Sulfate-Reducing Bacteria Mobilize Adsorbed Antimonate by

Letter Cite This: Environ. Sci. Technol. Lett. 2019, 6, 418−422

pubs.acs.org/journal/estlcu

Sulfate-Reducing Bacteria Mobilize Adsorbed Antimonate by Thioantimonate Formation Li Ye,†,‡ Haoze Chen,†,‡ and Chuanyong Jing*,†,‡ †

State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China ‡ College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China

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S Supporting Information *

ABSTRACT: The biogeochemical cycling of antimony (Sb) is often coupled with sulfur and sulfate-reducing bacteria (SRB). The biogenic sulfide is usually assumed to facilitate Sb immobilization via Sb2S3 precipitation. Here, on the contrary, we discovered that SRB mobilize adsorbed Sb(V). When SbV(OH)6−bearing goethite was incubated anaerobically with Desulfovibrio vulgaris DP4, an elevated level of antimony was released due to the formation of thioantimonate, which is the dominant Sb species in solution. Our Fourier transform ion cyclotron resonance mass spectrometry analysis revealed multiple six- or five-coordinate thioantimonate intermediates, suggesting stepwise ligand exchange of hydroxyl groups on SbV(OH)6− by biogenic sulfide. Direct H2S elimination reactions resulted in four-coordinate thioantimonate species as the stable end product, which was confirmed by our density functional theory calculations. The thiolation of antimonate is pH-dependent and occurs in neutral environments. The thiolation changed Sb(V) from a six-coordinate octahedral coordination to a four-coordinate tetrahedral coordination, weakening its affinity for iron oxides and thus facilitating its release into the aquatic environment. The results of this study highlight the importance of biogenic sulfide produced by SRB for the fate and transport of Sb.

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and pH 9.3).15 However, limited knowledge of thioantimony formation and its role in the fate and transport of Sb is available. The purpose of this study was to explore the fate of SbV(OH)6− adsorbed on goethite during the coupled Sb−S transformation process mediated by the sulfate-reducing bacterium Desulfovibrio vulgaris DP4. Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS) and anion-exchange chromatography inductively coupled plasma mass spectrometry (IC-ICP-MS) were used to identify and quantify Sb species. The thioantimonate formation pathway was discovered and confirmed by density functional theory (DFT) calculations. This study presents direct evidence that the formation of biogenic thioantimonate increases the extent of Sb mobilization.

INTRODUCTION The biogeochemical cycling of antimony (Sb) is usually coupled with sulfur (S) due to its chalcophilic nature.1,2 As stibnite (Sb2S3) is the primary ore of Sb,3 the formation of Sb2S3 is generally believed to be related to the activities of sulfate-reducing bacteria (SRB).4 Indeed, laboratory experiments have provided evidence of the Sb2S3 precipitation mediated by SRB in subsurface environments,5,6 and microbial sulfate reduction has been proposed as an alternative for removing Sb from wastewater by the formation of Sb2S3.7,8 On the other hand, elevated Sb concentrations have been reported under sulfate-reducing conditions in seawater9 and a pit lake.10 The seemingly contradictory observations remind us of the paradox of thiolation in the mobilization of arsenic,11−13 an extensively studied element in the same group in the periodic table. Similar to aqueous thioarsenic species, thioantimony species can also exist in solutions that contain sulfide.14 Our thermodynamic calculations suggest that thioantimony species are in fact predominant at neutral pH when the antimonate [SbV(OH)6−] concentration is 0.1 mM (Figures S1 and S2). This concentration constraint is readily satisfied in most Sbcontaminated water samples (0.01−190 μM Sb and 0.6−20 mM S) except for some mine drainages, as summarized in Table S1. Thioantimony species have also been detected in geothermal water samples (0.45−0.62 μM Sb, 0.06−0.1 mM S, © 2019 American Chemical Society

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MATERIALS AND METHODS Bacterial Strains and Materials. As a sulfate-reducing bacterium (99% similar, GeneBank accession number CP000527),16 D. vulgaris DP4 uses sulfate as a terminal electron acceptor, resulting in the production of sulfide.17 The specific components of the culture medium containing sulfate for DP4 are detailed in the Supporting Information. Received: June 10, 2019 Accepted: June 20, 2019 Published: June 20, 2019 418

DOI: 10.1021/acs.estlett.9b00353 Environ. Sci. Technol. Lett. 2019, 6, 418−422

Letter

Environmental Science & Technology Letters

Figure 1. Changes in total dissolved antimony (black), antimonate (red), trithioantimonate (green), and tetrathioantimonate (blue) as a function of incubation time in (a) DP4+Goe-Sb, (b) Goe-Sb, and (c) inactivated DP4+Goe-Sb.

