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Humic acid promotes arsenopyrite bio-oxidation and arsenic immobilization
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Humic acid promotes arsenopyrite bio-oxidation and arsenic immobilization Duo-rui Zhanga,1, Hong-rui Chena,1, Jin-lan Xiaa,⁎, Zhen-yuan Niea, Xiao-lu Fana, Hong-chang Liua, Lei Zhengb, Li-juan Zhangc, Hong-ying Yangd a
Key Lab of Biometallurgy of Ministry of Education of China, School of Minerals Processing and Bioengineering, Central South University, Changsha 410083, China Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China Shanghai Synchrotron Radiation Facility, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai 201204, China d School of Metallurgy, Northeastern University, Shenyang 110819, China b c
GRAPHICAL ABSTRACT
ARTICLE INFO
ABSTRACT
Editor: R. Debora
The bio-oxidative dissolution of arsenopyrite, the most severe arsenic contamination source, can be mediated by organic substances, but pertinent studies on this subject are scarce. In this study, the bio-oxidative dissolution of arsenopyrite by Sulfobacillus thermosulfidooxidans and arsenic immobilization were evaluated in the presence of humic acid (HA). The mineral dissolution was monitored through analyses of the parameters in solution, phase and element speciation transformations on the mineral surface, and arsenic immobilization on the surfaces of cells and jarosites-HA. The results show that the presence of HA enhances the dissolution of arsenopyrite, e.g., 7.1% of arsenopyrite was in the residue after 12 d of bio-oxidation compared to 19.3% in the absence of HA. Meanwhile, the presence of HA led to changes of the fates of As and Fe and no accumulation of elemental sulfur (S0) or ferric arsenate on the mineral surface. Moreover, a flocculent porous structure was formed on the surfaces of both microbial cells and jarosites, on which a large amount of arsenic was adsorbed. These results clearly indicate that HA can simultaneously promote the dissolution of arsenopyrite and arsenic immobilization, which may be significant for bioleaching of arsenopyrite-bearing contaminated sites.
Keywords: Arsenopyrite Bio-oxidation Humic acid Speciation transformation Arsenic immobilization
Corresponding author. E-mail address: [email protected] (J.-l. Xia). 1 These two authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.jhazmat.2019.121359 Received 17 July 2019; Received in revised form 15 September 2019; Accepted 28 September 2019 0304-3894/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: Duo-rui Zhang, et al., Journal of Hazardous Materials, https://doi.org/10.1016/j.jhazmat.2019.121359
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1. Introduction
As, 44.09; Fe, 33.52; S, 19.06; O, 2.25; Si, 0.34; Al, 0.21; Cu, 0.23; Pb, 0.12; Zn, 0.08; Ca, 0.11; and Ag, 0.01. The mineral was mainly composed by arsenopyrite according to the result of XRD (Fig. S1). The mineral was ground and passed through −200 + 400 mesh screens to achieve particles ranging in size from 38 to 75 μm.
Arsenic (As) is a toxic element of significant environmental concern due to its leaching from hazardous wastes and geological minerals. Arsenopyrite (FeAsS) is the most common As-bearing sulfide mineral in many ore deposits (Dave et al., 2008). Arsenopyrite is usually stable under a reducing environment, but under oxidizing conditions, it is easily decomposed with the release of a considerable amount of sulfate (SO42−), arsenite (AsO33-) and arsenate (AsO43-) to the solution, thereby contributing to the generation of hazardous acid mine drainage (AMD) (Corkhill and Vaughan, 2009; Wang et al., 2018; Coussy et al., 2011). The chemical and biological oxidations of arsenopyrite have been widely studied (Mckibben et al., 2008; Cornejo-Garrido et al., 2008; Yu et al., 2007; Corkhill et al., 2008). It has been found that the toxicity and fate of inorganic arsenic is highly dependent on arsenic speciation, which can be influenced by environmental parameters, including pH, redox potential (ORP), metal ions, microorganisms, and dissolved organic matter (DOM) (Yu et al., 2007; Sharma and Sohn, 2009; Zhang et al., 2015a, 2015b; Liu and Cai, 2013). Among these parameters, DOM is one of the important complexing agents that can change the physical and chemical properties of a mineral surface and critically affect the environmental behavior and distribution of iron and arsenic (Redman et al., 2002; Alsidcheikh et al., 2015). Humic acid (HA) is a common DOM in nature and can be an effective sorbent for toxic metal ions due to the amino, carboxyl, phenolic, and sulfhydryl moieties that can act as the potential binding sites for toxic metal ions (Celebi et al., 2009; Rashid et al., 2018), which means that HA may influence the fate of arsenic species during biooxidation of arsenopyrite. On the other hand, the arsenopyrite biooxidation process involves complex biochemical reactions and secondary products, such as elemental sulfur (S0), jarosite, orpiment, and ferric arsenate/scorodite (Corkhill et al., 2008; Márquez et al., 2012; Ramírez-Aldaba et al., 2016), which may influence the dissolution of arsenopyrite and the arsenic fate. However, no pertinent studies have been reported to date. In the present study, the influence of HA on the dissolution of arsenopyrite and the fate of arsenic was addressed, during which the biooxidation of arsenopyrite accompanied the transformation of Fe/S/As and the effect of the products on the immobilization of As were simultaneously investigated. This study helps to elucidate the bio-oxidation of arsenopyrite with simultaneous arsenic immobilization.
2.3. Experimental procedure The cultures were carried out in 250-mL Erlenmeyer flasks containing 100 mL sterilized basal medium and 1 g arsenopyrite. The initial pH of the medium was adjusted with 1 M sulfuric acid to pH 2.0 ± 0.05. The initial inoculated cell density was 4 × 107 cells/mL. The cultures were incubated in an incubator shaker (ZHTY-70S) at 180 rpm and 45 °C. The experiments were conducted with different concentrations of HA (HA-Na) (w/v, mg/L) (0, 20, 40, 60, 80, and 100), and no HA was added to the control. Meanwhile, abiotic controls were also performed under the same conditions. All experiments were performed in triplicate under the same conditions. 2.4. Analysis methods Solution samples were collected every 1–2 d for monitoring cell density, concentrations of sulfate ions and soluble Fe and As species, pH and ORP values. The cell density was determined by a blood corpuscle counter (XB-K-25). The concentration of sulfate ions ([SO42−]aq) was measured using a barium sulfate turbidimetric colorimetric method (Zhu et al., 2011). The concentrations of total Fe ([FeT]aq) and Fe3+ ([Fe3+]aq) were determined by 5-sulfosalicylic acid spectrophotometry (Karamanev et al., 2002). The concentration of total As ([AsT]aq) was measured by inductively coupled plasma-atomic emission spectroscopy (ICP-AES) (IRIS Intrepid II XSP, Thermo Fisher, USA). The concentration of arsenite ([As(III)]aq) was analyzed by atomic fluorescence spectrometer (AFS) (PS Analytical Ltd, Kent, U.K.). The pH and ORP values were measured using a Thermo Scientific Orion DUAL STARTM pH/ISE meter with a pH meter and a platinum (Pt) electrode with a calomel electrode (Hg/HgCl) as a reference. The surface morphology of the arsenopyrite was observed by scanning electron microscopy (SEM) coupled with an energy dispersive spectroscopy (EDS) facility (Nova™ NanoSEM 230, FEI, USA). Fourier transform infrared spectroscopy (FT-IR) analysis was performed with a Fourier transform spectrometer (Nexus 670, Nicolet, USA). X-ray diffraction (XRD) analysis was conducted with CuKα radiation (40 kV/ 250 mA) in a RINT2000 vertical goniometer. The scanning range was from 10° to 80° 2θ with a step of 0.02° and a dwell time of 4 s. The Fe, S and As speciation transformations on the mineral surfaces were analyzed by Fe L-edge and S K-edge XANES spectroscopy, and Xray photoelectron spectroscopy (XPS), respectively. The Fe L-edge and S K-edge XANES analyses were carried out on 4B7B beamline and 4B7A beamline, respectively, at the Beijing Synchrotron Radiation Facility, Beijing, China. The Fe L-edge XANES spectra data were recorded in total electron yield (TEY) mode at the step widths of 0.5 eV from 690 to 700 eV and 0.1 eV from 700 to 928 eV. The S K-edge XANES spectra data were recorded in the fluorescence mode at ambient temperature and scanned at a step width of 0.2 eV between 2460 and 2510 eV. The spectra were normalized to the maximum of the absorption jump (IdeEktessabi et al., 2004), and fitted for their linear combination fits (LCF) using the standard spectra with the IFEFFIT program (Ravel and Newville, 2010). The XPS spectra of the reacted arsenopyrite surfaces were collected using a Thermo ESCALAB 250XI X-ray photoelectron spectrometer equipped with a monochromatized Al Kα X-ray source (15 KeV) and a hemispherical analyzer fitted with a five-channeltron multidetection system. All photoelectron binding energies (BE) were referenced to C1s adventitious contamination peaks set at 284.6 eV BE. The distribution mapping for arsenic in a single cell was detected by scanning transmission X-ray microscopy (STXM) based on the dualenergy contrast image analysis of the near-edge X-ray absorption fine
2. Materials and methods 2.1. Strain and culture conditions The strain Sulfobacillus thermosulfidooxidans YN-22 (Accession number of 16S rRNA in GeneBank: DQ650351) was preserved at the Key Laboratory of Biometallurgy of Ministry of Education of China, Changsha, China. S. thermosulfidooxidans is widespread in sulfur-rich, acidic environments and possesses higher sulfur and iron oxidation activity at elevated temperatures compared with mesophilic bacteria (Pina et al., 2010; Dopson and Lindström, 2004). The basal medium for cell cultivation was comprised of the following components (in g/L): (NH4)2SO4, 3.0; MgSO4, 0.5; K2HPO4, 0.5; KCl, 0.1; Ca(NO3)2, 0.01 and yeast extracts 0.2. For domestication, S. thermosulfidooxidans was cultured in basal medium supplemented with 10 g/L arsenopyrite as the energy source. 2.2. Mineral sample The mineral sample used in this study were provided by the School of Minerals Processing and Bioengineering, Central South University, Changsha, China. The elemental composition of the mineral analyzed by X-ray fluorescence spectroscopy (XRF, Axios mAX) was (in wt.%): 2
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Fig. 1. Solution parameters during bio-oxidation of arsenopyrite by S. thermosulfidooxidans and in the sterile controls. Changes of cell density (a), [SO42−] (b), [FeT] (c), [Fe3+] (d), [AsT] (e), [As(III)] (f), pH (g) and ORP (h).
3
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Fig. 2. SEM images of arsenopyrite residues bio-oxidized in the absence of HA at days 4 (a) and 12 (c), in the presence of 60 mg/L HA at days 4 (e), 12 (g), and in the sterile controls reacted for 12 d in the absence (d) and presence of 60 mg/L HA (h). The EDS spectra in (b) and (f) correspond to the regions “A” and “B” in (a) and (e) as indicated by red rectangles.
