Redox transformation, solid phase speciation and solution dynamics of copper during soil reduction and reoxidation as affected by sulfate availability
Introduction
Copper (Cu) is an essential trace element for most living organisms. It is a constituent of a variety of proteins and enzymes that carry out fundamental biological functions (Rubino and Franz, 2012). However, elevated concentrations of Cu are toxic for microorganisms (Baath, 1989) and plants (Fernandes and Henriques, 1991). Ecosystem functioning can therefore be adversely affected as a result of soil contamination with Cu from anthropogenic activities such as metal mining or untreated waste water discharge.
While the behavior of Cu in well-drained oxic soils has been extensively studied, its biogeochemistry in periodically flooded soils, such as riparian wetlands and rice paddy soils, is less well-understood. In oxic soils, Cu dominantly occurs as bivalent (cupric) Cu(II). Cu(II) forms stable complexes with natural organic matter (Karlsson et al., 2006, Manceau and Matynia, 2010) and adsorbs on surfaces of Mn(III, IV) and Fe(III) (oxyhydr)oxides and clay minerals (Parkman et al., 1999, Strawn et al., 2004). However, Cu is a redox-active element and it may be reduced from cupric Cu(II) to cupreous Cu(I) or even Cu(0) by abiotic or biotic processes. Redox changes resulting from periodic overbank flooding and variations in groundwater level (Kirk, 2004) or flood irrigation (Koegel-Knabner et al., 2010) are therefore expected to strongly influence the chemical speciation and solubility of Cu in soils (Du Laing et al., 2009, Borch et al., 2010). Under sulfate-reducing conditions, the reduction of Cu(II) by dissolved sulfide (Luther et al., 2002, Ciglenecki et al., 2005) and subsequent precipitation as sparingly soluble metal sulfides (Pattrick et al., 1997, Morse and Luther, 1999) may substantially decrease Cu solubility. Recent studies on trace metal dynamics in a contaminated river floodplain soil showed that even at low levels of available sulfide and in the presence of other chalcophile metals (e.g., Hg, Cd, Pb and Fe), Cu can be effectively sequestered as Cu sulfide, due to the high thermodynamic stability of Cu sulfide minerals (Weber et al., 2009a, Hofacker et al., 2013).
In general, total S contents in freshwater floodplain soils are considerably lower than in marine or brackish wetlands and comprise only a small fraction (<5%) of inorganic S (Howarth et al., 1992). Riparian floodplain soils are aerated during most of the year, which prevents the accumulation of reduced inorganic S. Sulfate, on the other hand, is only weakly retained due to weak adsorption at pH > 6 (Tabatabai, 2005), and the mineralization of organic S is too slow to maintain high sulfate contents (Tabatabai and Alkhafaji, 1980, Zhou et al., 2005). As a result, the concentrations of chalcophile trace metals in contaminated freshwater floodplain soils may often exceed the amounts of reducible sulfate, resulting in the competition of different metal cations for reaction with limited amounts of sulfide formed by microbial sulfate reduction during periodic soil flooding (Weber et al., 2009a). Copper is expected to play a key role under sulfate-limited conditions, because it forms much more stable metal sulfides than Fe or trace metals like Pb, Cd, or Zn and typically occurs at much higher concentrations than Hg or Ag that would form even less soluble sulfides than Cu. However, in addition to the thermodynamic stability of metal sulfides, the solubility of other metal bearing phases and the kinetics of metal desorption, diffusion, and precipitation are also expected to strongly influence the formation of metal sulfide minerals (Weber et al., 2009a).
At low sulfide levels, Cu(II) may also be reduced by microorganisms (Wakatsuki, 1995), by reaction with dissolved Fe(II) (Matocha et al., 2005), or by redox-active functional groups of natural organic matter as recently shown (Pham et al., 2012). Biotic or abiotic reduction of Cu(II) to Cu(I) in sulfate-limited environments may have two major effects: the soft metal cation Cu+ may form strong complexes with thiol-groups of natural organic matter (R-SH), as reported for other soft metal cations like Ag+, Cd2+ and Hg2+ (Smith et al., 2002, Karlsson et al., 2005, Skyllberg et al., 2006). Association of Cu(I) with thiol-containing ligands has long been known to play a role in marine environments (Boulegue et al., 1982, Leal and van den Berg, 1998), but has hardly been considered for terrestrial soils. Another consequence of Cu reduction in sulfate-limited environments may be the formation of metallic Cu(0), since Cu(I) can rapidly disproportionate to Cu(II) and Cu(0) if the concentrations of Cu(I)-stabilizing ligands (e.g., sulfide, chloride and thiol) are too low. Metallic Cu has been observed in and near roots of wetland plants (Manceau et al., 2008) and in organic-rich bog soils (Lovering, 1927, Lett and Fletcher, 1980). Recently, Cu(0) formation has also been observed in microcosm flooding experiments with a contaminated floodplain soil (Weber et al., 2009b, Hofacker et al., 2013). In these studies Cu(0) was formed as intermediate phase, which was completely sulfidized during subsequent sulfate reduction. Under sulfate-limited conditions, however, Cu(0) may accumulate in reduced soils.
