous iron but also received the maximum cell density (21). More recently, much attention has been focused on the correlation between iron mineral formation and bacterial growth medium containing chloride/sulfate. It has been demonstrated by Burton et al. (22-24) that the cycling of Fe and As is often linked to the formation and fate of schwertmannite in ironrich acid sulfate waters in the presence of chloride. Moreover, Xiong et al. reported that sulfate inhibited drastically akagane´ite formation but facilitated schwertmannite occurrence in sulfate- and chloride-rich ferrous solutions with A. ferrooxidans (25). However, little information is available on dynamic variation of iron minerals induced by A. ferrooxidans in chloride-rich culture medium. In order to better understand the correlation between iron oxyhydroxides as well as bacterial cells and culture medium, in this study, we examine the morphology and elemental composition of cells in stationary phase and the development of iron oxyhydroxides produced in cultures initially with an identical ferrous concentration, in the absence/presence of chloride.

Materials and Methods Microorganism, Medium, and Growth Conditions. A. ferrooxidans strain LX5 (CGMCC No. 0727) was cultured in modified 9K medium (more details in the Supporting Information). Five percent (v/v) of A. ferrooxidans cultures was inoculated into the medium and incubated aerobically at 28 °C for about 3 days. Cultivation of A. ferrooxidans under Various Chloride Concentrations. The presence of 0.2 M Cl- as NaCl is considered to have no substantial influence on growth of A. ferrooxidans (Supporting Information Figure S1). In comparison with NaCl, FeCl2 not only can provide Cl- but also can act as energy source. To uncover the effect of chloride (FeCl2) on bacterial growth, the experiments were preformed in triplicate with 100 mL of modified 9K medium (pH 2.9) containing 0, 0.1, VOL. 45, NO. 1, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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TABLE 1. EDS Analyses of Iron Oxyhydroxides Produced during Cultivation of A. ferrooxidansd elemental composition (wt %) -

2-

treatment Cl (M) SO4 A B C A B C C

no 0.2b 0.2c

(M) time (days)

0.15 0.15 0.05

3 3 3 5 5 5 7

mineral Sch Sch Sch Sch Sch Sch Sch

+ Jt + Jt + Jt + Jt + Jt

Fe

S

K

37.9 56.2 54.8 48.0 44.2 54.4 54.5

5.74 4.69 4.14 7.20 6.77 4.30 5.18

0.97 0.22 0.00 1.11 1.32 0.00 0.45

total Fe/Sa Fe/S for Sch chemical formula for Sch 3.77 6.85 7.56 3.81 3.73 7.23 6.01

4.64 7.30 7.56 4.59 4.78 7.23 6.76

Fe8O8(OH)4.56(SO4)1.72 Fe8O8(OH)5.8(SO4)1.1 Fe8O8(OH)5.88(SO4)1.06 Fe8O8(OH)4.52(SO4)1.74 Fe8O8(OH)4.66(SO4)1.67 Fe8O8(OH)5.78(SO4)1.11 Fe8O8(OH)5.64(SO4)1.18

Fe/S mole ratio. b 0.2 M Cl- added as NaCl. c 0.2 M Cl- added as FeCl2. d Sch, schwertmannite; Jt, jarosite. The ideal formula for Sch: Fe8O8(OH)6SO4, Fe: 57.8%; S: 4.13%; Fe/S: 8. The ideal formula for Jt: KFe3(SO4)2(OH)6 with a K:Fe:S mole ratio of 1:3:2. a

FIGURE 1. (a) Percent Fe2+ oxidized during cultivation of A. ferrooxidans in modified 9K medium with different concentrations of chloride as FeCl2 and (b) percent Fe2+ oxidized (solid line) and the pH value (dash line) during 7-day cultivation of A. ferrooxidans (A, B, and C denote treatments displayed in Table 1).

FIGURE 2. (a) FESEM images for the morphology of cells in stationary phase and (b) EDS spectra (their correlative FESEM images not shown) of the examined cells (A, B, and C denote treatments displayed in Table 1). 0.2, 0.25, or 0.3 M of Cl- (FeCl2, instead of equal moles of FeSO4 pretreatment of samples for Fe2+ determination and cell included natively in modified 9K medium) as well as 5% (v/v) enumeration were detailed in the Supporting Information. inoculums of A. ferrooxidans cultures. All flasks were shaken at Finally, the two cultivations with 0.2 M of chloride as NaCl/ 180 rpm and 28 °C in a horizontal shaker. Collection and FeCl2 were selected to carry out further experiments. 236

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coated with gold prior to examination. Local morphology of iron minerals was further observed by a Philips Tecnai-12 transmission electron microscope (TEM, the prepared samples were deposited on carbon-copper grids). For the EDS analysis (the energy dispersive spectrometer associated with FESEM), iron precipitates or cell pellets were suspended in a small quantity of distilled water and fixed on Al stubs with electric adhesive tape, and the dry samples were not sputter-coated with gold, prior to examination.

