Production of Abundant Hydroxyl Radicals from Oxygenation of

Dec 7, 2015 - State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, 388 Lumo Road, Wuhan 430074, P. R. China...
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Production of Abundant Hydroxyl Radicals from Oxygenation of Subsurface Sediments Man Tong, Songhu Yuan,* Sicong Ma, Menggui Jin, Deng Liu, Dong Cheng, Xixiang Liu, Yiqun Gan, and Yanxin Wang State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, 388 Lumo Road, Wuhan 430074, P. R. China S Supporting Information *

ABSTRACT: Hydroxyl radicals (•OH) play a crucial role in the fate of redox-active substances in the environment. Studies of the •OH production in nature has been constrained to surface environments exposed to light irradiation, but is overlooked in the subsurface under dark. Results of this study demonstrate that abundant •OH is produced when subsurface sediments are oxygenated under fluctuating redox conditions at neutral pH values. The cumulative concentrations of •OH produced within 24 h upon oxygenation of 33 sediments sampled from different redox conditions are 2−670 μmol •OH per kg dry sediment or 6.7−2521 μM •OH in sediment pore water. Fe(II)containing minerals, particularly phyllosilicates, are the predominant contributor to •OH production. This production could be sustainable when sediment Fe(II) is regenerated by the biological reduction of Fe(III) during redox cycles. Production of •OH is further evident in a field injection-extraction test through injecting oxygenated water into a 23-m depth aquifer. The •OH produced can oxidize pollutants such as arsenic and tetracycline and contribute to CO2 emissions at levels that are comparable with soil respiration. These findings indicate that oxygenation of subsurface sediments is an important source of •OH in nature that has not been previously identified, and •OH-mediated oxidation represents an overlooked process for substance transformations at the oxic/ anoxic interface.

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INTRODUCTION The hydroxyl radical (•OH, standard reduction potential: 2.8 V1) is the most powerful reactive oxygen species (ROS) in the environment. The •OH produced in the atmosphere, surface waters and oceans exerts a significant impact on the fate of redox-active substances, the emission of CO2 by reacting with dissolved organic matters (DOM) and the elimination of nonCO2 greenhouse gases.2−4 Photolysis has been recognized as the predominant pathway for •OH production in surface environments.4−7 For example, photolysis of nitrate and DOM produces the majority of •OH in surface waters.4,6,7 Dark subsurface environments are as important as surface environments for the cycling of substances (i.e., nutrients and contaminants), however, the production of •OH in the subsurface environment under circumneutral conditions has been overlooked. Unlike surface environments, subsurface environments are often O2-deficient, which is presumably the reason that •OH production in the subsurface has rarely been reported.8 Nevertheless, the redox conditions of subsurface environments are often disturbed by O2 in natural and artificial processes (e.g., surface water and groundwater interactions and riverbank filtration treatment),9−12 leading to strong interactions between O2 and reduced components in this environment. Many © XXXX American Chemical Society

reduced substances can activate molecular O2 to produce superoxide (O2•−) through a one-electron transfer process,13 and a wide range of heterotrophic bacteria can produce extracellular O2•− in the aquatic environment.14 Fe(II) is an important and abundant component in the subsurface environment under reducing conditions.15 Fe(II) oxidation can be coupled to the transformation of O2•− (and O2) to H2O2 and further to •OH through the Haber-Weiss mechanism.16,17 Thus, we hypothesize that oxygenation of the subsurface environment could produce •OH through the interaction of O2 with the reduced components, particularly Fe(II). In the subsurface, Fe(II) mainly exists in the form of complexes in pore water and minerals in sediments. Production of •OH resulting from the interaction of O2 with ligandcomplexed Fe(II) has been confirmed in the lab and utilized for the degradation of organic pollutants in wastewaters.18,19 With respect to Fe(II) minerals, oxidation of pyrite by O2 was found to produce •OH under acidic conditions (pH < 3),20−24 and the reaction of Fe(II) minerals (i.e., siderite and magnetite) Received: September 6, 2015 Revised: December 1, 2015 Accepted: December 7, 2015