Variations in Cu speciation changes during soil reduction may also affect Cu dynamics during subsequent soil reoxidation, because different reduced Cu species may vary with respect to their reactivity under oxic conditions. While Cu sulfide clusters and Cu(I)-thiol complexes were shown to be stable over days to weeks in oxic waters (Leal and van den Berg, 1998, Rozan et al., 2000, Laglera and van den Berg, 2003, Sukola et al., 2005), Cu(0) oxidation occurs within tens of minutes (Kanninen et al., 2008).
Knowledge on the behavior of Cu during soil reduction and reoxidation at low sulfate availability is very limited (Weber et al., 2009a), and studies on Cu mobilization during transition from anoxic to oxic conditions were mainly conducted with sulfide-rich sediments and soils, focusing on the oxidative dissolution of Cu sulfides (e.g., Simpson et al., 1998, Carroll et al., 2002, Caetano et al., 2003). Thus, the aim of the present study was to elucidate the effect of sulfate availability on Cu dynamics in solution and solid phases during soil reduction and subsequent reoxidation. We conducted a time-resolved laboratory incubation experiment, in which we adjusted an uncontaminated paddy soil from Bangladesh to various sulfate-to-Cu ratios prior to an anoxic incubation period of 40 days, followed by reoxidation for 28 days. The dynamics of Cu in the solution phase and changes in Cu solid phase speciation were investigated by Cu K-edge X-ray absorption spectroscopy (XAS), sequential metal extractions, and chromium-reducible sulfur (CRS) distillation.
Section snippets
Soil sampling and characterization
A large batch of topsoil (∼150 kg, 0–10 cm depth) was collected from a rice paddy field near Sreenagar (Munshiganj district, Bangladesh) after the rice harvest in May 2007. The soil was classified as a non-calcareous Hydragric Anthrosol (Hypereutric, Siltic) with a silty clay loam texture (Dittmar et al., 2007).
The soil material was oven-dried at 60 °C, broken up into soil aggregates <2 cm using a jaw crusher (Retsch, Germany), mixed homogenously, and stored in plastic containers in the dark.
Solution dynamics during soil reduction and reoxidation
The dynamics of Eh, pH, DIC, DOC, major cations and anions, and Cu in solution during the reduction–reoxidation cycle followed similar trends in all incubation series (Figs. 1, EA3 and EA4). The observed changes in dissolved concentrations can be explained by the microbial respiration of electron acceptors following the classical sequence of redox reactions observed in submerged soils (Kirk, 2004, Koegel-Knabner et al., 2010). In the metal-spiked series (LS, MS and HS), soil reduction was
Discussion
In the following sections, we discuss the processes that control solid phase Cu speciation and dissolved Cu concentrations during different stages of the reduction–reoxidation cycle: (i) early stage of soil reduction prior to major sulfate reduction, (ii) period of major sulfate reduction, and (iii) soil reoxidation. Related to these three stages, we discuss the shift in solid phase Cu speciation between adsorbed Cu(II) and organically complexed Cu(I), metallic Cu, and Cu-sulfide, its impact on
Acknowledgments
The Angstroemquelle Karlsruhe (ANKA, Karlsruher Institute of Technology, Germany) is acknowledged for the allocation of beamtime. We are grateful to Jörg Rothe and Kathy Dardenne for their assistance at the INE beamline and Stephan Mangold for support at the XAS beamline. From ETH Zurich, we thank Anke Hofacker who kindly helped during all XAS measurements and Kurt Barmettler for technical and analytical support in the laboratory. Jessica Dittmar is acknowledged for providing and characterizing
References (85)
- et al.
Microbial sulfate reduction in littoral sediment of Lake Constance
FEMS Microbiol. Ecol.
(1991) - et al.
Sulfur speciation and associated trace-metals (Fe, Cu) in the pore waters of Great Marsh, Delaware
Geochim. Cosmochim. Acta
(1982) - et al.
A simple and inexpensive chromium-reducible sulfur method for acid-sulfate soils
Appl. Geochem.
(2008) - et al.
The use of chromium reduction in the analysis of reduced inorganic sulfur in sediments and shales
Chem. Geol.
(1986) - et al.
The impact of increased oxygen conditions on metal-contaminated sediments part I: Effects on redox status, sediment geochemistry and metal bioavailability
Water Res.
(2012) - et al.
