Copper Redox Transformation and Complexation by Reduced and

Sep 19, 2013 - Natural organic matter (NOM) exerts strong influence on copper speciation and bioavailability in soils and aquatic systems. In redox-dy...
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Copper Redox Transformation and Complexation by Reduced and Oxidized Soil Humic Acid. 1. X‑ray Absorption Spectroscopy Study Beate Fulda,† Andreas Voegelin,*,‡ Felix Maurer,† Iso Christl,† and Ruben Kretzschmar† †

Institute of Biogeochemistry and Pollutant Dynamics, ETH Zurich, CHN, CH-8092 Zurich, Switzerland Eawag, Swiss Federal Institute of Aquatic Science and Technology, CH-8600 Dübendorf , Switzerland

‡

S Supporting Information *

ABSTRACT: Natural organic matter (NOM) exerts strong influence on copper speciation and bioavailability in soils and aquatic systems. In redox-dynamic environments, electron transfer reactions between copper and redox-active moieties of NOM may trigger Cu(I) and Cu(0) formation. To date, little is known about Cu-NOM redox interactions and Cu(I) binding to NOM. Here, we present X-ray absorption spectroscopy results on copper redox transformations upon addition of Cu(II) or Cu(I) to untreated and electrochemically reduced soil humic acid (HA) under oxic and anoxic conditions. Both untreated and reduced HA mediated copper redox transformations. Under anoxic conditions, Cu(II) and Cu(I) added to reduced HA were primarily complexed and thereby stabilized as Cu(I)-HA at low loadings, whereas high copper loadings resulted in the additional formation of Cu(0) nanoparticles (16−64% of total copper). Cu(I) bound to HA was predominantly 2-fold coordinated and to a lower extent 3- to 4-fold coordinated, with a contribution of at least one nitrogen and/or sulfur ligand group. Under oxic conditions, Cu(II)-HA complexes prevailed, but smaller fractions of copper were also stabilized as Cu(I)-HA in a 3- to 4-fold coordination. Our results show that Cu-HA redox interactions are strongly affected by binding of Cu(II) and Cu(I) to HA and that HA contributes to the stabilization of Cu(I) against disproportionation.

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that shortly after flooding, Cu(II) was reduced to Cu(I) and even Cu(0),16,17 which was attributed to Cu(II) reduction in the course of microbial detoxification. In another study, Cu(II) was shown to be reduced by redox-active moieties of NOM,18 as reported previously for other redox-active elements like Fe, Hg, Ag, and As.19−22 Untreated Suwannee River fulvic acid was able to reduce Cu(II) to Cu(I) even under oxic conditions.18 Since humic substances are known to reversibly accept electrons during microbial respiration,23,24 the electron donating capacity (EDC) of NOM is expected to be even higher under reducing conditions which may promote metallic Cu(0) formation. Free aqueous Cu+ ions are considered to be rather unstable due to rapid oxidation to Cu2+ and disproportionation to Cu(0) and Cu2+.25,26 However, Cu(I) can be stabilized by complexation as shown for chloride27 and natural organic ligands in estuarine systems.28 Compared to Cu(II), binding of Cu(I) by organic ligands is expected to be significantly different due to its higher thiophilicity, suggesting that Cu(I) forms strong complexes with reduced organic sulfur.29 Thiol-containing

INTRODUCTION Copper (Cu) is an essential trace element for most living organisms as it is important for the viability of a variety of proteins and enzymes that carry out fundamental biological functions.1 In terrestrial and aquatic systems, copper is involved in important biogeochemical cycles such as methane oxidation and denitrification.2,3 However, elevated copper concentrations are toxic to most bacteria4 and plants5 as free copper ions can catalyze the formation of reactive oxygen species that cause oxidative cell damage.6 The bioavailability of copper is therefore an important factor for ecosystem functioning. Strong copper binding by natural organic matter (NOM) is one of the key factors controlling copper bioavailability in soils.7 Binding of Cu(II) to NOM has been intensively studied over the past decades.8−12 Five- to six-membered ring chelates formed by closely spaced carboxyl and hydroxyl groups were shown to be the dominant form of Cu(II)-NOM complexes.11 At low Cu-to-C ratios (90%), irrespective of copper loading and oxidation state of added copper. We assume that copper was dominantly Cu(I) in these samples when brought into contact with O2 (one hour after copper addition in the glovebox) because reduction of Cu(II) to Cu(I) by fulvic acid was shown to be a fast process, occurring on the time scale of minutes,18 while according to our companion study37 Cu(0) formation in the presence of HA was apparently a fairly slow process. Our results show that most Cu(I)-HA complexes present under anoxic conditions were unstable under oxic conditions. Page et al.54 recently reported that oxygenation of a reduced humic acid solution in the dark led to the formation of reactive oxygen species, which may have acted as strong Cu(I) oxidants in our experiments. The 10907