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and another control experiment was performed using the addition of 1% HgCl2 for sterilization. The relative contributions of sediment solids and pore water to •OH production were measured by separating the suspensions through a 0.22-μm membrane. Production of •OH was also measured upon the oxygenation of standard Fe(II) minerals, including siderite, montmorillonite, biotite, chlorite, and the surface sediments following the removal of iron oxyhydroxides and organic carbon (Sections S2 and S3). Biological Reduction of Sediments. The sustainability of •OH production was tested by biologically reducing the surface sediments with Shewanella putrefaciens strain CN32, which is effective in reducing ferric iron.29 The strain was isolated from a subsurface core sample (from 250 m beneath the surface) obtained from the Morrison Formation during drilling of a shale-sandstone sequence in northwestern New Mexico, U.S.A. The CN32 was routinely cultured aerobically in a tryptic soy broth (TSB) from a frozen stock culture, which was kept in 35% glycerol at 80 °C. After harvesting until the mid- to latelog phase, CN32 cells were washed in filter-sterilized 0.9% NaCl and concentrated to ∼1 × 109 cells/mL. CN32 cells were then added to five grams of sterilized sediments in 30 mL of deionized water to produce an initial concentration of ∼1 × 108 cells/mL. Sodium lactate at 20 mM was supplied to sustain microbial iron reduction. The reduction lasted for 7 days in the anaerobic glove chamber. Then, the reduced sediments were separated and subjected to oxygenation for •OH production. Injection-Extraction Field Test. The injection-extraction experiments were carried out in the Jianghan Plain, central China. A 23-m depth well was drilled in the confined aquifer (113.680651°E, 30.176817°N) and was cased using a polypropylene random (PPR) tube (33 mm in diameter). The aquifer materials at a depth of 23 m were medium and coarse sands, mainly containing chlorite, Illite, feldspar, and quartz.30 The PPR tube was perforated and screened at depths of 20.6 to 23.0 m, allowing for the injection of oxygenated water into the aquifer at specified depth. Clay suspensions were carefully backfilled into the outside of the tube to prevent vertical flow. A total of 360 L of oxygenated deionized water was injected at a rate of 40 L/min with a pump. The dissolved oxygen (DO) concentration in the injected water was 11 mg/L. In the injected water, 10 mM sodium benzoic was dissolved to trap the •OH produced in the aquifer, and 100 mg/L Cl− was dissolved as a tracer to evaluate the recovery of injected water. Then, 30 L of deoxygenated deionized water were injected to produce a baseline. It is worth noting that the concentration of •OH produced in the oxygenated water before injection into the aquifer is below the detection limit (0.59 μM). After settling overnight to allow for aquifer oxygenation, the groundwater was extracted from the same well at a rate of 0.72−0.90 L/min. The extracted groundwater passed through a flow-through chamber to prevent the groundwater from being exposed to the air. Different probes were placed in the chamber to measure DO and Eh. The pH and electric conductivity (EC) were also measured. About 10 mL of groundwater was collected at different time intervals and stored in a brown bottle, then transported to the lab for p-HBA and Cl− analysis. The extraction continued for about 13 h until EC decreased to background values. A total of 663 L of groundwater was extracted, which is approximately double the injected volume. A groundwater extraction experiment was conducted to evaluate the relative contributions of groundwater and sediments to the production of •OH in the aquifer. Another

with O2 was observed to oxidize contaminants at neutral pH although the mechanism is not clear.25,26 Importantly, dark formation of •OH resulting from the oxygenation of anoxic waters was reported recently. Page et al.8 found that •OH was produced from the oxygenation of surface water and arctic soil pore water, and production increased in the presence of elevated concentrations of DOM and Fe(II). Minella et al.27 measured the production of •OH upon aeration of anoxic hypolimnion water. Because sediment solids represent a more significant fraction of Fe(II) pools than pore water in subsurface environments, it is reasonable to speculate that more •OH might be produced from the oxygenation of subsurface sediments. To test our hypothesis, we measured concentrations of •OH produced from the oxygenation of sediments at different redox conditions in the lab, and from oxygenation of an aquifer in a field injection-extraction test. We identified the possible contributors, Fe(II) and organic carbon,8 in the sediments from which •OH is produced. The sustainability of •OH production was tested through biological reduction of the oxygenated sediments. The environmental impact of the •OH produced was evaluated with respect to its capability to oxidize arsenic and antibiotics, and its contribution to CO2 emissions. Our main objective is to explicitly demonstrate the production of •OH from oxygenation of subsurface sediments under fluctuating redox conditions at neutral pH values and to ascertain its associated environmental impacts.