Then, the precipitates were harvested with a 0.45-μm filter paper, dried and characterized by SEM and XRD. 2.6. Adsorption experiments The As(III) and As(V) solutions (100 mg/L, which is lower than the tolerance limit of S. thermosulfidooxidans, 3 g/L, see Fig. S2) were prepared by dissolving desired the amounts of Na3AsO3 and Na2HAsO4 in deionized water. The experiments for arsenic adsorption kinetics were conducted by adding 0.1 g of sorbent to 50 mL centrifuge tubes each containing 20 mL solution consisting of 0.01 M NaNO3 as the background electrolyte and 60 mg/L of As(III) and As(V). The solution pH was adjusted to 2.0 ± 0.05, and the centrifuge tubes were then placed in an incubator shaker at 180 rpm and 45 °C. Each experimental treatment was conducted in triplicate under the same conditions. The sampled suspension was directly filtered through a 0.45-μm filter paper, and then the arsenic concentrations were determined. The adsorbed-As (III) and As(V) in solid phase (Cs) were determined by mass balance using Eq. (1).
Fig. 3. FT-IR spectra of arsenopyrite residues bio-oxidized in the absence and presence of HA, in comparison with the spectra of HA before and after interaction with As(V) and Fe(III).
Cs = structure (NEXAFS) of arsenic at BL08U1A at the Shanghai Synchrotron Radiation Facility, Shanghai, China. NaAsO2 (As(III)) and Na2AsO4 (As (V)) were chosen as the references for the NEXAFS analyses of arsenic. Other parameters of the equipment and the procedures of measurement were the same as that of Zhu and co-authors (Zhu et al., 2014).
Ci
Ceq
M/V
(1)
where Ci and Ceq are the initial and equilibrium arsenic concentrations (mg/L), M is the mass of sorbent (g), and V is the volume of the solution (L). The isotherm assays were conducted with a sorbent load of 0.5 g/ 100 mL at pH 2.0 and initial As(III) and As(V) concentrations ranging from 5 to 100 mg/L. All flasks were shaken continuously at 180 rpm for 4 d to maximize the arsenic retention. Then, the samples were filtered through a 0.45-μm filter paper and the suspensions were monitored for As concentrations. The solid phases were characterized using XRD and SEM-EDS. These results were used for estimating the amount of arsenic adsorbed by the jarosites-HA complexes in the acidic biotic system.
2.5. Preparation of biogenic minerals The jarosites (a mixture of ammonium and potassium jarosite) were biosynthesized using S. thermosulfidooxidans grown in Norris medium (Norris and Barr, 1985) (g/L) (MgSO4, 0.5; (NH4)2SO4, 0.4 and K2HPO4, 0.2), supplemented with FeSO4∙7H2O at a final concentration of Fe2+ equal to 50 mM. Then, 60 mg/L HA was added. The reaction systems were incubated at 180 rpm and 45 °C in an incubator shaker for 7 d. 4
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Fig. 4. XRD patterns of arsenopyrite residues bio-oxidized at different times in the absence (a) and presence of (b) 60 mg/L HA.
Fig. 5. XPS spectra of the original arsenopyrite. (a) As (3d5/2), (b) S (2p3/2).
3. Results and discussion
presence of 20–60 mg/L HA, while it decreased with the further addition of more HA (80, 100 mg/L). These results indicate that the presence of a suitable concentration of HA (≤60 mg/L) promoted the biooxidation of sulfur. The further addition of more HA may block the contact of cells with the mineral surface and thus lead to a decrease in [SO42−], as well as in cell growth (Xu et al., 2017). Fig. 1c shows that in the presence of HA, the [FeT]aq was considerably lower than that in the absence of HA. By comparing the changes of the [Fe3+], it can be found that the dissolved Fe was dominated by Fe3+ (Fig. 1d), which may be the result of the rapid biooxidation of Fe2+ (Eq. (2)), and the decrease of [Fe3+]aq at the later stage confirmed the formation of precipitates of ferric arsenate and jarosites (Eqs. (3) and (4)). In contrast, for the sterile controls, the [FeT]aq increased slightly, and Fe existed mainly in the form of Fe2+.
3.1. Effect of HA concentration on the solution parameters The solution parameters in terms of cell density, [SO42−], [FeT], [Fe3+], [AsT], [As(III)], pH and ORP of the sterile control experiments and the bio-oxidation of arsenopyrite by S. thermosulfidooxidans at 45 °C in the presence of various concentration of HA (0–100 mg/L) are shown in Fig. 1. Fig. 1a shows that the cells grew rapidly during the first 2 d, reached a maximum at days 3 or 4, and then decreased. The growth rate increased in the presence of 20–60 mg/L HA, although it decreased with the further addition of more HA (80, 100 mg/L). No notable increase in growth rate of S. thermosulfidooxidans growing on S0 + HA in the basal medium, indicating that HA cannot be utilized as the organic carbon (Fig. S3). Fig. 1b shows that the [SO42−] in the biotic experiments, which was considerably higher than in the abiotic ones, also increased in the
4Fe2 + + 4H+ + O2
H3 AsO4 + Fe3+ 5
Microbial
4Fe3 + + 2H2 O
FeAsO4 + 3H+
(2) (3)
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Fig. 6. XPS spectra of the surface arsenic of arsenopyrite residues bio-oxidized in the absence of HA at days 2 (a), 4 (b), 8 (c), 12 (d), and in the presence 60 mg/L HA at days 2 (e), 4 (f), 8 (g), 12 (h), and in the sterile controls reacted for 12 d in the absence (i) and presence of (j) 60 mg/L HA.
M+ + 3Fe3 + + 2SO4 2 + 6H2 O
MFe3 (SO4) 2 (OH)6 + 6H+
(4)
H3 AsO3 + H2 O+ 2Fe3 +
where M is a monovalent cation, such as NH4+, K+, Na+ or H3O+. Fig. 1e shows that for the bio-oxidation experiments in the presence of HA, the [AsT]aq was always lower than that in the biotic system with no HA added, and the more HA was added, the more [AsT]aq was reduced. Fig. 1f shows that for the bio-oxidation experiments conducted in 20, 40, 60, 80, and 100 mg/L HA, the ratios of [As(III)]aq/[AsT]aq on day 12 were 56.8%, 60.4%, 61.7%, 62.3%, and 60.4%, respectively; and for the bio-oxidation experiment in the absence of HA, the ratio of [As(III)]aq/[AsT]aq on day 12 was 49.5%. This result indicates that the addition of HA is favorable for the accumulation of As(III). For the sterile controls in both the presence and absence of HA, the aqueous As mainly existed as As(III). Fig. 1g and h show that in the presence of HA, the pH values decreased more slowly and the ORP values were always lower, than in the absence of HA. For the sterile controls in the presence of HA, both the pH and ORP values were only slightly lower than that in the absence of HA. A previous study has demonstrated that Fe and As can form complexes with ligands or trace elements of HA (Sharma et al., 2010). These reactions reduced the concentrations of Fe and As in the solution, then led to a slower decline in pH and lower ORP values during arsenopyrite bio-oxidation. The ORP value in the biotic system was mainly determined by the coupling of Fe3+/Fe2+ (Zhang et al., 2015a, 2015b). The comparison showed that the oxidation of the aqueous As(III) to As (V) was highly responsible for the ORP value, and a lower ORP value was beneficial for the stability of As(III). These results are in agreement with Wiertz and co-authors (Wiertz et al., 2006), who reported that the oxidation of As(III) occurred only at a relatively high redox potential (ORP > 450 mV vs. Ag/AgCl) (Eq. (5)).
H3 AsO4 + 2Fe2 + + 2H+
(5)
3.2. Changes in morphology, composition and phase of arsenopyrite The SEM results (Fig. 2 and Fig. S4) show that in the presence of HA, the surface of the arsenopyrite was covered by a loose structure (Fig. 2e), and the elemental constituents of area B were mainly composed by As and Fe. The higher contents of C and O imply that small amounts of HA were adsorbed on the mineral surface. (Fig. 2f). While in the absence of HA, the mineral surface was covered by a fine and dense layer enriched in S, Fe and As (area A), and the most dominant one was S (Fig. 2b). After 12 d of bio-oxidation, the undissolved arsenopyrite was completely covered by a thick and compact product layer (Fig. 2c). In the presence of HA, the residue was covered by a porous layer with many bacteria embedded (Fig. 2g). For the sterile controls in the absence of HA, the mineral surface remained intact after 12 d (Fig. 2d), and only a few products were formed on the mineral surface when 60 mg/L HA was added (Fig. 2h). The FT-IR spectra for the arsenopyrite residues bio-oxidized in the absence and presence of HA at day 4 are shown in Fig. 3. In comparison with the spectra of HA, HA-As(V) and HA-Fe(III), some new bands appeared at 1032, 538 and 470 cm−1 for the residue bio-oxidized in the presence of HA, which were assigned to the CeO, CeOeC and MeeOH stretching of HA (Fakour and Lin, 2014), suggesting again that some HA adsorbed on the mineral surface. Meanwhile, new peaks appeared at 1384 and 628 cm-1, which were attributed to the As-O-HA and Fe-O-HA stretching (Brigante et al., 2010), suggesting the formation of HA-As(V) and/or HA-Fe(III) complexes that adsorbed on the mineral surface. XRD patterns (Fig. 4) show that in the presence of HA, the peaks of 6
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Fig. 7. XPS spectra of the surface sulfur of arsenopyrite residues bio-oxidized in the absence of HA at days 2 (a), 4 (b), 8 (c), 12 (d), and in the presence 60 mg/L HA at days 2 (e), 4 (f), 8 (g), 12 (h), and in the sterile controls reacted for 12 d in the absence (i) and presence of (j) 60 mg/L HA.
scorodite were not found until day 10, the peaks of S0 became weaker at the later stage, and no arsenopyrite was found at day 12 (Fig. 4b). While in the absence of HA, S0 and jarosites were detected at day 3 and scorodite (ferric arsenate) at day 4, then they became the main components, and some remnants of arsenopyrite could also be detected at day 12 (Fig. 4a). These results suggest that the HA clearly promotes the bio-oxidation of arsenopyrite. Compared with the changes of solution parameters, it can be found that the dissolution of arsenopyrite was gradually inhibited with accumulation of S0 and scorodite on the mineral surface, which is in agreement with the literature (Deng et al., 2018; Fantauzzi et al., 2011). Additionally, further oxidation of S0 in an acidic environment (pH < 2.0), as described in Eq. (6), can only be achieved in the presence of sulfur-oxidizing bacteria (Vera et al., 2013; Rohwerder et al., 2003). The presence of HA may bind considerable amounts of dissolved arsenic and iron through formation of amorphous As-Fe-HA complexation (Liu et al., 2011), and these reactions will prevent the formation of scorodite and jarosites.