Results and Discussion

FIGURE 3. (a) XRD patterns and (b) FTIR spectra of iron precipitates produced during cultivation of A. ferrooxidans (A, B, and C denote treatments displayed in Table 1). Cultivation of A. ferrooxidans in the Absence/Presence of Chloride. Three 7-day culture experiments (i.e., Treatments A, B and C, see Table 1) were preformed in triplicate with 100 mL of modified 9K medium (pH 2.9 ( 0.1) without/with 0.2 M of Cl- as NaCl/FeCl2, as well as containing 0.15 M of Fe2+ as FeSO4/FeCl2 and 5% (v/v) inoculums of A. ferrooxidans cultures. All flasks were shaken at 180 rpm and 28 °C in a horizontal shaker. During incubation, the culture pH values were monitored (using a pHS-3C model digital pH-meter), and all samples were collected at given intervals (see Figure 1b). Collection and pretreatment of samples for Fe2+ determination, preparation of iron precipitate and cell samples for characterization, and measurement of cell growth were detailed in the Supporting Information. Methods for Analysis and Characterization. The phases of iron precipitates were determined by powder X-ray diffraction (XRD), using a German Bruker AXS D8 ADVANCE Model diffractometer with a Cu target (40 kV and 200 mA). The FTIR spectra were taken on a Nicolet 740 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. Sample morphology was examined by a Hitachi S-4800 field emission-scanning electron microscope (FESEM, operated at 15.0 kV accelerating voltage under a high vacuum). The fresh iron precipitates dispersed in distilled water by ultrasonic vibration and cells pretreated by cytochemical methods (see theSupporting Information) were fixed on Al stubs, dried in air at room temperature, and then sputter-

Effect of Chloride on Growth of A. ferrooxidans Cultures. The dynamic variations of percent Fe(II) oxidation were displayed in Figure 1a. It was observed that almost all ferrous iron were oxidized by A. ferrooxidans in the three cultivations with 0, 0.1, and 0.2 M of chloride after 3 days, but only 85% and 55% of ferrous iron were oxidized in the other two cultivations with 0.25 and 0.3 M of chloride after 5 days, respectively. The enumeration of viable bacteria showed that there were ∼108, ∼106, and ∼104 cells mL-1 in the corresponding cultures with chloride of 0-0.2, 0.25, and 0.3 M, after 5 days of incubation completed. Obviously, the cultures with 0.2 M of chloride as FeCl2 were able to oxidize all ferrous iron to ferric iron and also received the maximum cell density (∼108 cells mL-1), which was consistent with the results for acclimation of A. ferrooxidans in 0.2 M chloride as NaCl (21), Variation of Culture pH, Percent Fe(II) Oxidation, and Cell Number during 7-day Cultivation. After about 2 or 3 days of incubation, bacterial exponential growth phase was end (according to all ferrous iron oxidized by A. ferrooxidans revealed in Figure 1b), which was further confirmed by the results of cell growth (see Supporting Information Figure S2). During the exponential phase, cell number, culture pH, and percent Fe(II) oxidation rapidly varied with the increase of incubation time. Percent Fe(II) oxidation in three cultivation treatments increased drastically to 51-61% during the first 24 h and then reached the corresponding values: 99% (A), 65% (B), and 82% (C) after 2 days. This indicated that the reduction of sulfate in treatment C should have no effect on ferrous iron oxidation, which was consistent with the result reported by Harahuc et al. (26). The differences in percent Fe(II) oxidation could be attributed to chloride acclimation of A. ferrooxidans (19, 21). After 3 days, percent Fe(II) oxidation in all treatments reached the values of 95-100%. Furthermore, the pH values of cultures were observed to decrease continuously from initial 2.9 ( 0.1 to 2.0 ( 0.1 within the first 3 days. Cells in the chloride-rich cultures (that received the maximum cell density of about 5.6 × 108 cells mL-1) reached the stationary phase after 3 days, so the cells in all cultures were harvested for the examination of morphology and elemental composition. Morphology and Elemental Composition of Cells in Stationary Phase. In Figure 2a, it was observed that the cells had a similar morphology of short rod holding a length of 1.1 ( 0.1 µm with an axial ratio of 2.8 ( 0.2 µm in the presence and absence of chloride. In addition, the EDS spectra (Figure 2b, their correlative FESEM images not shown) revealed the presence of P, S, and Fe in the examined cells from all treatments. The reasons were that P and S were required elements for bacterial growth, and Fe could be complexed to organic membranes (27, 28). Also, Mg and K were observed to be present in some examined cells from all treatments. However, sometime they were unexamined in other cells by EDS (data not shown). This could be due to Mg and K as trace elements occurrence in bacterial nutrition. Moreover, a trace amount of Si (that is excluded in culture medium) occasionally examined in some cells by EDS was attributed to the glass flask used in experiment (28). In summary, VOL. 45, NO. 1, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. The images for dynamic morphologies of iron precipitate samples. The letters denote treatments displayed in Table 1, except that T denotes TEM image. The numbers denote collection time of samples (after 1-7 days of incubation). The bars in the FESEM images represent 2 µm. chloride acclimation had little effect on cellular morphology and elemental uptake that was mainly related to culture medium. Iron Oxyhydroxides Produced in Exponential Phase of Bacterial Growth. During bacterial exponential growth phase, the rapid decrease of pH values in all cultures (with an initial pH of 2.9 ( 0.1) was due to ferrous oxidation by A. ferrooxidans and subsequent hydrolysis of the produced ferric iron (29). As is well-known, A. ferrooxidans can rapidly oxidize ferrous iron to ferric iron to obtain energy source for bacterial growth, where the mechanism proposed involves the oxidation of ferrous iron outside the cell membrane at pH of down 3 (reaction 1), under the action of main Fe2+-cytochrome c oxidoreductase and rusticyanin (30). A. ferrooxidans