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EXPERIMENTAL SECTION Chemicals. Sodium benzoic (99.5%), p-hydroxybenzoic acid (p-HBA, 99%), 2,2′-bipyridine (BPY) were purchased from Sinopharm Chemical Reagent Co., Ltd., China. As2O3 (99.8%) and tetracycline were purchased from Shanghai General Reagent Factory, China. Na2HAsO4·7H2O (99.99%) and 5,5-dimethyl-1- pyrroline-N-oxide (DMPO) were obtained from Sigma-Aldrich. Montmorillonite (SWy-2, Fe content: 2.0%) was acquired from the Source Clays Repository of the Clay Minerals Society. Biotite (Fe content: 10.3%) was obtained from Lingshou County, Hebei, China. Chlorite (Fe content: 8.9%) was purchased from Haicheng County, Liaoning, China. Siderite particles were synthesized according to the procedure reported by Guo et al.25 Deionized (DI) water (18.2 MΩ·cm) obtained from a Heal Force NW ultrapure water system was used in all the experiments. All other chemicals were above analytical grade. Sediment Oxygenation. A total of 33 sediments were sampled from four typical redox-fluctuation subsurface environments, including a river-groundwater interaction zone, a lakeshore, a farmland, a wetland, and a deep aquifer (108− 168 m) in the Jianghan Plain, central China (see details in Supporting Information Section S1, Figure S1a). The sediment depths mainly ranged from 0.1 to 5 m, which reflect the profile of redox conditions (Figure S1b). Five grams of sediments were mixed with 30 mL of 10 mM sodium benzoic in a container in an anaerobic glove chamber (Mikrouna Co., Ltd.) filled with Ar (99.999%). The container was then moved out of the chamber for oxygenation in the dark. At different time intervals, about 2 mL of suspensions were taken out and filtered through a 0.22μm membrane. In the filtrate, the cumulative concentration of •OH was measured using the transformation of benzoic acid to p-HBA as a probe reaction.4,28 Control experiments in the absence of O2 were carried out in the anaerobic glove chamber, B

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•OH was produced under anoxic conditions, and sterilization led to negligible difference in •OH accumulation under oxic conditions (Table S2). These findings indicate that •OH is produced from an O2-induced chemical process, instead of a biological process. Oxygenation of all 33 sediments produced 2−670 μmol •OH per kg dry sediment within 24 h (Table S1), which translates to 6.7−2521 μM •OH in the sediment pore water. Oxygenation of sediment solids and pore water separately reveal that the solid phase contributed 76.5−98.8% of •OH production, while the pore water contributed slightly (Table S2). As a result of the much higher contribution of sediment solids compared to pore water, the cumulative concentrations of •OH are orders of magnitude higher than those reported for oxygenation of surface waters and arctic tundra soil pore water.8,27 The cumulative concentration of •OH increased quickly with the time of oxygenation and stabilized after 12 h (Figure 1).

well with a depth of 26 m, at a distance of 10 m from the injection well was used. The groundwater was extracted at a rate of 40 L/min. When the redox conditions stabilized (DO = 0 mg/L, Eh = −155 mV (vs Ag/AgCl), EC = 890 μS/cm, pH = 7.60), the extracted groundwater was collected in a 500-mL cylinder containing 10 mL of 500 mM sodium benzoic. When a total of 500 mL was collected, the cylinder was exposed to air for oxygenation. The cylinder was wrapped with foil to block light. About 10 mL of groundwater was stored in a brown bottle and transported to the lab for the analysis of p-HBA. Contaminant Oxidation. Sediment samples at a depth of 5 m and a distance of 7 m from the Tongshun River (No. 8 in Table S1) were employed. Five grams of sterilized sediments were mixed with 30 mL of deionized water (pH 7.2 ± 0.2) in the anaerobic glove chamber and were then moved out of the chamber for oxygenation. It should be noted that arsenic occurred naturally in the sediments, while tetracycline was produced artificially at an initial concentration of 5 mg/L. At different time intervals (0−24 h), about 2 mL of suspensions were taken out. As(III) and As(V) in the suspensions were extracted with 1.2 M HCl at 80 °C for 1 h.31 Tetracycline was extracted with 10 mL of methanol and EDTA mixture solution (1:1) (recovery >80%). Analysis. The •OH produced was first identified by an electron spin resonance (ESR) assay. During the oxygenation of the 5-m depth sediment (No. 8 in Table S1), a 950-μL sample was immediately mixed with 50 μL of 1.47 M DMPO to form an DMPO-radical adduct, which was then measured on a Bruker EMX ESR spectrometer with a microwave bridge (receiver gain, 5020; modulation amplitude, 2 G; microwave power, 6.35 mW; modulation frequency, 100 kHz; center field: 348.5 mT). The concentration of •OH was obtained by measuring p-HBA in an LC-15C HPLC (Shimadzu) equipped with a UV detector and an Inter Sustain C18 column (4.6 × 250 mm2). The concentration of p-HBA was used to estimate the cumulative •OH concentration with a conversion factor of 5.87.4,28 The detection limit was 0.1 μM for p-HBA, which corresponds to 0.59 μM for •OH. H2O2 was analyzed by a modified N,N-diethyl-p-phenylenediamine (DPD) method at 551 nm using a UV−vis spectrophotometer.32 During the measurement, BPY and Na2EDTA were added to complex Fe2+ and Fe3+, respectively. Soluble Fe2+ was measured by the 1, 10-o-phenanthroline analytical method at 510 nm. Total soluble iron concentrations were assayed through the reduction of Fe3+ to Fe2+ by hydroxylamine-HCl. Fe(II) and total iron in solid were measured after digestion by 1.3 M HF and 0.9 M H2SO4 at 100 °C for 30 min.33 As(III) and As(V) were measured on an HPLC coupled to an atomic fluorescence spectrometer (AFS 9600, Beijing Kechuang Haiguang Instrument Co., Ltd., Beijing, China).34 Tetracycline was measured by HPLC. Identification of Main Mineral Compositions. Sediments were dried and passed though a 200-mesh screen in the anaerobic glove chamber. The main mineral compositions were identified by a D8-FOCUS X-ray diffractometer with Cu K radiation (Bruker AXS.). The analysis was carried out at 40 kV and 40 mA at a scanning step size of 0.01° and step time of 0.05 s.