2S0 (surface ) + 3O2 + 2H2 O
Microbial
2SO4 2 + 4H+
(AsS)2− at 162.30 eV (Nesbitt et al., 1995). The As 3d(5/2) XPS spectra and S 2p(3/2) XPS spectra for the residues are shown in Figs. 6 and 7, respectively. The fitted results (Table S2) show that during arsenopyrite bio-oxidation, the intensities of the peaks of As(-I)-S, As(0) and As(I) gradually decreased, while the intensities of the peaks of As(III)eO and As(V)eO increased (Fig. 6a–h). In agreement with other studies (Corkhill et al., 2008; Schaufuss et al., 2000), these results indicated that the oxidation of arsenic during bio-oxidation of arsenopyrite proceeds with a series of one-electron transfer steps. In addition, as shown by the S 2p(3/2) XPS spectra (Fig. 7 and Table S3), the sulfur species for the residues during bio-oxidation were mainly SO42−, S0 and Sn2−, besides (AsS)2−, regardless of whether HA was present. The intensity of the peak of (AsS)2− decreased more quickly when HA was added, indicating that the presence of HA notably promoted the process. 3.4. Sulfur and iron speciation transformation
(6)
The S K-edge XANES spectra for the residues are shown in Fig. 8, with the fitted results being given in Table 1. By comparison with these reference samples (Fig. 8a), it can be found that during bio-oxidation, the intensity of the peak at 2471.8 eV for arsenopyrite gradually decreased, while the intensity of the peak at 2482.8 eV for SO42− gradually increased, and the presence of HA accelerated these changes (Fig. 8b). Table 1 further shows that the sulfur species of the residues biooxidized in the absence of HA were mainly composed of 88.6% arsenopyrite, 3.8% S0, 3.1% schwertmannite, and 4.5% jarosites at day 1 compared with 91.4% arsenopyrite, 3.0% S0, 2.4% schwertmannite, and 3.2% jarosites in the presence of HA. Then, the content of
3.3. Changes in surface components of arsenopyrite The XPS spectra of the original arsenopyrite (Fig. 5 and Table S1) shows that the surface arsenic species, as shown by the As 3d(5/2) spectra (Fig. 5a), are composed of As(0) (42.00 eV), As(I)-O (43.20 eV) and As(III)-O (44.15 eV), besides the major component As(-I)-S at 41.15 eV [8], and the surface sulfur species, as shown by S 2p(3/2) spectra (Fig. 5b), are composed by S2− (161.35 eV), Sn2- (163.26 eV), S0 (164.20 eV), and SO32− (166.50 eV), besides the major component 7
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Fig. 8. S K-edge XANES spectra of reference samples (a), and arsenopyrite residues bio-oxidized at different times, and in the sterile control reacted for 12 d, in the absence (b) and presence (c) of 60 mg/L HA. Table 1 Fitted results of S K-edge XANES spectra of arsenopyrite residues bio-oxidized at different times, and in the sterile controls leached for 12 d, in the absence (a) and presence (b) of 60 mg/L HA, with different reference spectra. Sample
Percentage of contribution of reference samples (%) S0
Arsenopyrite
1d 2d 4d 8d 12 d SC-12 d
Schwertmannite
Jarosites
R-factor
a
b
a
b
a
b
a
b
a
b
88.6 74.8 45 25.6 19.3 93.6
91.4 65.9 36.3 16.2 7.1 87.4
3.8 10.9 18.4 28.3 25.4 6.4
3.0 8.7 13.6 10.2 9.3 7.9
3.1 6.1 11.8 8.4 9.2 –
2.4 11.3 18.9 18.5 19.4 –
4.5 8.2 24.8 37.7 46.1 –
3.2 14.1 31.2 55.1 64.2 4.7
0.016 0.059 0.028 0.063 0.081 0.022
0.023 0.047 0.041 0.079 0.052 0.014
arsenopyrite decreased, while the other sulfur species gradually increased. After 12 d of bio-oxidation, the sulfur species of the residue were composed of 19.3% arsenopyrite, 25.4% S0, 9.2% schwertmannite, and 46.1% jarosites in the absence of HA, while they were 7.1% arsenopyrite, 9.3% S0, 19.4% schwertmannite, and 64.2% jarosites in the presence of HA. These results demonstrate that in the presence of HA, the surface sulfur was oxidized and transformed faster to schwertmannite and jarosites during bio-oxidation of arsenopyrite, which is consistent with the results of the XRD (Fig. 4) and XPS (Fig. 7) analyses. The Fe L-edge XANES spectra for the residues (Fig. 9) showed that both the L3-edge and L2-edge contained the Fe(II) and Fe(III) absorption peaks, i.e., Ea (706.8 eV) and Eb (708.3 eV) for L3-edge, and Ec (719.9 eV) and Ed (721.9 eV) for L2-edge (Mikhlin and Tomashevich, 2005). The area of the peak for Fe(II) gradually decreased with the
increase in the area of the peak for Fe(III), and this trend became more clear when HA was added (Fig. 9b), indicating that the presence of HA promotes the transformation of Fe(II) to Fe(III) on the mineral surface during arsenopyrite bio-oxidation. The oxidation of Fe(II) is notably slow under acidic conditions but can be catalyzed by many orders of magnitude by acidophilic bacteria, such as A. ferrooxidans and S. thermosulfidooxidans (Millero et al., 1987). Combining with the changes of solution parameters (Fig. 1) and phase transformation (Fig. 3), it can be concluded that the presence of HA in the arsenopyrite bio-oxidation system promotes the growth of bacteria, which ensures the fast generation of Fe3+. On the other hand, HA on the mineral surface can absorb and enrich considerable amounts of Fe3+ (Sharma et al., 2010), thereby ensuring the rapid dissolution of arsenopyrite due to the increased attack of Fe3+ on the mineral.
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Fig. 9. Fe L-edge XANES spectra of arsenopyrite residues bio-oxidized at days 4, 8 and 12, and in the sterile controls reacted for 12 d, in the absence (a) and presence (b) of 60 mg/L HA.
Fig. 10. SEM images and EDS analyses of elemental composition of the cells of S. thermosulfidooxidans grown on arsenopyrite at stationary phase (day 4) in the absence (a) and presence (b) of 60 mg/L HA.
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Fig. 11. L edge NEXAFS spectra of As(III) (NaAsO2) and As(V) (Na2AsO4) (left), and the dual-energy images of arsenic overlaid on the STXM map of cells that reacted with arsenopyrite for 4 d in the absence (a: As(III), c: As(V)) and presence (b: As(III), d: As(V)) of HA. The color change from purple to red represents the increase of element contents from 0% to 100% (right).
Fig. 12. XRD patterns and SEM images of the biogenetic jarosites (a, c) and jarosites-HA (b, d) used in this study.
3.5. Surface morphology and composition of bacterial cells
adsorbed onto the cells, which may promote arsenic adsorption. Further distribution analysis of arsenic on the single cell surface by STXM (Fig. 11) clearly indicates that more As(III) and As(V) were adsorbed onto the cell surface when HA was added, as shown by the difference in the surface densities of As(III) and As(V) on the cell: 0.78 × 10−5-2.51 × 10−5 g/cm2 and 0.99 × 10−5-3.25 × 10−5 g/cm2 in the presence of HA (Fig. 11b, d), compared with 0.59 × 10−52.18 × 10−5 g/cm2 and 0.65 × 10−5-2.37 × 10−5 g/cm2 in the absence of HA (Fig. 10a, c). According to Sand and co-authors (Sand and Gehrke, 2006), the extracellular polymeric substances (EPS) of acidophilic bacteria can adsorb a high amount of Fe3+ by forming a positively charged adduct during bio-oxidation of metal sulfides, which combines easily with negatively charged HA molecules via an
The differences in surface morphology and composition of the cells of S. thermosulfidooxidans grown on arsenopyrite in the absence and presence of HA were characterized by SEM-EDS (Fig. 10) and STXM (Fig. 11). As shown in Fig. 10, the cells collected in the biotic system in the absence of HA were small with smooth surfaces (Fig. 10a). However, in the presence of HA, the cells were larger and were covered with a flocculent layer (Fig. 10b), which was mainly comprised by C, O, Fe, Na, P, Ca and As according to the EDS analyses, indicating both HA and arsenic adsorbed onto the cells. It is noteworthy that in the presence of HA, the contents of the elements on the surface of cells, especially C, Fe and As, significantly increased. These results demonstrate that some HA 10
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Fig. 13. SEM images (left) and EDS analyses of elemental composition (top right) and in situ content distributions of key elements (bottom right) of the jarosites (a) and jarosites-HA (b) after reaction with As(V) for 4 d.
electrostatic interaction and thus enhances the adsorption of arsenic (Ren et al., 2016). The results of FT-IR (Fig. S5) and μ-XRF (Fig. S6) show the evidence of the bound Fe and As on the cell surface.
obviously increased, with slight decreases in the contents of Fe and S (Fig. 13b), clearly indicating more adsorption of As(V) onto jarositesHA than on jarosites.
3.6. Characterization of arsenic adsorption onto biogenic minerals
3.7. Adsorption kinetics and isotherms of arsenic onto biogenic minerals
The XRD results (Fig. 12a, b) show that the biogenic minerals have the same main component potassium jarosite with small amount of ammoniojarosite, whether there was HA or not. The SEM results, however, show that the biogenic minerals formed in the presence of HA exist with some villous structure covered on the loose mineral surface (Fig. 12d), while in the absence of HA, a polyhedron-shaped and dense structure was formed (Fig. 12c). After adsorption by As(V), the precipitates jarosites and jarosites-HA complexes were further analyzed by SEM-EDS. The results (Fig. 13) show the existence of As besides Fe, S, O, C, N, and K, which were all distributed on the precipitate surface. Compared with the jarosites (Fig. 13a), the contents of C, O and As on the surface of jarosites-HA
To clarify the difference in the adsorption properties of jarosites and jarosites-HA that may affect the fate of arsenic species and thus the biooxidation of arsenopyrite, the adsorption kinetics and isotherms of As (III) and As(V) onto the precipitates above were investigated by batch experiments, and the results are shown in Fig. 14. The kinetics results (Fig. 14a, b and Table S4) show that the arsenic adsorption occurred considerably faster during the initial period and then became slow, finally reached equilibrium after 4320 min (72 h). Compared with the jarosites, the jarosites-HA demonstrated a greater adsorption capacity for both As(III) and As(V), and more adsorption of As(V) than As(III) when pH ≤ 2.0 (Fig. 14b), indicating that the presence of HA promotes more adsorption of As(V) than As(III) in the acidic bioleaching 11
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Fig. 14. Adsorption kinetics (a, b) and isotherm (c, d) of As(III) (a, c) and As(V) (b, d) on jarosites and jarosites-HA, respectively. Table 2 Langmuir and Freundlich adsorption isotherm parameters for the binding of As(III) and As(V) onto jarosites (J) and jarosites-HA (J-HA) at pH 2.0 ± 0.1. Sample
J J-HA J J-HA
Langmuir
As(III) As(III) As(V) As(V)
Freundlich
KL(L/mg)
qm(mg/g)
R2
Chi square
KF
n
R2
Chi square
0.0096 0.0127 0.0132 0.0149
6.22 10.95 7.76 13.62
0.998 0.994 0.997 0.996
0.098 1.103 0.115 1.221
0.1451 0.3568 0.2471 0.4297
0.549 0.606 0.615 0.632
0.932 0.921 0.916 0.924
1.389 9.886 2.714 11.583
environment. The adsorption isotherm results (Fig. 14c, d, Table 2) show that both As(III) and As(V) adsorbed on both jarosites and jarosites-HA are in greater accordance with the Langmuir model (Eq. (7)) than with the Freundlich model (Eq. (8)), indicating that the adsorption occurs on a homogeneous surface with a finite number of identical adsorption sites (Qi et al., 2015). Calculated from the Langmuir equation, the maximum adsorption capacities of As(III) and As(V) were found to be 6.22 and 7.76 mg/g for jarosites, while they were 10.95 and 13.62 mg/g for jarosites-HA, respectively.
qee =
qm KL Ce 1 + KL Ce
qee = KF Ce1/n
4. Conclusions The findings of the present study clearly indicated that the presence of HA could change the physicochemical properties of the surface of arsenopyrite during bio-oxidation and could affect the speciation transformation of iron and sulfur and arsenic immobilization. The specific conclusions are as follows: (i) The presence of HA apparently affects the changes of solution parameters during arsenopyrite bio-oxidation, with enhancement of the growth rate of cells and releasing more [SO42−] but less [FeT] and [AsT], and lower ORP values that may be beneficial for the stability of As(III). (ii) The formation of a porous structure of residue during bio-oxidation of arsenopyrite in the presence of HA benefits the cells’ adsorption and Fe3+ attack on the mineral, which may play an important role in the enhancement of the bio-oxidation of S0 and the dissolution of arsenopyrite. (iii) The adsorption of HA onto the surface of bacteria cells obviously enhances the adsorption of As(III) and As(V), and the jarosites in the presence of HA significantly enhance the arsenic adsorption, and both of them may contribute to the in-situ arsenic immobilization during arsenopyrite bio-oxidation.