4Fe2+ + O2 + 4H+ 98 4Fe3+ + 2H2O

(1)

In reaction 1, there is consumption of hydrogen ions, which can be rapidly supplied by subsequent hydrolysis of the ferric iron (reaction 2). Fe3+ + 3H2O S Fe(OH)3 + 3H+

(2)

The ferrous biooxidation and ferric hydrolysis corporately resulted in the decrease of pH values from initial 2.9 ( 0.1 to 2.0 ( 0.1 in all cultures. The pH range facilitated precipitation of schwertmannite or jarosite in cultures. During the first 24 h of cultivation, the only schwertmannite was identified by XRD patterns to be present in 1-day precipitates from all cultures (Herein, only the experimental data for treatment A were given in this paper, as exemplified by Figures 3 and 4). This result coincided with those demonstrated by Burton et al. (10, 11) that schwertmannite was facilitated to precipitate first in iron- and sulfaterich acid waters with a favorable pH range of 2.5-4.5. Only schwermannite occurrence in cultures was because of variation of pH value in the range of initial 2.9 ( 0.1 to 2.6 238

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( 0.1 (Figure 1b). It was also due to the case that, in the sulfate-rich cultures of A. ferrooxidans, the relatively abundant species of Fe3+-OH and Fe3+-SO4 kinetically facilitated initial precipitation of schwertmannite (11, 31, 32). The overall reaction is described as 8Fe3+ + xSO24 + (16-2x)H2O S Fe8O8(OH)8-2x(SO4)x + (24-2x)H+ (3) Obviously, not only the pH value of culture but also the requirement for sulfate is important to chemolithotrophic iron oxidation by A. ferrooxidans and precipitation of iron oxyhydroxides (1, 18). The schwertmannite was further confirmed by the correlative FTIR spectra (Figure 3b). The FTIR revealed the vibrational modes of two O-H-SO4 hydrogen bonds at 681 and 842 cm-1 (representative characteristics of SO4-containing schwertmannite) and the bands at about 1122, 981, and 605 cm-1 that were typically caused by SO4 (12). The schwertmannite had a typical morphology of aggregated spheres (1-2 µm in diameter) covered by some “pincushions”, as shown in images A1 and T-A1 (Figure 4), in good agreement with the biogenic schwertmannite formed in the surface layer of acid sediment, or in FeSO4-solutions with NH4+ of down 11.4 mM (16, 33). During the next 2 days of cultivation, the mixtures of schwertmannite and jarosite were observed in 3-day precipitates from treatments A and B and 2-day precipitates from treatment A, according to XRD results. Especially the 3-day precipitates from treatment A, some characteristic peaks of jarosite could be clearly observed in the XRD pattern (Figure 3a), and the FTIR spectrum represented three sequential bands for jarosite at 1184, 1085, and 1003 cm-1, which were absent in the other FTIR spectra (Figure 3b). The lozenge-shaped jarosite particles (with a length of 1 ( 0.2 µm, a width of 0.5 ( 0.1 µm, and a height of 0.3 ( 0.1 µm) was observed to be present in surface of schwertmannite