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Table 3. Shell Fitting Results for k3-Weighted EXAFS Spectra of Model Compounds and Sample L1-redanox and H1-untranoxg compound

S02

ΔE0 (eV)

Cu(II)-malate Cu(I)-2S Cu(I)-3S L1-redanox

0.91 ± 0.23 1.01 ± 0.08 1.02 ± 0.10 0.98b

−3.88 ± 3.30 −5.83 ± 0.99 −5.94 ± 1.10 −5.22c

H1-untranox

0.98b

−5.22c

path

CN

Cu−O Cu−S Cu−S Cu−O(N)f Cu−S(Cl)f Cu−O(N)f Cu−S(Cl)f

a

4 2a 3a 1.0 1.1 1.8 0.8

± ± ± ±

0.2 0.2 0.3 0.3

R (Å)

σ2 (10‑3 Å2)

NSSR (%)

± ± ± ± ± ± ±

3.9 ± 2.7 3.7 ± 0.7 10.4 ± 1.1 3.9d 7.1e 3.9d 7.1e

0.8 0.2 0.3 1.5

1.94 2.15 2.26 1.93 2.25 1.92 2.22

0.02 0.01 0.01 0.02 0.01 0.01 0.02

1.3

Fixed according to crystal structure. bAverage S02 of the reference compounds. cAverage ΔE0 of the reference compounds. dDebye−Waller factor of Cu−O in Cu(II)-malate. eAverage Debye−Waller factor of Cu−S in Cu(I)-2S and Cu(I)-3S. fTheoretical scattering paths for Cu−O and Cu−S were used for shell-fitting but may also represent contributions from Cu−N and Cu−Cl, respectively, due to the similar EXAFS phase and amplitude functions of elements with similar atomic number. gShell fitting was performed in R-space over the first coordination shell (k-range 2.5−9.5, dk = 2.5; R+ΔR-range 0.9−2.3). a

represented by the linear Cu(I)-OCl reference (rather than the Cu(I)-2Cl or Cu(I)-2S references) (Table 2). The fraction of 3- and 4-fold coordinated Cu(I) was represented equally often by reference compounds with mixed O/N- and S-coordinated Cu(I) or exclusively S/Cl-coordinated Cu(I). The mixture of O/N and S/Cl in the first coordination shell caused substantial dampening or even extinction of the first-shell EXAFS oscillations in the higher k-range due to destructive interferences of O/N and S/Cl signals (Figure 2a), which is particularly evident in the L2-redanox and L1-redanox spectra (Figure 2c and e). We investigated the mode of Cu(I)-HA coordination in more detail by fitting the k3-weighted EXAFS spectra of the L1redanox and H1-untranox samples over the first coordination shell (R+ΔR-range of 0.9−2.3 Å). We selected these samples because the content of Cu(0) was negligible and copper speciation was dominated by 80% (L1-redanox) and 60% (H1untranox) Cu(I) according to XANES LCF analysis (Figure 1, SI Table S2). The amplitude reduction factor (S02), the energyshift parameter (ΔE0), and the Debye−Waller factor (σ2) for Cu−O and Cu−S single scattering paths were derived from well-defined reference compounds (Cu(II)-malate, Cu(I)-2S, and Cu(I)-3S). The fits and the corresponding EXAFS parameters are presented in Table 3 and SI Figure S6, respectively. The fitted distances for Cu−O and Cu−S paths in the reference compounds were in line with their theoretical crystallographic structure.56−58 The shell-fit for L1-redanox suggested that copper was on average coordinated by 1.0 O/ N atoms at a distance of 1.93 Å and by 1.1 S/Cl atoms at a distance of 2.25 Å. For the H1-untranox sample Cu−O/N and Cu−S/Cl coordination numbers of 1.8 and 0.8 with distances of 1.92 Å and 2.22 Å were determined, respectively. Similar values were also obtained when the coordination numbers and interatomic distances were calculated from the EXAFS LCF fractions and the structural information of the included reference compounds (SI Table S6). The fitted Cu−S/Cl distance of 2.25 Å in the L1-redanox sample matched the average distance known for 3-fold S-coordinated Cu(I) complexes,59 rather than that of Cu−S/Cl distances in linear coordinated complexes, which is typically less than 2.20 Å.60,61 Considering that copper in sample L1-redanox was predominantly Cu(I), the low fitted oxygen and sulfur coordination numbers pointed to the presence of Cu(I) in both coordination geometries in line with XANES and EXAFS LCF results. Since we found in our companion study that more than 99% of total Cu(I) was strongly bound to the humic acid,37 Cu(I) is expected to be coordinated to at least one ligating HA atom.