Figure 1. Production of •OH upon oxygenation of sediments at different depths. The samples locate 7-m distance from Tongshun river (Sediment No. 5−8 in Table S1). The groundwater level is about 2 m below the ground. The associated oxidation of Fe(II) is presented in Figure S3.

Assuming a production time of 12 h and a scavenging coefficient of 105 s−1,3 the average steady-state concentration of •OH is deduced to be 1.3 × 10−13 M (Section S4), which is 3−6 orders of magnitude higher than those produced from photolysis of surface waters.4,6 As a consequence, the sediment oxygenation process can produce abundant •OH, which is an important but overlooked source of •OH production in the nature. Contributors in the Sediments for •OH Production. The cumulative concentrations of •OH produced through sediment oxygenation are positively correlated with sediment Fe(II) content (R2 = 0.816) and organic carbon content (R2 = 0.570) (Figure 2). This indicates the possible contributions of Fe(II) and organic carbon to •OH production. To further investigate the relative contributions of each contributor to •OH production, we carried out a series of batch experiments. Fe(II) versus Organic Carbon. A portion of the surface sediment that produced minimal •OH upon oxygenation was reduced by dithionite to evaluate the contribution of Fe(II) in phyllosilicates. In this process, structural Fe(III) in phyllosilicates was transformed to structural Fe(II), while Fe(III) oxyhydroxides were reduced to soluble Fe(II), which was removed during washing (Section S2). Another portion was oxidized by H2O2 to remove organic carbon, then reduced by dithionite to produce structural Fe(II) in phyllosilicates. Oxygenation of the surface sediment after reduction produced

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RESULTS AND DISCUSSION Production of •OH from Sediment Oxygenation. Production of •OH from sediment oxygenation is evident by the characteristic 1:2:2:1 ESR spectrum (SI Figure S2). No C

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Figure 2. Correlation of •OH production with (a) sediment Fe(II) and (b) sediment organic carbon.

high concentrations of •OH (Figure 3a), which are even higher than those produced in the 5-m depth sediment (Figure 1). This suggests that structural Fe(II) in phyllosilicates contributed significantly to •OH production. Removal of organic carbon only caused a slight decrease in •OH production (Figure 3a), implying a minor contribution of sediment organic carbon to •OH production, this is consistent with the weaker correlation of •OH production with organic carbon compared with Fe(II) (Figure 2), and is also supported by the production of extremely low concentrations of •OH upon oxygenation of reduced humic acid.35 Adsorbed Fe(II) versus Structural Fe(II). The above findings demonstrate that structural Fe(II) in sediment solids contributed significantly to •OH production, while dissolved Fe(II) in the pore water contributed to a much lesser extent. Adsorbed Fe(II) is another form of Fe(II) with high reactivity.36,37 To further evaluate the contribution of adsorbed Fe(II), BPY was added because of its strong chelating ability with Fe(II).32 The addition of 1−30 mM BPY suppressed 28− 42% of •OH production (Figure S5). As the adsorption of BPY on the sediment surface may partly screen the reaction of structural Fe(II) with O2, the contribution of adsorbed Fe(II) could be lower than the percentage suppressed. Speciation of Structural Fe(II). Selected sediments were characterized by XRD, and the analysis demonstrated that chlorite, mica, and montmorillonite are the main Fe-containing minerals (Figure S6, Table S4). Because of the limits of XRD analysis, it is possible that amorphous minerals, such as amorphous ferric oxides and other iron minerals, occur in concentrations too low to be identified by XRD. As bicarbonate is abundant in sediment pore water (Table S1), it is assumed that siderite is present. To test this, we measured •OH produced from the oxidation of four standard minerals: chlorite, biotite, montmorillonite, siderite (Section S3). As