spheres (which aggregation extent increased with the increase of incubation time), as shown in images A3, T-A3, and B3 in Figure 4. Obviously, the occurrence of jarosite in the chloride-rich cultures was one day later than in the control cultures, although the sulfate level and pH value were almost the same. It could be due to chloride acclimation resulting in the lower level of ferric iron present in the cultures. The jarosite formation in the cultures with 0.15 M of sulfate was a result of the pH values decreasing from 2.6 to 2.1 or 2.0 (Figure 1b). It was also reported that pH values of down 2.5 facilitated the transformation of jarosite from schwertmannite in AMD and acid coastal lowland soil (10, 11, 17, 33). However, in the cultures with 0.05 M of sulfate, although the final pH value was 1.9, the jarosite occurrence was unobserved during the exponential phase. This could be attributed to the presence of sulfate at a low level in cultures restricting the jarosite formation. Furthermore, the EDS analyses for 3-day precipitates were exhibited in Table 1. The contents (wt %) of K (an important structural element of jarosite) in the examined locations of samples were 0.97 (A), 0.22 (B), and 0 (C). According to the K contents and total Fe/S mole ratios (3.77, 6.85, and 7.56 for treatments A, B, and C, respectively), the Fe/S mole ratios for schwertmannite in 3-day precipitates analyzed with EDS were 4.64 (A), 7.30 (B), and 7.56 (C). The corresponding chemical formula for schwertmannite could be expressed as Fe8O8(OH)4.56(SO4)1.72, Fe8O8(OH)5.8(SO4)1.1, and Fe8O8(OH)5.88(SO4)1.06. Iron Oxyhydroxides Developed in Stationary Phase of Bacterial Growth. During the last 4 days of cultivation, pH values of cultures slowly decreased from 2.0 ( 0.1 to a constant value of 1.8 ( 0.1, and ferric iron was the only iron species in all cultures (Figure 1b), which promoted jarosite formation, as revealed by the XRD and FTIR data for the correlative precipitates (Figure 3), and their morphologies (Figure 4). In the cultures with 0.15 M of sulfate, the number of jarosite particles significantly increased, and their sizes hardly changed with the increase of cultivation time. In contrast, in the cultures with 0.05 M of sulfate, jarosite occurrence could be observed in 6-day precipitates (which represented a lag period of 5 and 4 days compared to treatments A and B, respectively), and the number of jarosite particles in 7-day precipitates increased distinctly. In addition, the EDS analyses for 5-day precipitates (Table 1) revealed that the contents (wt %) of K in examined locations of samples were 1.11 (A), 1.32 (B), and 0 (C). Also, the K content was 0.45% for the analyzed 7-day precipitates (C). The examined K contents were lower than those in other artificial iron minerals mainly containing jarosite (15, 16). According to the K contents and total Fe/S mole ratios (3.81, 3.73, and 7.23 for treatments A, B, and C, respectively), the Fe/S mole ratios for schwertmannite in 5-day precipitates analyzed with EDS were 4.59 (A), 4.78 (B), and 7.23 (C). The corresponding chemical formula for schwertmannite could be expressed as Fe8O8(OH)4.52(SO4)1.74, Fe8O8(OH)4.66(SO4)1.67, and Fe8O8(OH)5.78(SO4)1.1. Also, for schwertmannite in the analyzed 7-day precipitates (C), there was a formula Fe8O8(OH)5.64(SO4)1.18 with a Fe/S mole ratio of 6.76. Element Na was not examined in the analyzed precipitates from the treatment with 0.2 M chloride as NaCl, showing absence of Na-jarosite in the mixtures. It was consistent with the results demonstrated by Gramp et al. (34) that the transformation of Na-jarosite from schwertmannite was more difficult than K-jarosite. The jarosite formation was markedly retarded in the cultures with 0.05 M of sulfate, which could be interpreted as representation of the inhibitory effects of sulfate at a low level on the transformation. Moreover, chloride acclimation could indirectly affect precipitation of

schwertmannite and jarosite through its effects on bacterial growth (18, 19). Environmental Implications. The study results can contribute to understanding the formation and fate of natural iron oxyhydroxides associated with bacterially catalyzed oxidation and growth conditions. Moreover, these results are especially promising and noteworthy for minimizing jarosite formation during coal desulfurization and bleaching as jarosite is a major issue in this industry. It is also a convenient and economic approach to obtain pure schwertmannite (an excellent adsorbent for removal of heavy metals) directly from bacterial metabolic byproducts by using an adapted level of FeCl2 as energy source for bacterial growth.

Acknowledgments The research was supported jointly by National Natural Science Foundations of China (20773106 and 40902018). We thank Associate Editor Michelle M. Scherer and all anonymous reviewers for their constructive comments on this manuscript.

Supporting Information Available Source and growth medium of Acidithiobacillus ferrooxidans; experimental methods for sample preparation and measurement of cell number; available data from the literature (Figure S1); and cell growth curve (Figure S2). This material is available free of charge via the Internet at http://pubs.acs.org.

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