Influence of hydrological regime on pore water metal concentrations in a contaminated sediment-derived soil
Environ. Pollut.
(2007) - et al.
Trace metal behaviour in estuarine and riverine floodplain soils and sediments: A review
Sci. Total Environ.
(2009) - et al.
Ferrihydrite flocs, native copper nanocrystals and spontaneous remediation in the Fosso dei Noni stream, Tuscany
Italy. Appl. Geochem.
(2007) - et al.
Is trace metal release in wetland soils controlled by organic matter mobility or Fe-oxyhydroxides reduction?
J. Colloid Interface Sci.
(2007) - et al.
Increasing pH drives organic matter solubilization from wetland soils under reducing conditions
Geoderma
(2009)
Effects of freeze-drying on partitioning patterns of major elements and trace metals in lake sediments
Anal. Chim. Acta
Temperature-dependent formation of metallic copper and metal sulfide nanoparticles during flooding of a contaminated soil
Geochim. Cosmochim. Acta
Controls on the stability of sulfide sols: colloidal covellite as an example
Geochim. Cosmochim. Acta
Influence of ligand structure on the stability and oxidation of copper nanoparticles
J. Colloid Interface Sci.
Copper complexation by thiol compounds in estuarine waters
Mar. Chem.
The nature of Cu bonding to natural organic matter
Geochim. Cosmochim. Acta
Chemical influences on trace metal-sulfide interactions in anoxic sediments
Geochim. Cosmochim. Acta
Reduction of Ag(I), Au(III), Cu(II), and Hg(II) by Fe(II)/Fe(III) hydroxysulfate green rust
Chemosphere
Kinetics of microbial sulfate reduction in estuarine sediments
Geochim. Cosmochim. Acta
The structure of amorphous copper sulfide precipitates: An X-ray absorption study
Geochim. Cosmochim. Acta
Coordination chemistry of copper proteins: How nature handles a toxic cargo for essential function
J. Inorg. Biochem.
Kinetics of inhibited crystal-growth: Precipitation of CuS from solutions containing chelated copper(II)
J. Colloid Interface Sci.
Solubility product constants of covellite and a poorly crystalline copper sulfide precipitate at 298K
Geochim. Cosmochim. Acta
Metal speciation in natural waters with emphasis on reduced sulfur groups as strong metal binding sites
Comp. Biochem. Physiol. C
Molecular characterization of copper in soils using X-ray absorption spectroscopy
Environ. Pollut.
Metal-sulfide species in oxic waters
Anal. Chim. Acta
Multi-metal contaminant dynamics in temporarily flooded soil under sulfate limitation
Geochim. Cosmochim. Acta
Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium
Geochim. Cosmochim. Acta
Mineralization of organic sulfur in paddy soils under flooded conditions and its availability to plants
Geoderma
Distribution and changes in heavy metal contents of paddy soils in different physiographic units of Bangladesh
Soil Sci. Plant Nutr.
A redox switch in CopC: an intriguing copper trafficking protein that binds copper(I) and copper(II) at different sites
PNAS
Effects of heavy-metals in soil on microbial processes and populations (a review)
Water Air Soil Pollut.
Biogeochemical redox processes and their impact on contaminant dynamics
Environ. Sci. Technol.
Acid-volatile sulfide oxidation in coastal flood plain drains: iron–sulfur cycling and effects on water quality
Environ. Sci. Technol.
Metal remobilisation during resuspension of anoxic contaminated sediment: short-term laboratory study
Water Air Soil Pollut.
Mobilization and scavenging of heavy metals following resuspension of anoxic sediments from the Elbe River
Speciation and fate of trace metals in estuarine sediments under reduced and oxidized conditions, Seaplane Lagoon, Alameda Naval Air Station (USA)
Geochem. Trans.
Adsorption and desorption phenomena of sulfate ions in soils
Soil Sci. Soc. Am. J.
Competitive-exclusion of sulfate reduction by Fe (III)-reducing bacteria: a mechanism for producing discrete zones of high-iron ground-water
Ground Water
Voltammetry of copper sulfide particles and nanoparticles: investigation of the cluster hypothesis
Environ. Sci. Technol.
Extractability and adsorption of sulphate in soils
J. Soil Sci.
Spatial distribution and temporal variability of arsenic in irrigated rice fields in Bangladesh. 2. Paddy soil∗∗∗∗
Environ. Sci. Technol.
Cited by (77)
Multi-metal contaminant mobilizations by natural colloids and nanoparticles in paddy soils during reduction and reoxidation
2024, Journal of Hazardous MaterialsInfluence of sulfate reducing bacteria cultured from the paddy soil on the solubility and redox behavior of Cd in a polymetallic system
2023, Science of the Total EnvironmentDistribution of Cu in agricultural soils with different land uses through stable isotope analysis
2023, Ecological Indicators