environment and discuss coordination geometry and types of neighboring atoms in detail. Linear combination fitting of the XANES spectra of samples with significant Cu(I) fractions suggested the presence of a mixture of 2-fold and 3- to 4-fold coordinated Cu(I) complexes (Figure 1b-e, SI Figure S2). These Cu(I) coordination geometries are distinguishable by their differences in the normalized absorption amplitude of the 1s→4p transition peak at 8982−8984 eV, which is most pronounced in the 2-fold near linearly coordinated Cu(I) compounds, and the shape of the XANES spectra on the higher energy side of the 1s→4p transition peak50,55 (Figure 1a). Based on XANES LCF, 60− 70% of the Cu(I) fraction in anoxic HAred were fitted by 2-fold coordinated references (Figure 1d-e, SI Table S3). In anoxic HAuntr, the fraction of 2-fold coordinated Cu(I) was slightly lower, and in the aerated samples, only 3- to 4-fold coordinated Cu(I) reference compounds appeared in the best XANES LCF. Although EXAFS analysis in general provides sensitive information on the type of neighboring atoms, it should be noted that differing backscattering properties of the neighboring atoms are a prerequisite since EXAFS does not allow differentiating between atoms with similar atomic number due to their similar phase and amplitude functions. Consequently, Cu−O vs Cu−N and Cu−S vs Cu−Cl coordination cannot be distinguished unequivocally. Furthermore, high intensity of the EXAFS oscillations of metallic copper overlay with the oscillations of lighter neighboring atoms and complicate the analysis of Cu(I) coordination. Therefore, we will discuss the Cu(I) coordination environment with respect to the type of neighboring atoms based on the EXAFS spectra of samples which were dominated by Cu(I) and did not contain Cu(0). The position of the major Fourier-transform peak in L2redanox and L1-redanox spectra (80% Cu(I) in XANES LCF) pointed to the presence of S/Cl neighbors in the first coordination shell (Figure 2f). Compared to spectra where Cu(II) was the dominant oxidation state and the major Fouriertransform peak at ∼1.5 Å (R+ΔR) corresponded to O/N atoms in the first coordination shell, the first shell peak in the L2redanox and L1-redanox was shifted to the 1.5−2.2 Å R+ΔRrange, which indicates S/Cl neighboring atoms. This shift was also present but less apparent in H1-untranox (62% Cu(I) in XANES LCF) (Figure 2d). Correspondingly, these spectra were accurately described by a linear combination of Cu(II)-O/ N and Cu(I) references containing S/Cl atoms in the first coordination shell. In agreement with XANES LCF results on coordination geometry, Cu(I) speciation in the best EXAFS LCF was dominated by 2-fold coordinated Cu(I) exclusively 10908

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sorbent for copper. The mutual electron transfer between copper and humic acid and the complexation of both Cu(I) and Cu(II) by functional groups of humic acids described in this study are expected to critically affect copper solubility in redoxdynamic environments. For example, in flooded contaminated soils with limited sulfate or prior to sulfate reduction, humic acid may effectively transfer electrons to Cu(II) and contribute to the stabilization of Cu(I) by its complexation at high-affinity sites, as suggested in earlier soil incubation studies.16 In sulfiderich environments under strongly reducing conditions, Cu(I)HA complexation may be less relevant as inorganic sulfide is expected to compete with organic ligands. However, for mercury it was shown that Hg(II)-thiol complexes and metacinnabar (β-HgS(s)) can coexist in mixtures of organic soil and mackinawite,68 which may also apply for Cu(I)-HA complexes. On the other hand, humic acid has the potential for stabilizing small fractions of Cu(I) even upon soil reoxidation and to some extent also for reducing Cu(II) to Cu(I) under oxic conditions, an aspect that needs further investigation. Both mutual electron transfer between humic acid and copper and Cu(II) and Cu(I) binding by humic acid will influence the solubility of copper in equilibrium with humic acid. This aspect is further addressed in our companion study where we used potentiometric titrations and dialysis cell experiments to obtain binding isotherms for Cu2+ and Cu+ and gain quantitative information on the influence of copper binding by HA on copper redox speciation and solubility in the presence of reduced and reoxidized HA.37