(7) (8)
where qe is the concentration of arsenic adsorbed on the solid phase (mg/g), Ce is the equilibrium concentration of arsenic in the aqueous phase (mg/L), KL is the Langmuir sorption coefficient related to the affinity of the binding sites (L/mg), qm is the total concentration of surface sites (mg/g), and KF and n are the Freundlich constants. The results of fitting the Langmuir and Freundlich equations to the isotherm curves are summarized in Table 2. 12
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The results of this study may be useful in selecting management strategies for metal recovery and arsenic disposal in arsenopyrite bearing environment sites.
Mckibben, M.A., Tallant, B.A., Del Angel, J.K., 2008. Kinetics of inorganic arsenopyrite oxidation in acidic aqueous solutions. Appl. Geochem. 23, 121–135. Mikhlin, Y., Tomashevich, Y., 2005. Pristine and reacted surfaces of pyrrhotite and arsenopyrite as studied by X-ray absorption near-edge structure spectroscopy. Phys. Chem. Miner. 32, 19–27. Millero, F.J., Sotolongo, S., Izaguirre, M., 1987. The oxidation kinetics of Fe(II) in seawater. Geochim. Cosmochim. Acta 51, 793–801. Nesbitt, H.W., Muir, I.J., Prarr, A.R., 1995. Oxidation of arsenopyrite by air and airsaturated, distilled water, and implications for mechanism of oxidation. Geochim. Cosmochim. Acta 59, 1773–1786. Norris, P.R., Barr, D.W., 1985. Growth and iron oxidation by acidophilic moderate thermophiles. FEMS Microbiol. Lett. 28, 221–224. Pina, P.S., Oliveira, V.A., Cruz, F.L.S., Leão, V.A., 2010. Kinetics of ferrous iron oxidation by Sulfobacillus thermosulfidooxidans. Biochem. Eng. J. 51, 194–197. Qi, J., Zhang, G., Li, H., 2015. Efficient removal of arsenic from water using a granular adsorbent: Fe-Mn binary oxide impregnated chitosan bead. Bioresour. Technol. Rep. 193, 243–249. Ramírez-Aldaba, H., Valles, O.P., Vazquez-Arenas, J., Rojas-Contreras, J.A., Valdez-Pérez, D., Ruiz-Baca, E., Lara, R.H., 2016. Chemical and surface analysis during evolution of arsenopyrite oxidation by Acidithiobacillus thiooxidans in the presence and absence of supplementary arsenic. Sci. Total Environ. 566, 1106–1119. Rashid, M., Sterbinsky, G.E., Pinilla, M.A.G., Cai, Y., O’Shea, K.E., 2018. Kinetic and mechanistic evaluation of inorganic arsenic species adsorption onto humic acid grafted magnetite nanoparticles. J. Phys. Chem. C. 122, 13540–13547. Ravel, B., Newville, M., 2010. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12, 537–541. Redman, A.D., Macalady, D.L., Ahmann, D., 2002. Natural organic matter affects arsenic speciation and sorption onto hematite. Environ. Sci. Technol. 36, 2889–2896. Ren, J., Fan, W., Wang, X., Ma, Q., Li, X., Xu, Z., Wei, C., 2016. Influences of size-fractionated humic acids on arsenite and arsenate complexation and toxicity to Daphnia magna. Water Res. 108, 68–77. Rohwerder, T., Gehrke, T., Kinzler, K., Sand, W., 2003. Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl. Microbiol. Biotechnol. 63, 239–248. Sand, W., Gehrke, T., 2006. Extracellular polymeric substances mediate bioleaching/ biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria. Res. Microbiol. 157, 49–56. Schaufuss, A.G., Nesbitt, H.W., Scaini, M.J., Hoechst, H., Bancroft, M.G., Szargan, R., 2000. Reactivity of surface sites on fractured arsenopyrite (FeAsS) toward oxygen. Am. Mineral. 85, 1754–1766. Sharma, P., Ofner, J., Kappler, A., 2010. Formation of binary and ternary colloids and dissolved complexes of organic matter, Fe and As. Environ. Sci. Technol. 44, 4479–4485. Sharma, V.K., Sohn, M., 2009. Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ. Int. 35, 743–759. Vera, M., Schippers, A., Sand, W., 2013. Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation-part A. Appl. Microbiol. Biotechnol. 97, 7529–7541. Wang, S.F., Jiao, B.B., Zhang, M.M., Zhang, G.Q., Wang, X., Jia, Y.F., 2018. Arsenic release and speciation during the oxidative dissolution of arsenopyrite by O2, in the absence and presence of EDTA. J. Hazard. Mater. 346, 184–190. Wiertz, J.V., Mateo, M., Escobar, B., 2006. Mechanism of pyrite catalysis of As(III) oxidation in bioleaching solutions at 30 °C and 70 °C. Hydrometallurgy 83, 35–39. Xu, B., Yang, Y., Li, Q., Jiang, T., Zhang, X., Li, G., 2017. Effect of common associated sulfide minerals on thiosulfate leaching of gold and the role of humic acid additive. Hydrometallurgy 171, 44–52. Yu, Y., Zhu, Y., Gao, Z., Gammons, C.H., Li, D., 2007. Rates of arsenopyrite oxidation by oxygen and Fe(III) at pH 1.8-12.6 and 15-45 degrees C. Environ. Sci. Technol. 41, 6460–6464. Zhang, G., Chao, X., Guo, P., Cao, J., Yang, C., 2015a. Catalytic effect of Ag+ on arsenic bioleaching from orpiment (As₂S₃) in batch tests with Acidithiobacillus ferrooxidans and Sulfobacillus sibiricus. J. Hazard. Mater. 283, 117–122. Zhang, S.Y., Zhao, F.J., Sun, G.X., Su, Q.J., Yang, X.R., Li, H., Zhu, Y.G., 2015b. Diversity and abundance of arsenic biotransformation genes in paddy soils from Southern China. Environ. Sci. Technol. 49, 4138–4146. Zhu, T., Lu, X., Liu, H., Li, J., Zhu, X., Lu, J., Wang, R., 2014. Quantitative X-ray photoelectron spectroscopy-based depth profiling of bioleached arsenopyrite surface by Acidithiobacillus ferrooxidans. Geochim. Cosmochim. Acta 127, 120–139. Zhu, W., Xia, J.L., Yang, Y., Nie, Z.Y., Zheng, L., Ma, C.Y., Qiu, G.Z., 2011. Sulfur oxidation activities of pure and mixed thermophiles and sulfur speciation in bioleaching of chalcopyrite. Bioresour. Technol. Rep. 102, 3877–3882.
Acknowledgements This work was supported by the Joint Funds of NSFC and Liaoning Science Foundation (U1608254), the National Natural Science Foundation of China (No. 51861135305, 41830318, 51774342), the Open Funds of Beijing Synchrotron Radiation Facility (2018-BEPC-PT001390 and 2018-BEPC-PT-001391), and the Open Funds of Shanghai Synchrotron Radiation Facility (2018-SSRF-PT-005070, 2019-SSRF-PT008827). Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.jhazmat.2019.121359. References Alsidcheikh, M., Dia, A., Guenet, H., Vantelon, D., Davranche, M., Delhaye, T., 2015. Interactions between natural organic matter, sulfur, arsenic and iron oxides in reoxidation compounds within riparian wetlands: NanoSIMS and X-ray adsorption spectroscopy evidences. Sci. Total Environ. 515, 118–128. Brigante, M., Zanini, G., Avena, M., 2010. Effect of humic acids on the adsorption of paraquat by goethite. J. Hazard. Mater. 184, 241–247. Celebi, O., Kilikli, A., Erten, H.N., 2009. Sorption of radioactive cesium and barium ions onto solid humic acid. J. Hazard. Mater. 168, 695–703. Corkhill, C.L., Vaughan, D.J., 2009. Arsenopyrite oxidation-a review. Appl. Geochem. 24, 2342–2361. Corkhill, C.L., Wincott, P.L., Lloyd, J.R., Vaughan, D.J., 2008. The oxidative dissolution of arsenopyrite (FeAsS) and enargite (Cu3AsS4) by Leptospirillum ferrooxidans. Geochim. Cosmochim. Acta 72, 5616–5633. Cornejo-Garrido, H., Fernández-Lomelín, P., Guzmán, J., Cervini-Silva, J., 2008. Dissolution of arsenopyrite (FeAsS) and galena (PbS) in the presence of desferrioxamine-B at pH 5. Geochim. Cosmochim. Acta 72, 2754–2766. Coussy, S., Benzaazoua, M., Blanc, D., Moszkowicz, P., Bussière, B., 2011. Arsenic stability in arsenopyrite-rich cemented paste backfills: a leaching test-based assessment. J. Hazard. Mater. 185, 1467–1476. Dave, S.R., Gupta, K.H., Tipre, D.R., 2008. Characterization of arsenic resistant and arsenopyrite oxidizing Acidithiobacillus ferrooxidans from Hutti gold leachate and effluents. Bioresour. Technol. Rep. 99, 7514–7520. Deng, S., Gu, G.H., Xu, B., Li, L., Wu, B., 2018. Surface characterization of arsenopyrite during chemical and biological oxidation. Sci. Total Environ. 626, 349–356. Dopson, M., Lindström, E.B., 2004. Analysis of community composition during moderately thermophilic bioleaching of pyrite, arsenical pyrite, and chalcopyrite. Microb. Ecol. 48, 19–28. Fakour, H., Lin, T.F., 2014. Experimental determination and modeling of arsenic complexation with humic and fulvic acids. J. Hazard. Mater. 279, 569–578. Fantauzzi, M., Licheri, C., Atzei, D., Loi, G., Elsener, B., Rossi, G., Rossi, A., 2011. Arsenopyrite and pyrite bioleaching: evidence from XPS, XRD and ICP techniques. Anal. Bioanal. Chem. 401, 2237–2248. Ide-Ektessabi, A., Kawakami, T., Watt, F., 2004. Distribution and chemical state analysis of iron in the Parkinsonian substantia nigra using synchrotron radiation micro beams. Nucl. Instrum. Meth. B 213, 590–594. Karamanev, D.G., Nikolov, L.N., Mamatarkova, V., 2002. Rapid simultaneous quantitative determination of ferric and ferrous ions in drainage. Miner. Eng. 15, 341–346. Liu, G., Cai, Y., 2013. Studying arsenite-humic acid complexation using size exclusion chromatography-inductively coupled plasma mass spectrometry. J. Hazard. Mater. 262, 1223–1229. Liu, G.L., Fernandez, A., Cai, Y., 2011. Complexation of arsenite with humic acid in the presence of ferric iron. Environ. Sci. Technol. 45, 3210–3216. Márquez, M.A., Ospina, J.D., Morales, A.L., 2012. New insights about the bacterial oxidation of arsenopyrite: a mineralogical scope. Miner. Eng. 39, 248–254.