were quantified on the basis of SbV(OH)6− as suggested by a previous study.15 FT-ICR MS Analysis. Both the separated Sb species from IC (Figure S6) and the formed Sb species during the reaction between SbV(OH)6− and sulfide were assessed by FT-ICR MS. The thioantimonate formation process was studied by reacting 1 mM SbV(OH)6− with 2 mM sulfide at pH 7.5. The SbV(OH)6− concentration was set as 1 mM rather than 10 μM in the DP4 system to increase the concentration of the intermediates for FT-ICR MS analysis. Analysis of the reaction between 10 μM and 2 mM sulfide at pH 7.5 by FT-ICR MS was also attempted, but the signals of Sb species were too weak to observe (Figure S7). The reactions between SbV(OH)6− and sulfide at five pH values (11.5, 10.5, 9.5, 8.5, and 7.5) and four S:Sb molar ratios (40:1, 20:1, 4:1, and 2:1) were also analyzed by FT-ICR MS. Details about FT-ICR MS experimental conditions are provided in the Supporting Information. Density Functional Theory (DFT) Calculations. Transformation reactions of Sb species were investigated using Gaussian 09.24 The equilibrium geometries were optimized using the B3LYP hybrid functional with the LANL0825 basis set for Sb and 6-311+G(d, p) for S, O, and H atoms. The electronic energies of optimized structures were recalculated with the SMD solvation model using a higher-level basis set of aug-cc-pVTZ-PP26 for Sb and aug-cc-pVTZ27 for S, O, and H atoms. The Gibbs free energies (G) for the structure-optimized thioantimonates were determined by adding the electronic energy terms in B3LYP/aug-cc-pVTZ-PP/aug-cc-pVTZ levels, the zero-point vibrational energy (ZPE) corrections, and thermal corrections (from 0 to 298.15 K). The Gibbs free energy changes (ΔG) for the target reactions were then calculated from the resulting G values.

Goethite (α-FeOOH) was selected to represent a natural adsorbent for Sb.18 Goethite was synthesized according to the modified method of Schwertmann and Cornell19 and validated by X-ray powder diffraction (XRD) (Figure S3) as detailed in the Supporting Information. Antimonate [SbV(OH)6−] was first loaded on goethite at a concentration of 12 mmol/kg to simulate the Sb species and content in natural contaminated soils.18,20,21 The details of the Sb loading procedure are provided in the Supporting Information. Incubation Experiments. Inoculation and sampling were conducted inside an anaerobic glovebox (100% N2). DP4 was activated in an incubator at 30 °C to the logarithmic phase. Then, DP4 was inoculated [0.5% (v/v)] into culture medium (100 mL) containing 1 g/L goethite-Sb solid and labeled as DP4+Goe-Sb. Triplicate samples were incubated in anaerobic bottles closed with sterilized rubber stoppers. Abiotic controls (labeled as Goe-Sb) were prepared following the same procedures that were used for the DP4+Goe-Sb system without DP4 inoculation. Except for sampling, the bottles were placed in the dark without agitation during the incubation process (168 h) at 30 °C. A 1.6 mL sample was taken in a glovebox with a sterile syringe and passed through a 0.22 μm membrane filter. Approximately 0.5 mL of a filtered sample was flash-frozen in liquid nitrogen and stored at −80 °C until Sb speciation analysis. The remaining sample (∼1 mL) was used for pH (LE438 pH electrode, Mettler Toledo) and Eh (9678BNWP ORP electrode, Thermo Scientific) measurements. Then, the sample was diluted 10 times for sulfide, ferrous, and total Fe analysis. Sulfide was assessed with the methylene blue method, and Fe(II) and total Fe concentrations were quantified using the colorimetric 1,10-phenanthroline method.22 Total dissolved Sb concentrations were analyzed by inductively coupled plasma mass spectrometry (ICP-MS, NexION350X, PerkinElmer). The solids at the end of the incubation were collected by centrifugation at 16000g (12000 rpm, model 5424, Eppendorf, Hamburg, Germany) and washed three times with autoclaved deionized water. The solid samples were then freeze-dried for X-ray absorption fine structure (XAFS) spectroscopic analysis as described in the Supporting Information. Antimony Speciation Analysis. The filtrate samples that had been stored at −80 °C were thawed in a glovebox prior to analysis.15,23 The Sb species were separated by a DX-1100 ion chromatograph (IC, Dionex, Sunnyvale, CA) with an AG16/ AS 16 IonPac column before quantification via ICP-MS. The mobile phase was 70 mM KOH with a flow rate of 1.2 mL/ min. The chromatogram of IC-ICP-MS is shown in Figure S5. Due to the lack of available standards, thioantimony species

