Article pubs.acs.org/est
Arsenite Binding to Natural Organic Matter: Spectroscopic Evidence for Ligand Exchange and Ternary Complex Formation Martin Hoffmann, Christian Mikutta,* and Ruben Kretzschmar Institute of Biogeochemistry and Pollutant Dynamics, Department of Environmental Systems Science, ETH Zurich, CHN, CH-8092 Zurich, Switzerland S Supporting Information *
ABSTRACT: The speciation of As in wetlands is often controlled by natural organic matter (NOM), which can form strong complexes with Fe(III). Here, we elucidated the molecular-scale interaction of arsenite (As(III)) with Fe(III)−NOM complexes under reducing conditions. We reacted peat (40−250 μm size fraction, 1.0 g Fe/kg) with 0−15 g Fe/kg at pH 1.0 g Fe/kg peat exhibit a pronounced signal at k ∼6 Å−1 (SI Figure S9). This signal, originating from second Fe neighbors of As, increased in intensity with increasing Fe content of the peat. Because the speciation of Fe in the peat samples was dominated by mononuclear Fe(III) species, the detection of Fe in the second coordination shell of As is clear evidence for the formation of ternary As(III) complexes. Moreover, we observed weak signals in the WT plots of all peat samples at k ∼3−5 Å−1 and R + ΔR ∼1.9 Å. These features are comparable with that of an As−C single scattering path calculated with FEFF v.8.4,24 which provides first suggestive evidence for a direct association of As(III) with organic C. Although the WT of sodium(meta)arsenite exhibits a similar feature at low k, its precipitation can be excluded since the signal of As backscatterers at k ∼8 Å−1 and R + ΔR ∼2.8 Å is missing in all peat samples (SI Figure S9). Figure 2B−D illustrates the As K-edge EXAFS spectra and their Fourier transforms (magnitudes and real parts) of As(III)reacted peat samples and As(III) sorbed to ferrihydrite. Here, the first peak in the Fourier transforms at R + ΔR ∼1.3 Å is due to O atoms in the pyramidal As(III) molecule. All peat samples with >1.0 g Fe/kg exhibited one to two additional small Fourier transform peaks at R + ΔR ∼2.5 and ∼3.0 Å attributable to Fe neighbors.43 These peaks intensified with increasing Fe content and anticorrelated with the intensity of a small Fourier transform peak at ∼2.2 Å (Figure 2C), whose distance is consistent with C neighbors of As.28,44 The presence of other 12170
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Figure 3. Schematic representation of As(III) complexes identified in this study. For simplicity organic ligands are shown as (A) phenolate and (B, C) oxalate. In (A) As(III) is covalently bound to three phenolate groups. In (B) As(III) binds in a bidentate mononuclear (1E) fashion to a monomeric Fe(III)−oxalate complex and in (C) As(III) forms a monodentate binuclear (2C) ternary complex with a μ3-oxo bridged FeO6 trimer bound to oxalate ligands. Color code: As = purple, Fe = orange, O = blue, and C = black balls.
to Fe(III)−HS complexes at pH 7.10 Our shell-fit results indicate that the fraction of 2C complexes in the peat increased with increasing Fe loading and pH (Table 2), which explains the As(III) sorption trends shown in Figure 2. Taking the nuclearity of the 1E and 2C complexes and their fitted CNs (0.4−0.6 for 1E and 0.3−0.8 for 2C) into account, we can estimate that between 50 and 90% of As(III) is bound in ternary As(III) complexes. Because the precipitation of a minor fraction of Fe(III)-oxyhydroxides at high pH and Fe loadings cannot be fully excluded based on EPR and Fe EXAFS spectroscopy results, we conservatively estimate that only up to 34% of total As could theoretically be adsorbed to these phases. For this estimate we assumed (i) the precipitation of ferrihydrite with a CN of edge-sharing Fe of 3.4,12 (ii) a minimal CN of 0.1 for edge-sharing Fe detectable with Fe EXAFS spectroscopy, (iii) 25% of surface-Fe atoms in ferrihydrite,50 and (iv) the highest molar Fe/As ratio of 46 in the peat. Surprisingly, no ternary As(III) complexes were observed in the peat sample with 1.0 g Fe/kg, despite that this sample sorbed as much as 161 mg As/kg (Figure 2A). Instead of to Fe, As(III) was directly coordinated to organic C of the peat as implied by the observation of 1.7 C atoms at a mean distance of 2.73 Å. This As−C shell was also present in all other peat samples (Table 2). The fitted As−C distances of 2.70−2.77 Å are consistent with As(III) covalently bound to phenolates and aliphatic hydroxylates,44,51,52 and the CNs of the As−C path of 1.5−2.0 indicate that each As(III) is, on average, coordinated to one or two C atoms. However, because EXAFS tends to be insensitive toward weakly scattering atoms, especially when the sorbate exhibits signals of strong backscatterers at a similar distance,53 values of CN(As−C) must be treated with caution. Taking CN(As−C) of the pure peat (Table 2), subtracting the associated fit uncertainty, and assuming a maximum of three C neighbors of As(III), we conservatively estimate that at least 27% of total As(III) was directly bound to the C backbone in the Fe-spiked peat samples. Despite the large uncertainties of the CNs of the As−C path, our data provide the first spectroscopic evidence for a ligand-exchange reaction between oxygen functionalities of NOM and As(III). This mechanism has previously been hypothesized to take place between As(III) and phenolates of humic acid.3 Indeed, the observation that As(III) sorption to pure peat (1.0 g Fe/kg) was independent of pH (Figure 2A) supports a reaction between aliphatic hydroxylic and/or phenolic groups and As(III) according to nR−OH + As(OH)3 ↔ (R−O)nAs(OH)3‑n + nH2O (n ≤3).