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Humic acid promotes arsenopyrite bio-oxidation and arsenic immobilization Duo-rui Zhanga,1, Hong-rui Chena,1, Jin-lan Xiaa,⁎, Zhen-yuan Niea, Xiao-lu Fana, Hong-chang Liua, Lei Zhengb, Li-juan Zhangc, Hong-ying Yangd a
Key Lab of Biometallurgy of Ministry of Education of China, School of Minerals Processing and Bioengineering, Central South University, Changsha 410083, China Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing 100049, China Shanghai Synchrotron Radiation Facility, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai 201204, China d School of Metallurgy, Northeastern University, Shenyang 110819, China b c
GRAPHICAL ABSTRACT
ARTICLE INFO
ABSTRACT
Editor: R. Debora
The bio-oxidative dissolution of arsenopyrite, the most severe arsenic contamination source, can be mediated by organic substances, but pertinent studies on this subject are scarce. In this study, the bio-oxidative dissolution of arsenopyrite by Sulfobacillus thermosulfidooxidans and arsenic immobilization were evaluated in the presence of humic acid (HA). The mineral dissolution was monitored through analyses of the parameters in solution, phase and element speciation transformations on the mineral surface, and arsenic immobilization on the surfaces of cells and jarosites-HA. The results show that the presence of HA enhances the dissolution of arsenopyrite, e.g., 7.1% of arsenopyrite was in the residue after 12 d of bio-oxidation compared to 19.3% in the absence of HA. Meanwhile, the presence of HA led to changes of the fates of As and Fe and no accumulation of elemental sulfur (S0) or ferric arsenate on the mineral surface. Moreover, a flocculent porous structure was formed on the surfaces of both microbial cells and jarosites, on which a large amount of arsenic was adsorbed. These results clearly indicate that HA can simultaneously promote the dissolution of arsenopyrite and arsenic immobilization, which may be significant for bioleaching of arsenopyrite-bearing contaminated sites.
Keywords: Arsenopyrite Bio-oxidation Humic acid Speciation transformation Arsenic immobilization
Corresponding author. E-mail address: [email protected] (J.-l. Xia). 1 These two authors contributed equally to this work. ⁎
https://doi.org/10.1016/j.jhazmat.2019.121359 Received 17 July 2019; Received in revised form 15 September 2019; Accepted 28 September 2019 0304-3894/ © 2019 Elsevier B.V. All rights reserved.
Please cite this article as: Duo-rui Zhang, et al., Journal of Hazardous Materials, https://doi.org/10.1016/j.jhazmat.2019.121359
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1. Introduction
As, 44.09; Fe, 33.52; S, 19.06; O, 2.25; Si, 0.34; Al, 0.21; Cu, 0.23; Pb, 0.12; Zn, 0.08; Ca, 0.11; and Ag, 0.01. The mineral was mainly composed by arsenopyrite according to the result of XRD (Fig. S1). The mineral was ground and passed through −200 + 400 mesh screens to achieve particles ranging in size from 38 to 75 μm.
Arsenic (As) is a toxic element of significant environmental concern due to its leaching from hazardous wastes and geological minerals. Arsenopyrite (FeAsS) is the most common As-bearing sulfide mineral in many ore deposits (Dave et al., 2008). Arsenopyrite is usually stable under a reducing environment, but under oxidizing conditions, it is easily decomposed with the release of a considerable amount of sulfate (SO42−), arsenite (AsO33-) and arsenate (AsO43-) to the solution, thereby contributing to the generation of hazardous acid mine drainage (AMD) (Corkhill and Vaughan, 2009; Wang et al., 2018; Coussy et al., 2011). The chemical and biological oxidations of arsenopyrite have been widely studied (Mckibben et al., 2008; Cornejo-Garrido et al., 2008; Yu et al., 2007; Corkhill et al., 2008). It has been found that the toxicity and fate of inorganic arsenic is highly dependent on arsenic speciation, which can be influenced by environmental parameters, including pH, redox potential (ORP), metal ions, microorganisms, and dissolved organic matter (DOM) (Yu et al., 2007; Sharma and Sohn, 2009; Zhang et al., 2015a, 2015b; Liu and Cai, 2013). Among these parameters, DOM is one of the important complexing agents that can change the physical and chemical properties of a mineral surface and critically affect the environmental behavior and distribution of iron and arsenic (Redman et al., 2002; Alsidcheikh et al., 2015). Humic acid (HA) is a common DOM in nature and can be an effective sorbent for toxic metal ions due to the amino, carboxyl, phenolic, and sulfhydryl moieties that can act as the potential binding sites for toxic metal ions (Celebi et al., 2009; Rashid et al., 2018), which means that HA may influence the fate of arsenic species during biooxidation of arsenopyrite. On the other hand, the arsenopyrite biooxidation process involves complex biochemical reactions and secondary products, such as elemental sulfur (S0), jarosite, orpiment, and ferric arsenate/scorodite (Corkhill et al., 2008; Márquez et al., 2012; Ramírez-Aldaba et al., 2016), which may influence the dissolution of arsenopyrite and the arsenic fate. However, no pertinent studies have been reported to date. In the present study, the influence of HA on the dissolution of arsenopyrite and the fate of arsenic was addressed, during which the biooxidation of arsenopyrite accompanied the transformation of Fe/S/As and the effect of the products on the immobilization of As were simultaneously investigated. This study helps to elucidate the bio-oxidation of arsenopyrite with simultaneous arsenic immobilization.
2.3. Experimental procedure The cultures were carried out in 250-mL Erlenmeyer flasks containing 100 mL sterilized basal medium and 1 g arsenopyrite. The initial pH of the medium was adjusted with 1 M sulfuric acid to pH 2.0 ± 0.05. The initial inoculated cell density was 4 × 107 cells/mL. The cultures were incubated in an incubator shaker (ZHTY-70S) at 180 rpm and 45 °C. The experiments were conducted with different concentrations of HA (HA-Na) (w/v, mg/L) (0, 20, 40, 60, 80, and 100), and no HA was added to the control. Meanwhile, abiotic controls were also performed under the same conditions. All experiments were performed in triplicate under the same conditions. 2.4. Analysis methods Solution samples were collected every 1–2 d for monitoring cell density, concentrations of sulfate ions and soluble Fe and As species, pH and ORP values. The cell density was determined by a blood corpuscle counter (XB-K-25). The concentration of sulfate ions ([SO42−]aq) was measured using a barium sulfate turbidimetric colorimetric method (Zhu et al., 2011). The concentrations of total Fe ([FeT]aq) and Fe3+ ([Fe3+]aq) were determined by 5-sulfosalicylic acid spectrophotometry (Karamanev et al., 2002). The concentration of total As ([AsT]aq) was measured by inductively coupled plasma-atomic emission spectroscopy (ICP-AES) (IRIS Intrepid II XSP, Thermo Fisher, USA). The concentration of arsenite ([As(III)]aq) was analyzed by atomic fluorescence spectrometer (AFS) (PS Analytical Ltd, Kent, U.K.). The pH and ORP values were measured using a Thermo Scientific Orion DUAL STARTM pH/ISE meter with a pH meter and a platinum (Pt) electrode with a calomel electrode (Hg/HgCl) as a reference. The surface morphology of the arsenopyrite was observed by scanning electron microscopy (SEM) coupled with an energy dispersive spectroscopy (EDS) facility (Nova™ NanoSEM 230, FEI, USA). Fourier transform infrared spectroscopy (FT-IR) analysis was performed with a Fourier transform spectrometer (Nexus 670, Nicolet, USA). X-ray diffraction (XRD) analysis was conducted with CuKα radiation (40 kV/ 250 mA) in a RINT2000 vertical goniometer. The scanning range was from 10° to 80° 2θ with a step of 0.02° and a dwell time of 4 s. The Fe, S and As speciation transformations on the mineral surfaces were analyzed by Fe L-edge and S K-edge XANES spectroscopy, and Xray photoelectron spectroscopy (XPS), respectively. The Fe L-edge and S K-edge XANES analyses were carried out on 4B7B beamline and 4B7A beamline, respectively, at the Beijing Synchrotron Radiation Facility, Beijing, China. The Fe L-edge XANES spectra data were recorded in total electron yield (TEY) mode at the step widths of 0.5 eV from 690 to 700 eV and 0.1 eV from 700 to 928 eV. The S K-edge XANES spectra data were recorded in the fluorescence mode at ambient temperature and scanned at a step width of 0.2 eV between 2460 and 2510 eV. The spectra were normalized to the maximum of the absorption jump (IdeEktessabi et al., 2004), and fitted for their linear combination fits (LCF) using the standard spectra with the IFEFFIT program (Ravel and Newville, 2010). The XPS spectra of the reacted arsenopyrite surfaces were collected using a Thermo ESCALAB 250XI X-ray photoelectron spectrometer equipped with a monochromatized Al Kα X-ray source (15 KeV) and a hemispherical analyzer fitted with a five-channeltron multidetection system. All photoelectron binding energies (BE) were referenced to C1s adventitious contamination peaks set at 284.6 eV BE. The distribution mapping for arsenic in a single cell was detected by scanning transmission X-ray microscopy (STXM) based on the dualenergy contrast image analysis of the near-edge X-ray absorption fine
2. Materials and methods 2.1. Strain and culture conditions The strain Sulfobacillus thermosulfidooxidans YN-22 (Accession number of 16S rRNA in GeneBank: DQ650351) was preserved at the Key Laboratory of Biometallurgy of Ministry of Education of China, Changsha, China. S. thermosulfidooxidans is widespread in sulfur-rich, acidic environments and possesses higher sulfur and iron oxidation activity at elevated temperatures compared with mesophilic bacteria (Pina et al., 2010; Dopson and Lindström, 2004). The basal medium for cell cultivation was comprised of the following components (in g/L): (NH4)2SO4, 3.0; MgSO4, 0.5; K2HPO4, 0.5; KCl, 0.1; Ca(NO3)2, 0.01 and yeast extracts 0.2. For domestication, S. thermosulfidooxidans was cultured in basal medium supplemented with 10 g/L arsenopyrite as the energy source. 2.2. Mineral sample The mineral sample used in this study were provided by the School of Minerals Processing and Bioengineering, Central South University, Changsha, China. The elemental composition of the mineral analyzed by X-ray fluorescence spectroscopy (XRF, Axios mAX) was (in wt.%): 2
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Fig. 1. Solution parameters during bio-oxidation of arsenopyrite by S. thermosulfidooxidans and in the sterile controls. Changes of cell density (a), [SO42−] (b), [FeT] (c), [Fe3+] (d), [AsT] (e), [As(III)] (f), pH (g) and ORP (h).
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Fig. 2. SEM images of arsenopyrite residues bio-oxidized in the absence of HA at days 4 (a) and 12 (c), in the presence of 60 mg/L HA at days 4 (e), 12 (g), and in the sterile controls reacted for 12 d in the absence (d) and presence of 60 mg/L HA (h). The EDS spectra in (b) and (f) correspond to the regions “A” and “B” in (a) and (e) as indicated by red rectangles.