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RESULTS AND DISCUSSION Sb Mobilization Mediated by DP4. Figure 1 shows the concentration of Sb species as a function of time in the presence of D. vulgaris DP4. The biogenic sulfide induced goethite dissolution and reduction of Fe(III) to Fe(II) (Figure S8a,b),28 leading to the initial Sb release as suggested by the positive correlation between soluble Fe and Sb concentrations [p < 0.001 (Figure S8c,d)]. The equilibrium Sb concentration with DP4 [11.6 μM, DP4+Goe-Sb (Figure 1a)] and its rate of increase were higher than those in the non-inoculated control [3.8 μM, Goe-Sb (Figure 1b)]. The inactivated DP4 cells did not enhance Sb release as evidenced by the comparable dissolved Sb concentrations in Goe-Sb [3.8 μM (Figure 1b)] and in inactivated DP4+Goe-Sb [3.9 μM (Figure 1c)]. The DP4-facilitated increase in Sb concentration was mainly 419

DOI: 10.1021/acs.estlett.9b00353 Environ. Sci. Technol. Lett. 2019, 6, 418−422

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Environmental Science & Technology Letters attributed to the transformation from SbV (OH) 6 − to thioantimonate species (Figure S9). The formation of thioantimonate reportedly takes place through the oxidation of thioantimonite, the product of reaction of antimonite [Sb III (OH)3 ] with sulfide.15 In our system, however, thioantimonate was derived directly from reacting SbV(OH)6− with biogenic sulfide, because DP4 itself is unable to enzymatically reduce SbV(OH)6− to SbIII(OH)3 (Figure S10). Thioantimonate species were identified by FT-ICR MS as tetrathioantimonate (H3−xSbVS4x−, where x = 1−3) and trithioantimonate [H3−xSbVOS3x−, where x = 1−3 (Figure S6)] in chemical reactions, whose oxidation states [Sb(V)] are consistent with the extended X-ray absorption fine structure (EXAFS) analysis in previous studies.14,15 Interestingly, H3−xSbVOS3x− and H3−xSbVS4x− are stable in the sulfatereducing environment [∼2 mM S2− (Figure S11)], and this observation provides a plausible explanation for the occurrence of Sb(V) in anoxic waters.29 Contrary to previous studies,5,8 we discovered that the formation of biogenic thioantimonate species (H3−xSbVS4x− and H3−xSbVOS3x−) induced the mobilization of solid-bound Sb(V). Formation of thioantimonate shifts the weakly bound Sb(V) further toward the aqueous phase, which leads to a netto mobilization compared to the Goe-Sb control. This observation was ascribed to the weak affinity of H3−xSbVS4x− and H3−xSbVOS3x− for iron oxides. In fact, the total concentration of thioantimonate remained constant during the Fe precipitation process (Figure S8), implying that it did not adsorb on or co-precipitate with Fe(III) precipitates. Fe(III) precipitated as ferrihydrite as evidenced by Fe XANES (Figure S12 and Table S3) and Mössbauer analysis (Figure S13 and Table S4). Even though the biogenic ferrihydrite has a surface reactivity higher than that of goethite,30 the uptake of thioantimonate was not improved. The weak affinity of H3−xSbVS4x− and H3−xSbVOS3x− for iron minerals can be attributed to their coordination chemistry. Unlike SbV(OH)6− where Sb is coordinated with six hydroxyl groups, the Sb coordination in H3−xSbVS4x− is completed by four thiol groups, and Sb in H3−xSbVOS3x− is bonded to three thiol groups and one hydroxyl group.15 The change from octahedron to tetrahedron makes thioantimonate structurally incompatible with the octahedral geometry of goethite, thus preventing its incorporation into the goethite structure compared with SbV(OH)6−.31 In addition, tetrathioantimonate may be 3 times more negatively charged (SbVS43−) than antimonate [Sb(OH)6−] if its pKa values are analogous to that of tetrathioarsenate (pKa3 = 5.2),32 which would hinder its adsorption. On the other hand, the larger size and lower electronic density of the SH− group compared to those of the OH− group may inhibit surface complex formation. Thioantimonate Formation Pathway. The thiolation process was studied by reacting SbV(OH)6− with sulfide from pH 11.5 to 7.5 (Figures S14−S16) and at S:Sb ratio from 2 to 40 (Figure S17) using FT-ICR MS. Figure 2 shows the proposed pathway for thioantimonate formation with the ΔG for each step. Initially, soluble Sb species existed as six-coordinate SbV(OH)6− as evidenced by the peaks at m/z 222.92080 and 224.92120 (Figure S15a). The intensity ratio of these two peaks corresponded well to the natural isotopic distribution of Sb (100:75 121Sb:123Sb). When SbV(OH)6− reacted with sulfide, its four OH− groups were replaced with HS− to form six-coordinate thioantimonate [SbV(OH)2(SH)4−], resulting in