Based on the interatomic As−C distances, we can exclude negatively charged adducts stabilized by H-bonds, formed between As(III) and carboxylates as proposed by Buschmann et al.3 In such adducts, the As−C distances would be considerably shorter and comparable to distances in As(III)-tricarboxylates (2.58−2.68 Å).28,54 In summary, our results show that As(III) reacts with peat by the formation of ternary As(III) complexes, which is accompanied by covalent bond formation between As(III) and aliphatic hydroxylic/phenolic groups of NOM. The As(III) complexes identified in this study are schematically summarized in Figure 3. Environmental Significance. Our spectroscopic analyses showed that NOM can effectively bind As(III) under reducing conditions through a ligand exchange reaction and ternary complex formation. In addition to As(III) binding to sulfhydryl groups of NOM, 8 these so far unconfirmed sorption mechanisms may have an important bearing on the environmental fate of the metalloid, especially in NOM-rich soils and sediments. While the association of As(III) with particulate NOM potentially leads to a reduced mobility and thus bioavailability, the contrary can be expected for colloidal and dissolved NOM species. Many observations made in field or field-related studies can be explained by the two As(III) sorption mechanisms identified in this study. Examples include correlations between dissolved As and dissolved NOM released from ombrotrophic peatlands during flooding events,6 anticorrelations between solid-phase As and Fe (Mn) in watersaturated peat bogs,51 and the simultaneous mobilization of As with NOM from wetland soils in percolation and extraction experiments.55,56 Ligand exchange and ternary complex formation of As(III) may also account for the strong correlation observed between dissolved As(III) and dissolved NOM in a blackwater system,57 a significant correlation between solidphase NOM and As in moderately reducing sediments of the Chianan Plain, Taiwan,58 and the association of As(III) with organic colloids in groundwaters of the Hetao basin, Inner Mongolia.59 Furthermore, the observed ligand-exchange mechanism may clarify the binding of As(III) to S(-II)-reacted peat and HS where As(III) retained its first-shell oxygens7 and the As(III)-dependent fluorescence quenching of HS extracted from mangrove forest sediments.60
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ASSOCIATED CONTENT
S Supporting Information *
Influence of temperature on the quality of Fe K-edge EXAFS spectra, synchrotron XRD patterns, EPR spectra, first derivatives of normalized Fe and As K-edge XANES spectra, 12171
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wavelet transforms of Fe and As K-edge EXAFS spectra, shell fits of Fe and As K-edge EXAFS spectra of reference compounds, As K-edge EXAFS shell-fit tests for the peat samples, and alternative Fe and As K-edge EXAFS shell-fit models. This information is available free of charge via the Internet at http://pubs.acs.org/.
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AUTHOR INFORMATION
Corresponding Author
*Phone: +41-44-6336024; fax: +41-44-6331118; e-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We are grateful to P. Langner, K. Ehlert, and P. Mandaliev (ETH Zurich) for their help during the synchrotron measurements. We are indebted to K. Barmettler and E. Süß (ETH Zurich) for analytical support, and to graduate students E. Ibrahim, L. Burger, and S. Tanner (ETH Zurich) for their help with the peat fractionation. We thank G. Jeschke (ETH Zurich) for the opportunity to collect EPR spectra. Iron K-edge XAS experiments were in part performed at the light source DORIS III at HASYLAB, a member of the Helmholtz Association. We are grateful to E. Welter for assistance in using beamline C. We also acknowledge the ESRF for the provision of synchrotron radiation facilities and thank S. Nikitenko, D. Banerjee, and C. Strohm for providing support in using beamlines BM23 and BM26A. We also thank A. Cervellino for his help during the synchrotron XRD experiments at beamline X04SA of the SLS. The sampling permission for Federseemoor was granted by J. Einstein (NABU - Naturschutzbund Deutschland e.V.) and financial support of this study was provided by ETH Zurich (research grant 2708-2).
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