Then, the precipitates were harvested with a 0.45-μm filter paper, dried and characterized by SEM and XRD. 2.6. Adsorption experiments The As(III) and As(V) solutions (100 mg/L, which is lower than the tolerance limit of S. thermosulfidooxidans, 3 g/L, see Fig. S2) were prepared by dissolving desired the amounts of Na3AsO3 and Na2HAsO4 in deionized water. The experiments for arsenic adsorption kinetics were conducted by adding 0.1 g of sorbent to 50 mL centrifuge tubes each containing 20 mL solution consisting of 0.01 M NaNO3 as the background electrolyte and 60 mg/L of As(III) and As(V). The solution pH was adjusted to 2.0 ± 0.05, and the centrifuge tubes were then placed in an incubator shaker at 180 rpm and 45 °C. Each experimental treatment was conducted in triplicate under the same conditions. The sampled suspension was directly filtered through a 0.45-μm filter paper, and then the arsenic concentrations were determined. The adsorbed-As (III) and As(V) in solid phase (Cs) were determined by mass balance using Eq. (1).
Fig. 3. FT-IR spectra of arsenopyrite residues bio-oxidized in the absence and presence of HA, in comparison with the spectra of HA before and after interaction with As(V) and Fe(III).
Cs = structure (NEXAFS) of arsenic at BL08U1A at the Shanghai Synchrotron Radiation Facility, Shanghai, China. NaAsO2 (As(III)) and Na2AsO4 (As (V)) were chosen as the references for the NEXAFS analyses of arsenic. Other parameters of the equipment and the procedures of measurement were the same as that of Zhu and co-authors (Zhu et al., 2014).
Ci
Ceq
M/V
(1)
where Ci and Ceq are the initial and equilibrium arsenic concentrations (mg/L), M is the mass of sorbent (g), and V is the volume of the solution (L). The isotherm assays were conducted with a sorbent load of 0.5 g/ 100 mL at pH 2.0 and initial As(III) and As(V) concentrations ranging from 5 to 100 mg/L. All flasks were shaken continuously at 180 rpm for 4 d to maximize the arsenic retention. Then, the samples were filtered through a 0.45-μm filter paper and the suspensions were monitored for As concentrations. The solid phases were characterized using XRD and SEM-EDS. These results were used for estimating the amount of arsenic adsorbed by the jarosites-HA complexes in the acidic biotic system.
2.5. Preparation of biogenic minerals The jarosites (a mixture of ammonium and potassium jarosite) were biosynthesized using S. thermosulfidooxidans grown in Norris medium (Norris and Barr, 1985) (g/L) (MgSO4, 0.5; (NH4)2SO4, 0.4 and K2HPO4, 0.2), supplemented with FeSO4∙7H2O at a final concentration of Fe2+ equal to 50 mM. Then, 60 mg/L HA was added. The reaction systems were incubated at 180 rpm and 45 °C in an incubator shaker for 7 d. 4
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Fig. 4. XRD patterns of arsenopyrite residues bio-oxidized at different times in the absence (a) and presence of (b) 60 mg/L HA.
Fig. 5. XPS spectra of the original arsenopyrite. (a) As (3d5/2), (b) S (2p3/2).
3. Results and discussion
presence of 20–60 mg/L HA, while it decreased with the further addition of more HA (80, 100 mg/L). These results indicate that the presence of a suitable concentration of HA (≤60 mg/L) promoted the biooxidation of sulfur. The further addition of more HA may block the contact of cells with the mineral surface and thus lead to a decrease in [SO42−], as well as in cell growth (Xu et al., 2017). Fig. 1c shows that in the presence of HA, the [FeT]aq was considerably lower than that in the absence of HA. By comparing the changes of the [Fe3+], it can be found that the dissolved Fe was dominated by Fe3+ (Fig. 1d), which may be the result of the rapid biooxidation of Fe2+ (Eq. (2)), and the decrease of [Fe3+]aq at the later stage confirmed the formation of precipitates of ferric arsenate and jarosites (Eqs. (3) and (4)). In contrast, for the sterile controls, the [FeT]aq increased slightly, and Fe existed mainly in the form of Fe2+.
3.1. Effect of HA concentration on the solution parameters The solution parameters in terms of cell density, [SO42−], [FeT], [Fe3+], [AsT], [As(III)], pH and ORP of the sterile control experiments and the bio-oxidation of arsenopyrite by S. thermosulfidooxidans at 45 °C in the presence of various concentration of HA (0–100 mg/L) are shown in Fig. 1. Fig. 1a shows that the cells grew rapidly during the first 2 d, reached a maximum at days 3 or 4, and then decreased. The growth rate increased in the presence of 20–60 mg/L HA, although it decreased with the further addition of more HA (80, 100 mg/L). No notable increase in growth rate of S. thermosulfidooxidans growing on S0 + HA in the basal medium, indicating that HA cannot be utilized as the organic carbon (Fig. S3). Fig. 1b shows that the [SO42−] in the biotic experiments, which was considerably higher than in the abiotic ones, also increased in the
4Fe2 + + 4H+ + O2
H3 AsO4 + Fe3+ 5
Microbial
4Fe3 + + 2H2 O
FeAsO4 + 3H+
(2) (3)
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Fig. 6. XPS spectra of the surface arsenic of arsenopyrite residues bio-oxidized in the absence of HA at days 2 (a), 4 (b), 8 (c), 12 (d), and in the presence 60 mg/L HA at days 2 (e), 4 (f), 8 (g), 12 (h), and in the sterile controls reacted for 12 d in the absence (i) and presence of (j) 60 mg/L HA.
M+ + 3Fe3 + + 2SO4 2 + 6H2 O
MFe3 (SO4) 2 (OH)6 + 6H+
(4)
H3 AsO3 + H2 O+ 2Fe3 +
where M is a monovalent cation, such as NH4+, K+, Na+ or H3O+. Fig. 1e shows that for the bio-oxidation experiments in the presence of HA, the [AsT]aq was always lower than that in the biotic system with no HA added, and the more HA was added, the more [AsT]aq was reduced. Fig. 1f shows that for the bio-oxidation experiments conducted in 20, 40, 60, 80, and 100 mg/L HA, the ratios of [As(III)]aq/[AsT]aq on day 12 were 56.8%, 60.4%, 61.7%, 62.3%, and 60.4%, respectively; and for the bio-oxidation experiment in the absence of HA, the ratio of [As(III)]aq/[AsT]aq on day 12 was 49.5%. This result indicates that the addition of HA is favorable for the accumulation of As(III). For the sterile controls in both the presence and absence of HA, the aqueous As mainly existed as As(III). Fig. 1g and h show that in the presence of HA, the pH values decreased more slowly and the ORP values were always lower, than in the absence of HA. For the sterile controls in the presence of HA, both the pH and ORP values were only slightly lower than that in the absence of HA. A previous study has demonstrated that Fe and As can form complexes with ligands or trace elements of HA (Sharma et al., 2010). These reactions reduced the concentrations of Fe and As in the solution, then led to a slower decline in pH and lower ORP values during arsenopyrite bio-oxidation. The ORP value in the biotic system was mainly determined by the coupling of Fe3+/Fe2+ (Zhang et al., 2015a, 2015b). The comparison showed that the oxidation of the aqueous As(III) to As (V) was highly responsible for the ORP value, and a lower ORP value was beneficial for the stability of As(III). These results are in agreement with Wiertz and co-authors (Wiertz et al., 2006), who reported that the oxidation of As(III) occurred only at a relatively high redox potential (ORP > 450 mV vs. Ag/AgCl) (Eq. (5)).
H3 AsO4 + 2Fe2 + + 2H+
(5)
3.2. Changes in morphology, composition and phase of arsenopyrite The SEM results (Fig. 2 and Fig. S4) show that in the presence of HA, the surface of the arsenopyrite was covered by a loose structure (Fig. 2e), and the elemental constituents of area B were mainly composed by As and Fe. The higher contents of C and O imply that small amounts of HA were adsorbed on the mineral surface. (Fig. 2f). While in the absence of HA, the mineral surface was covered by a fine and dense layer enriched in S, Fe and As (area A), and the most dominant one was S (Fig. 2b). After 12 d of bio-oxidation, the undissolved arsenopyrite was completely covered by a thick and compact product layer (Fig. 2c). In the presence of HA, the residue was covered by a porous layer with many bacteria embedded (Fig. 2g). For the sterile controls in the absence of HA, the mineral surface remained intact after 12 d (Fig. 2d), and only a few products were formed on the mineral surface when 60 mg/L HA was added (Fig. 2h). The FT-IR spectra for the arsenopyrite residues bio-oxidized in the absence and presence of HA at day 4 are shown in Fig. 3. In comparison with the spectra of HA, HA-As(V) and HA-Fe(III), some new bands appeared at 1032, 538 and 470 cm−1 for the residue bio-oxidized in the presence of HA, which were assigned to the CeO, CeOeC and MeeOH stretching of HA (Fakour and Lin, 2014), suggesting again that some HA adsorbed on the mineral surface. Meanwhile, new peaks appeared at 1384 and 628 cm-1, which were attributed to the As-O-HA and Fe-O-HA stretching (Brigante et al., 2010), suggesting the formation of HA-As(V) and/or HA-Fe(III) complexes that adsorbed on the mineral surface. XRD patterns (Fig. 4) show that in the presence of HA, the peaks of 6
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Fig. 7. XPS spectra of the surface sulfur of arsenopyrite residues bio-oxidized in the absence of HA at days 2 (a), 4 (b), 8 (c), 12 (d), and in the presence 60 mg/L HA at days 2 (e), 4 (f), 8 (g), 12 (h), and in the sterile controls reacted for 12 d in the absence (i) and presence of (j) 60 mg/L HA.
scorodite were not found until day 10, the peaks of S0 became weaker at the later stage, and no arsenopyrite was found at day 12 (Fig. 4b). While in the absence of HA, S0 and jarosites were detected at day 3 and scorodite (ferric arsenate) at day 4, then they became the main components, and some remnants of arsenopyrite could also be detected at day 12 (Fig. 4a). These results suggest that the HA clearly promotes the bio-oxidation of arsenopyrite. Compared with the changes of solution parameters, it can be found that the dissolution of arsenopyrite was gradually inhibited with accumulation of S0 and scorodite on the mineral surface, which is in agreement with the literature (Deng et al., 2018; Fantauzzi et al., 2011). Additionally, further oxidation of S0 in an acidic environment (pH < 2.0), as described in Eq. (6), can only be achieved in the presence of sulfur-oxidizing bacteria (Vera et al., 2013; Rohwerder et al., 2003). The presence of HA may bind considerable amounts of dissolved arsenic and iron through formation of amorphous As-Fe-HA complexation (Liu et al., 2011), and these reactions will prevent the formation of scorodite and jarosites.