Accordingly, 2-fold coordinated Cu(I) can be bound to HA in three possible ways: (i) via one O/N-group and coordinated with an additional chloride ion, (ii) via one S-group and coordinated with one H2O or OH− molecule, or (iii) as a bidentate complex bound to one O/N- and one S-group. In 3and 4-fold coordinated geometry Cu(I) is most likely ligated by more than one HA atom. The binding environment may be similar to Cu(I) binding sites known for cuproproteines, where Cu(I) is bound via histidine (imidazol-N), cysteine (thiol, RS), and methionine (thioether, RSR) residues.1 Such coordination environments are known to have a high formal Cu(II/I) redox potential keeping copper preferably in its Cu(I) oxidation state by destabilizing the Cu(II) oxidation state.62 This effect has been found to be pronounced for tripodal ligands with increasing numbers of sulfur atoms, especially thioether donors (see Rorabacher and Schroeder63 and references therein). In this context, it is noteworthy that 3- and 4-fold Cu(I) coordinated geometry was found to dominate Cu(I) speciation in HA equilibrated under oxic conditions, indicating a high stability of these Cu(I)-HA complexes against oxidation (SI Table S3). Concerning a contribution of oxygen donors, also binding of Cu(I) in thiolacetate-like bis-five-membered sulfhydryl/carboxyl chelates may represent a possible structure for Cu(I) complexation by NOM.11 Concerning the type of Cu(I)-ligating atoms, the presence of up to 50−100 mmol kg−1 Cu(I) at high loadings (corresponding to XANES LCF analysis) would require an amount of 40− 80 mmol kg−1 reduced S-groups based on the average Cu−S coordination number of 0.8 in the H1-untranox sample and assuming that coordination to Cl− was negligible. However, S K-edge XANES spectroscopy of the HA used in this study showed that HA contained only 45 mmol kg−1 reduced organic sulfur.22 Thus, even if all reduced sulfur is assumed to coordinate to Cu(I), the amount of reduced sulfur is not sufficient to completely account for Cu(I)−S/Cl coordination as derived from XAS analysis. This points to the presence of chloride in the first coordination sphere for binding of Cu(I) at high loading and suggests that a considerable fraction of Cu(I) was likely bound to the HA via O/N-groups. In contrast, at low loadings, the amount of reduced sulfur was sufficient to explain fitted amounts of S/Cl-coordinated Cu(I) (Cu(I)/Sred in LHAred = 0.13) considering the average Cu−S coordination of 1:1. Among the reduced S-groups, thiolates (RS−) may serve as high affinity binding sites for Cu+ as it was shown for other soft metal cations like Cd2+ and Hg2+.29,64,65 However, a previous study on competitive Cd2+ and Ca2+ binding to the HA used here revealed that at most 1 mmol kg−1 of reduced sulfur was present as thiols.22 Consequently, thioether (RSR) and disulfide (RSSR) groups must also have contributed to Cu(I) complexation if Cu(I) in samples with low loadings was mainly ligated to sulfur groups. For cuproproteins, it is well-known that methionine groups play an important role for Cu(I) binding.1 Likewise, thioethers in HA may be involved in Cu(I) complexation. Disulfide groups were found to contribute to Hg(II) complexation by soil organic matter as inferred from the presence of a second shell S atom at a higher distance in the coordination sphere of Hg(II).66 Since the soft cations Hg2+ and Cu+ have a similar electronegativity,67 it seems likely that disulfide complexes may also be relevant for Cu(I) binding in HA. Environmental Implications. Our results highlight the dual role of humic acid as an electron donor/acceptor and

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ASSOCIATED CONTENT

S Supporting Information *

Details for copper reference compounds, further results for XANES and EXAFS LCF and shell fitting, TEM images of Cu(0) particles and corresponding EDX spectra and calculations for Cu(0) saturation. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Phone: +41 58 76 55 470. E-mail: andreas.voegelin@eawag. ch. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Parts of this research were carried out at the Stanford Synchrotron Radiation Lightsource (SSRL), a Directorate of SLAC National Accelerator Laboratory and an Office of Science User Facility operated for the U.S. Department of Energy Office of Science by Stanford University. We are grateful to Joe Rogers for his support at beamline 11-2 (SSRL). We acknowledge the Angströ mquelle Karlsruhe (ANKA, Karlsruhe, Germany) for the allocation of beamtime and thank Stephan Mangold for assistance at the XAS beamline and Anke Hofacker (ETH Zurich) who kindly helped during the measurements at ANKA. We are grateful to Ralf Kaegi (EAWAG) for performing the TEM analyses. From ETH Zurich, we also thank Kurt Barmettler for support in the laboratory and Martin Hoffmann for valuable discussions on data processing. This research was financially supported by the Swiss National Science Foundation under grants No 200021117933 and No. 200020-135338. 10909

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dx.doi.org/10.1021/es4024089 | Environ. Sci. Technol. 2013, 47, 10903−10911