Figure 2. Equilibrium structures of the six main Sb molecular ions, possible reactions during the thioantimonate formation process, and reaction ΔG values were calculated using the density functional theory (DFT) method.

two peaks at m/z 330.79332 and 332.79371 [SbV(OH)2(SH)2(SNa)2− (Figure S15k)], as shown in reaction 1. SbV (OH)6− + 4HS− + 4H+ → SbV (OH)2 (SH)4 − + 4H 2O

(1)

This nucleophilic substitution reaction was exothermic [ΔG = −377.1 kJ/mol (Figure 2, I)], indicating that the substitution of OH− with SH− is energetically favorable. The SH − substitution may occur stepwise because the intermediates, SbV (OH) 5(SH)− and SbV (OH) 4(SH) 2−, were detected (Figure S16). In the second step, SbV(OH)2(SH)4− readily transformed to five-coordinate SbVS(OH)(SH)3− [SbVS(OH)(SH)(SNa)2− (Figure S15j)] through a spontaneous H2O elimination reaction [ΔG = −52.3 kJ/mol (Figure 2, II)]. Then, the newly formed SbVS(OH)(SH)3− transformed to SbVS(SH)4− via ligand exchange of OH− for SH− as in the third step, as evidenced by the peaks at m/z 350.74185 and 352.74225 [SbVS(SH)(SNa)3− (Figure S15m)] [ΔG = −109.8 kJ/mol (Figure 2, III)]. Unlike the unstable SbV(OH)2(SH)4−, the two five-coordinate thioantimonates [SbVS(OH)(SH)3− and SbVS(SH)4−] were still observable after 2 min (Figure S15j,m). Subsequently, SbVS(OH)(SH)3− and SbVS(SH)4− would lose an H2S and transform into four-coordinate H2SbVOS3− (Figure S15f) [ΔG = −68.5 kJ/mol (Figure 2, IV)] and H2SbVS4− (Figure S15g−i) [ΔG = −70.2 kJ/mol (Figure 2, V)], respectively. These spontaneous elimination reactions (Figure 2, II, IV, and V) led to the decrease in the Sb coordination number from six to four, and the four-coordinate thioantimonate was the final end product. Consistent with our results, four-coordinate thioantimonate was also identified by EXAFS.14,15 In the final step, H2SbVOS3− would transform into H2SbVS4− in a sulfide solution [ΔG = −111.5 kJ/mol (Figure 2, VI)]. The spontaneous transformation explained why H3−xSbVS4x−, 420

DOI: 10.1021/acs.estlett.9b00353 Environ. Sci. Technol. Lett. 2019, 6, 418−422

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Environmental Science & Technology Letters instead of H3−xSbVOS3x−, was the main thioantimonate species in the microbial sulfate-reducing environment (Figure 1a). The overall thiolation reaction is written as eq 2.

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SbV (OH)6− + 4HS− + (5 − x)H+ → H3 − xSbV S4 x − + 6H 2O

(2)

In fact, this reaction was thought to be infeasible in a previous experiment conducted at pH 11.15 In line with the proton consumption in eq 2, the concentration of H3−xSbVS4x− increased when the pH decreased from 11.5 to 7.5 as evidenced by IC-ICP-MS (Figure S20). Meanwhile, the pH in the DP4+Goe-Sb system slightly increased from 7.5 to 8.2, whereas the pH in the control without Sb V (OH) 6 − (DP4+Goe) remained relatively constant [pH 7.5−7.7 (Figure S22)]. Our study discovered a new thioantimonate formation pathway by direct substitution reactions between SbV(OH)6− and sulfide. The reaction is pH-dependent and occurs in neutral environments. SRB mobilize the adsorbed Sb(V) by mediating the formation of thioantimonate, which is the primary soluble Sb species. The insight gained from our study helps in the deciphering of the complex biogeochemistry of antimony coupled with sulfur.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.estlett.9b00353. Details of microbial culture medium, XRD analysis, adsorption experiments, FT-ICR MS spectra, XANES analysis, and additional tables and figures (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: +86 10 6284 9523. Fax: +86 10 6284 9523. E-mail: [email protected]. ORCID

Chuanyong Jing: 0000-0002-4475-7027 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors acknowledge the financial support of the National Basic Research Program of China (2015CB932003), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB14020201), and the National Natural Science Foundation of China (41877378 and 41425016).

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