2S0 (surface ) + 3O2 + 2H2 O
Microbial
2SO4 2 + 4H+
(AsS)2− at 162.30 eV (Nesbitt et al., 1995). The As 3d(5/2) XPS spectra and S 2p(3/2) XPS spectra for the residues are shown in Figs. 6 and 7, respectively. The fitted results (Table S2) show that during arsenopyrite bio-oxidation, the intensities of the peaks of As(-I)-S, As(0) and As(I) gradually decreased, while the intensities of the peaks of As(III)eO and As(V)eO increased (Fig. 6a–h). In agreement with other studies (Corkhill et al., 2008; Schaufuss et al., 2000), these results indicated that the oxidation of arsenic during bio-oxidation of arsenopyrite proceeds with a series of one-electron transfer steps. In addition, as shown by the S 2p(3/2) XPS spectra (Fig. 7 and Table S3), the sulfur species for the residues during bio-oxidation were mainly SO42−, S0 and Sn2−, besides (AsS)2−, regardless of whether HA was present. The intensity of the peak of (AsS)2− decreased more quickly when HA was added, indicating that the presence of HA notably promoted the process. 3.4. Sulfur and iron speciation transformation
(6)
The S K-edge XANES spectra for the residues are shown in Fig. 8, with the fitted results being given in Table 1. By comparison with these reference samples (Fig. 8a), it can be found that during bio-oxidation, the intensity of the peak at 2471.8 eV for arsenopyrite gradually decreased, while the intensity of the peak at 2482.8 eV for SO42− gradually increased, and the presence of HA accelerated these changes (Fig. 8b). Table 1 further shows that the sulfur species of the residues biooxidized in the absence of HA were mainly composed of 88.6% arsenopyrite, 3.8% S0, 3.1% schwertmannite, and 4.5% jarosites at day 1 compared with 91.4% arsenopyrite, 3.0% S0, 2.4% schwertmannite, and 3.2% jarosites in the presence of HA. Then, the content of
3.3. Changes in surface components of arsenopyrite The XPS spectra of the original arsenopyrite (Fig. 5 and Table S1) shows that the surface arsenic species, as shown by the As 3d(5/2) spectra (Fig. 5a), are composed of As(0) (42.00 eV), As(I)-O (43.20 eV) and As(III)-O (44.15 eV), besides the major component As(-I)-S at 41.15 eV [8], and the surface sulfur species, as shown by S 2p(3/2) spectra (Fig. 5b), are composed by S2− (161.35 eV), Sn2- (163.26 eV), S0 (164.20 eV), and SO32− (166.50 eV), besides the major component 7
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Fig. 8. S K-edge XANES spectra of reference samples (a), and arsenopyrite residues bio-oxidized at different times, and in the sterile control reacted for 12 d, in the absence (b) and presence (c) of 60 mg/L HA. Table 1 Fitted results of S K-edge XANES spectra of arsenopyrite residues bio-oxidized at different times, and in the sterile controls leached for 12 d, in the absence (a) and presence (b) of 60 mg/L HA, with different reference spectra. Sample
Percentage of contribution of reference samples (%) S0
Arsenopyrite
1d 2d 4d 8d 12 d SC-12 d
Schwertmannite
Jarosites
R-factor
a
b
a
b
a
b
a
b
a
b
88.6 74.8 45 25.6 19.3 93.6
91.4 65.9 36.3 16.2 7.1 87.4
3.8 10.9 18.4 28.3 25.4 6.4
3.0 8.7 13.6 10.2 9.3 7.9
3.1 6.1 11.8 8.4 9.2 –
2.4 11.3 18.9 18.5 19.4 –
4.5 8.2 24.8 37.7 46.1 –
3.2 14.1 31.2 55.1 64.2 4.7
0.016 0.059 0.028 0.063 0.081 0.022
0.023 0.047 0.041 0.079 0.052 0.014
arsenopyrite decreased, while the other sulfur species gradually increased. After 12 d of bio-oxidation, the sulfur species of the residue were composed of 19.3% arsenopyrite, 25.4% S0, 9.2% schwertmannite, and 46.1% jarosites in the absence of HA, while they were 7.1% arsenopyrite, 9.3% S0, 19.4% schwertmannite, and 64.2% jarosites in the presence of HA. These results demonstrate that in the presence of HA, the surface sulfur was oxidized and transformed faster to schwertmannite and jarosites during bio-oxidation of arsenopyrite, which is consistent with the results of the XRD (Fig. 4) and XPS (Fig. 7) analyses. The Fe L-edge XANES spectra for the residues (Fig. 9) showed that both the L3-edge and L2-edge contained the Fe(II) and Fe(III) absorption peaks, i.e., Ea (706.8 eV) and Eb (708.3 eV) for L3-edge, and Ec (719.9 eV) and Ed (721.9 eV) for L2-edge (Mikhlin and Tomashevich, 2005). The area of the peak for Fe(II) gradually decreased with the
increase in the area of the peak for Fe(III), and this trend became more clear when HA was added (Fig. 9b), indicating that the presence of HA promotes the transformation of Fe(II) to Fe(III) on the mineral surface during arsenopyrite bio-oxidation. The oxidation of Fe(II) is notably slow under acidic conditions but can be catalyzed by many orders of magnitude by acidophilic bacteria, such as A. ferrooxidans and S. thermosulfidooxidans (Millero et al., 1987). Combining with the changes of solution parameters (Fig. 1) and phase transformation (Fig. 3), it can be concluded that the presence of HA in the arsenopyrite bio-oxidation system promotes the growth of bacteria, which ensures the fast generation of Fe3+. On the other hand, HA on the mineral surface can absorb and enrich considerable amounts of Fe3+ (Sharma et al., 2010), thereby ensuring the rapid dissolution of arsenopyrite due to the increased attack of Fe3+ on the mineral.
8
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Fig. 9. Fe L-edge XANES spectra of arsenopyrite residues bio-oxidized at days 4, 8 and 12, and in the sterile controls reacted for 12 d, in the absence (a) and presence (b) of 60 mg/L HA.
Fig. 10. SEM images and EDS analyses of elemental composition of the cells of S. thermosulfidooxidans grown on arsenopyrite at stationary phase (day 4) in the absence (a) and presence (b) of 60 mg/L HA.
9
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Fig. 11. L edge NEXAFS spectra of As(III) (NaAsO2) and As(V) (Na2AsO4) (left), and the dual-energy images of arsenic overlaid on the STXM map of cells that reacted with arsenopyrite for 4 d in the absence (a: As(III), c: As(V)) and presence (b: As(III), d: As(V)) of HA. The color change from purple to red represents the increase of element contents from 0% to 100% (right).
Fig. 12. XRD patterns and SEM images of the biogenetic jarosites (a, c) and jarosites-HA (b, d) used in this study.
3.5. Surface morphology and composition of bacterial cells
adsorbed onto the cells, which may promote arsenic adsorption. Further distribution analysis of arsenic on the single cell surface by STXM (Fig. 11) clearly indicates that more As(III) and As(V) were adsorbed onto the cell surface when HA was added, as shown by the difference in the surface densities of As(III) and As(V) on the cell: 0.78 × 10−5-2.51 × 10−5 g/cm2 and 0.99 × 10−5-3.25 × 10−5 g/cm2 in the presence of HA (Fig. 11b, d), compared with 0.59 × 10−52.18 × 10−5 g/cm2 and 0.65 × 10−5-2.37 × 10−5 g/cm2 in the absence of HA (Fig. 10a, c). According to Sand and co-authors (Sand and Gehrke, 2006), the extracellular polymeric substances (EPS) of acidophilic bacteria can adsorb a high amount of Fe3+ by forming a positively charged adduct during bio-oxidation of metal sulfides, which combines easily with negatively charged HA molecules via an
The differences in surface morphology and composition of the cells of S. thermosulfidooxidans grown on arsenopyrite in the absence and presence of HA were characterized by SEM-EDS (Fig. 10) and STXM (Fig. 11). As shown in Fig. 10, the cells collected in the biotic system in the absence of HA were small with smooth surfaces (Fig. 10a). However, in the presence of HA, the cells were larger and were covered with a flocculent layer (Fig. 10b), which was mainly comprised by C, O, Fe, Na, P, Ca and As according to the EDS analyses, indicating both HA and arsenic adsorbed onto the cells. It is noteworthy that in the presence of HA, the contents of the elements on the surface of cells, especially C, Fe and As, significantly increased. These results demonstrate that some HA 10
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Fig. 13. SEM images (left) and EDS analyses of elemental composition (top right) and in situ content distributions of key elements (bottom right) of the jarosites (a) and jarosites-HA (b) after reaction with As(V) for 4 d.
electrostatic interaction and thus enhances the adsorption of arsenic (Ren et al., 2016). The results of FT-IR (Fig. S5) and μ-XRF (Fig. S6) show the evidence of the bound Fe and As on the cell surface.
obviously increased, with slight decreases in the contents of Fe and S (Fig. 13b), clearly indicating more adsorption of As(V) onto jarositesHA than on jarosites.
3.6. Characterization of arsenic adsorption onto biogenic minerals
3.7. Adsorption kinetics and isotherms of arsenic onto biogenic minerals
The XRD results (Fig. 12a, b) show that the biogenic minerals have the same main component potassium jarosite with small amount of ammoniojarosite, whether there was HA or not. The SEM results, however, show that the biogenic minerals formed in the presence of HA exist with some villous structure covered on the loose mineral surface (Fig. 12d), while in the absence of HA, a polyhedron-shaped and dense structure was formed (Fig. 12c). After adsorption by As(V), the precipitates jarosites and jarosites-HA complexes were further analyzed by SEM-EDS. The results (Fig. 13) show the existence of As besides Fe, S, O, C, N, and K, which were all distributed on the precipitate surface. Compared with the jarosites (Fig. 13a), the contents of C, O and As on the surface of jarosites-HA
To clarify the difference in the adsorption properties of jarosites and jarosites-HA that may affect the fate of arsenic species and thus the biooxidation of arsenopyrite, the adsorption kinetics and isotherms of As (III) and As(V) onto the precipitates above were investigated by batch experiments, and the results are shown in Fig. 14. The kinetics results (Fig. 14a, b and Table S4) show that the arsenic adsorption occurred considerably faster during the initial period and then became slow, finally reached equilibrium after 4320 min (72 h). Compared with the jarosites, the jarosites-HA demonstrated a greater adsorption capacity for both As(III) and As(V), and more adsorption of As(V) than As(III) when pH ≤ 2.0 (Fig. 14b), indicating that the presence of HA promotes more adsorption of As(V) than As(III) in the acidic bioleaching 11
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Fig. 14. Adsorption kinetics (a, b) and isotherm (c, d) of As(III) (a, c) and As(V) (b, d) on jarosites and jarosites-HA, respectively. Table 2 Langmuir and Freundlich adsorption isotherm parameters for the binding of As(III) and As(V) onto jarosites (J) and jarosites-HA (J-HA) at pH 2.0 ± 0.1. Sample
J J-HA J J-HA
Langmuir
As(III) As(III) As(V) As(V)
Freundlich
KL(L/mg)
qm(mg/g)
R2
Chi square
KF
n
R2
Chi square
0.0096 0.0127 0.0132 0.0149
6.22 10.95 7.76 13.62
0.998 0.994 0.997 0.996
0.098 1.103 0.115 1.221
0.1451 0.3568 0.2471 0.4297
0.549 0.606 0.615 0.632
0.932 0.921 0.916 0.924
1.389 9.886 2.714 11.583
environment. The adsorption isotherm results (Fig. 14c, d, Table 2) show that both As(III) and As(V) adsorbed on both jarosites and jarosites-HA are in greater accordance with the Langmuir model (Eq. (7)) than with the Freundlich model (Eq. (8)), indicating that the adsorption occurs on a homogeneous surface with a finite number of identical adsorption sites (Qi et al., 2015). Calculated from the Langmuir equation, the maximum adsorption capacities of As(III) and As(V) were found to be 6.22 and 7.76 mg/g for jarosites, while they were 10.95 and 13.62 mg/g for jarosites-HA, respectively.
qee =
qm KL Ce 1 + KL Ce
qee = KF Ce1/n
4. Conclusions The findings of the present study clearly indicated that the presence of HA could change the physicochemical properties of the surface of arsenopyrite during bio-oxidation and could affect the speciation transformation of iron and sulfur and arsenic immobilization. The specific conclusions are as follows: (i) The presence of HA apparently affects the changes of solution parameters during arsenopyrite bio-oxidation, with enhancement of the growth rate of cells and releasing more [SO42−] but less [FeT] and [AsT], and lower ORP values that may be beneficial for the stability of As(III). (ii) The formation of a porous structure of residue during bio-oxidation of arsenopyrite in the presence of HA benefits the cells’ adsorption and Fe3+ attack on the mineral, which may play an important role in the enhancement of the bio-oxidation of S0 and the dissolution of arsenopyrite. (iii) The adsorption of HA onto the surface of bacteria cells obviously enhances the adsorption of As(III) and As(V), and the jarosites in the presence of HA significantly enhance the arsenic adsorption, and both of them may contribute to the in-situ arsenic immobilization during arsenopyrite bio-oxidation.
(7) (8)
where qe is the concentration of arsenic adsorbed on the solid phase (mg/g), Ce is the equilibrium concentration of arsenic in the aqueous phase (mg/L), KL is the Langmuir sorption coefficient related to the affinity of the binding sites (L/mg), qm is the total concentration of surface sites (mg/g), and KF and n are the Freundlich constants. The results of fitting the Langmuir and Freundlich equations to the isotherm curves are summarized in Table 2. 12
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The results of this study may be useful in selecting management strategies for metal recovery and arsenic disposal in arsenopyrite bearing environment sites.
Mckibben, M.A., Tallant, B.A., Del Angel, J.K., 2008. Kinetics of inorganic arsenopyrite oxidation in acidic aqueous solutions. Appl. Geochem. 23, 121–135. Mikhlin, Y., Tomashevich, Y., 2005. Pristine and reacted surfaces of pyrrhotite and arsenopyrite as studied by X-ray absorption near-edge structure spectroscopy. Phys. Chem. Miner. 32, 19–27. Millero, F.J., Sotolongo, S., Izaguirre, M., 1987. The oxidation kinetics of Fe(II) in seawater. Geochim. Cosmochim. Acta 51, 793–801. Nesbitt, H.W., Muir, I.J., Prarr, A.R., 1995. Oxidation of arsenopyrite by air and airsaturated, distilled water, and implications for mechanism of oxidation. Geochim. Cosmochim. Acta 59, 1773–1786. Norris, P.R., Barr, D.W., 1985. Growth and iron oxidation by acidophilic moderate thermophiles. FEMS Microbiol. Lett. 28, 221–224. Pina, P.S., Oliveira, V.A., Cruz, F.L.S., Leão, V.A., 2010. Kinetics of ferrous iron oxidation by Sulfobacillus thermosulfidooxidans. Biochem. Eng. J. 51, 194–197. Qi, J., Zhang, G., Li, H., 2015. Efficient removal of arsenic from water using a granular adsorbent: Fe-Mn binary oxide impregnated chitosan bead. Bioresour. Technol. Rep. 193, 243–249. Ramírez-Aldaba, H., Valles, O.P., Vazquez-Arenas, J., Rojas-Contreras, J.A., Valdez-Pérez, D., Ruiz-Baca, E., Lara, R.H., 2016. Chemical and surface analysis during evolution of arsenopyrite oxidation by Acidithiobacillus thiooxidans in the presence and absence of supplementary arsenic. Sci. Total Environ. 566, 1106–1119. Rashid, M., Sterbinsky, G.E., Pinilla, M.A.G., Cai, Y., O’Shea, K.E., 2018. Kinetic and mechanistic evaluation of inorganic arsenic species adsorption onto humic acid grafted magnetite nanoparticles. J. Phys. Chem. C. 122, 13540–13547. Ravel, B., Newville, M., 2010. ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12, 537–541. Redman, A.D., Macalady, D.L., Ahmann, D., 2002. Natural organic matter affects arsenic speciation and sorption onto hematite. Environ. Sci. Technol. 36, 2889–2896. Ren, J., Fan, W., Wang, X., Ma, Q., Li, X., Xu, Z., Wei, C., 2016. Influences of size-fractionated humic acids on arsenite and arsenate complexation and toxicity to Daphnia magna. Water Res. 108, 68–77. Rohwerder, T., Gehrke, T., Kinzler, K., Sand, W., 2003. Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl. Microbiol. Biotechnol. 63, 239–248. Sand, W., Gehrke, T., 2006. Extracellular polymeric substances mediate bioleaching/ biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria. Res. Microbiol. 157, 49–56. Schaufuss, A.G., Nesbitt, H.W., Scaini, M.J., Hoechst, H., Bancroft, M.G., Szargan, R., 2000. Reactivity of surface sites on fractured arsenopyrite (FeAsS) toward oxygen. Am. Mineral. 85, 1754–1766. Sharma, P., Ofner, J., Kappler, A., 2010. Formation of binary and ternary colloids and dissolved complexes of organic matter, Fe and As. Environ. Sci. Technol. 44, 4479–4485. Sharma, V.K., Sohn, M., 2009. Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ. Int. 35, 743–759. Vera, M., Schippers, A., Sand, W., 2013. Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation-part A. Appl. Microbiol. Biotechnol. 97, 7529–7541. Wang, S.F., Jiao, B.B., Zhang, M.M., Zhang, G.Q., Wang, X., Jia, Y.F., 2018. Arsenic release and speciation during the oxidative dissolution of arsenopyrite by O2, in the absence and presence of EDTA. J. Hazard. Mater. 346, 184–190. Wiertz, J.V., Mateo, M., Escobar, B., 2006. Mechanism of pyrite catalysis of As(III) oxidation in bioleaching solutions at 30 °C and 70 °C. Hydrometallurgy 83, 35–39. Xu, B., Yang, Y., Li, Q., Jiang, T., Zhang, X., Li, G., 2017. Effect of common associated sulfide minerals on thiosulfate leaching of gold and the role of humic acid additive. Hydrometallurgy 171, 44–52. Yu, Y., Zhu, Y., Gao, Z., Gammons, C.H., Li, D., 2007. Rates of arsenopyrite oxidation by oxygen and Fe(III) at pH 1.8-12.6 and 15-45 degrees C. Environ. Sci. Technol. 41, 6460–6464. Zhang, G., Chao, X., Guo, P., Cao, J., Yang, C., 2015a. Catalytic effect of Ag+ on arsenic bioleaching from orpiment (As₂S₃) in batch tests with Acidithiobacillus ferrooxidans and Sulfobacillus sibiricus. J. Hazard. Mater. 283, 117–122. Zhang, S.Y., Zhao, F.J., Sun, G.X., Su, Q.J., Yang, X.R., Li, H., Zhu, Y.G., 2015b. Diversity and abundance of arsenic biotransformation genes in paddy soils from Southern China. Environ. Sci. Technol. 49, 4138–4146. Zhu, T., Lu, X., Liu, H., Li, J., Zhu, X., Lu, J., Wang, R., 2014. Quantitative X-ray photoelectron spectroscopy-based depth profiling of bioleached arsenopyrite surface by Acidithiobacillus ferrooxidans. Geochim. Cosmochim. Acta 127, 120–139. Zhu, W., Xia, J.L., Yang, Y., Nie, Z.Y., Zheng, L., Ma, C.Y., Qiu, G.Z., 2011. Sulfur oxidation activities of pure and mixed thermophiles and sulfur speciation in bioleaching of chalcopyrite. Bioresour. Technol. Rep. 102, 3877–3882.
Acknowledgements This work was supported by the Joint Funds of NSFC and Liaoning Science Foundation (U1608254), the National Natural Science Foundation of China (No. 51861135305, 41830318, 51774342), the Open Funds of Beijing Synchrotron Radiation Facility (2018-BEPC-PT001390 and 2018-BEPC-PT-001391), and the Open Funds of Shanghai Synchrotron Radiation Facility (2018-SSRF-PT-005070, 2019-SSRF-PT008827). Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.jhazmat.2019.121359. References Alsidcheikh, M., Dia, A., Guenet, H., Vantelon, D., Davranche, M., Delhaye, T., 2015. Interactions between natural organic matter, sulfur, arsenic and iron oxides in reoxidation compounds within riparian wetlands: NanoSIMS and X-ray adsorption spectroscopy evidences. Sci. Total Environ. 515, 118–128. Brigante, M., Zanini, G., Avena, M., 2010. Effect of humic acids on the adsorption of paraquat by goethite. J. Hazard. Mater. 184, 241–247. Celebi, O., Kilikli, A., Erten, H.N., 2009. Sorption of radioactive cesium and barium ions onto solid humic acid. J. Hazard. Mater. 168, 695–703. Corkhill, C.L., Vaughan, D.J., 2009. Arsenopyrite oxidation-a review. Appl. Geochem. 24, 2342–2361. Corkhill, C.L., Wincott, P.L., Lloyd, J.R., Vaughan, D.J., 2008. The oxidative dissolution of arsenopyrite (FeAsS) and enargite (Cu3AsS4) by Leptospirillum ferrooxidans. Geochim. Cosmochim. Acta 72, 5616–5633. Cornejo-Garrido, H., Fernández-Lomelín, P., Guzmán, J., Cervini-Silva, J., 2008. Dissolution of arsenopyrite (FeAsS) and galena (PbS) in the presence of desferrioxamine-B at pH 5. Geochim. Cosmochim. Acta 72, 2754–2766. Coussy, S., Benzaazoua, M., Blanc, D., Moszkowicz, P., Bussière, B., 2011. Arsenic stability in arsenopyrite-rich cemented paste backfills: a leaching test-based assessment. J. Hazard. Mater. 185, 1467–1476. Dave, S.R., Gupta, K.H., Tipre, D.R., 2008. Characterization of arsenic resistant and arsenopyrite oxidizing Acidithiobacillus ferrooxidans from Hutti gold leachate and effluents. Bioresour. Technol. Rep. 99, 7514–7520. Deng, S., Gu, G.H., Xu, B., Li, L., Wu, B., 2018. Surface characterization of arsenopyrite during chemical and biological oxidation. Sci. Total Environ. 626, 349–356. Dopson, M., Lindström, E.B., 2004. Analysis of community composition during moderately thermophilic bioleaching of pyrite, arsenical pyrite, and chalcopyrite. Microb. Ecol. 48, 19–28. Fakour, H., Lin, T.F., 2014. Experimental determination and modeling of arsenic complexation with humic and fulvic acids. J. Hazard. Mater. 279, 569–578. Fantauzzi, M., Licheri, C., Atzei, D., Loi, G., Elsener, B., Rossi, G., Rossi, A., 2011. Arsenopyrite and pyrite bioleaching: evidence from XPS, XRD and ICP techniques. Anal. Bioanal. Chem. 401, 2237–2248. Ide-Ektessabi, A., Kawakami, T., Watt, F., 2004. Distribution and chemical state analysis of iron in the Parkinsonian substantia nigra using synchrotron radiation micro beams. Nucl. Instrum. Meth. B 213, 590–594. Karamanev, D.G., Nikolov, L.N., Mamatarkova, V., 2002. Rapid simultaneous quantitative determination of ferric and ferrous ions in drainage. Miner. Eng. 15, 341–346. Liu, G., Cai, Y., 2013. Studying arsenite-humic acid complexation using size exclusion chromatography-inductively coupled plasma mass spectrometry. J. Hazard. Mater. 262, 1223–1229. Liu, G.L., Fernandez, A., Cai, Y., 2011. Complexation of arsenite with humic acid in the presence of ferric iron. Environ. Sci. Technol. 45, 3210–3216. Márquez, M.A., Ospina, J.D., Morales, A.L., 2012. New insights about the bacterial oxidation of arsenopyrite: a mineralogical scope. Miner. Eng. 39, 248–254.
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