Figure 3. (a) Production of •OH in solution upon oxygenation of surface sediment after chemical and microbial reduction. The associated oxidation of Fe(II) is shown in Figure S4. (b) Normalized yield of •OH upon oxygenation of standard Fe(II)-containing minerals and field sediments. The associated oxidation of Fe(II) is shown in Figure S7. The dosages are 2 g/L for siderite (Fe(II): 48.3%), 50 g/L for montmorillonite (Fe(II): 1.5%) and 2 g/L for biotite (Fe(II): 6.3%) and chlorite (Fe(II): 5.5%).

expected, high concentrations of •OH were produced, and production was accompanied by a linear decrease in Fe(II) content (Figure S7). After normalization by the oxidized Fe(II), •OH yield (μmol •OH per g Fe(II)) in the presence of the four minerals occurred in the following order: biotite (1317) > chlorite (1074) ≫ montmorillonite (231) > siderite (55) (Figure 3b). All the Fe(II)-containing minerals in the sediments contributed to •OH production upon oxygenation. The normalized yields of •OH were calculated to be 123 μmol •OH per g Fe(II) based on the correlation of •OH production with Fe(II) content in the 33 sediments (Figure 2a), 153 μmol •OH per g Fe(II) from the oxidation of 5 m depth sediment (Figure S3b), and 1546 μmol •OH per g Fe(II) based on the oxidation of surface sediment after reduction by dithionite (Figure S4c). As phyllosilicates are abundant and widespread in soils and sediments,38,39 and the normalized yields of •OH are higher for Fe(II) in phyllosilicates compared to other forms, we postulate that Fe(II) in phyllosilicates is the primary contributor to •OH production. Therefore, the relative contributions of organic carbon and different forms of Fe(II) in sediments to •OH production are assumed to occur in the following order: Fe(II) in phyllosilicates ≫ Fe(II) in other forms of minerals > adsorbed Fe(II) ≫ organic carbon. The other redox-active components in the sediments such as Mn may contribute, but D

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•OH was produced from oxygenation of the 23-m depth aquifer, and reached a maximum concentration of 26 μM (Figure 4). The variation in •OH concentrations agrees well

their contribution is of minor importance because of the much lower concentrations relative to Fe (Table S1). Since the speciation of Fe(II) determines the yield of •OH from sediment oxygenation, pH values might significantly affect •OH production as a result of their impact on the speciation and oxidation kinetics of Fe(II).40 Pathway for •OH Production from O2. The instantaneous concentrations of H2O2 over the course of oxygenation increased to 9.62 μM at 2 h, and then gradually decreased to 0 at 12 h (Figure S8a). The sharp increase within 2 h is consistent with the rapid production of •OH (Figure 1) and oxidation of Fe(II) (Figure S3). The decrease observed after 2 h is attributed to increased decomposition due to the formation of Fe(III) minerals20 compared with the decreased production due to the oxidation of Fe(II). Thus, H2O2 is an intermediate ROS for the production of •OH from O2. To explore the number of electrons transferred from O2 to H2O2, the generation of O2•−, a one-electron transfer intermediate ROS, was tested by the addition of an O2•− scavenger, nitroblue tetrazolium (NBT).41 The presence of NBT greatly reduced H2O2 concentrations to less than 0.80 μM (Figure S8a), suggesting the generation of O2•−. However, •OH production was only suppressed by 57% through the addition of NBT (Figure S8b). This implies that one-electron reduction is not the sole mechanism for the reduction of O2 to H2O2. Twoelectron transfer has been demonstrated virtually as the mechanism for the reduction of O2 to H2O2 by pyrite and ligand-complexed Fe(II).42,43 Therefore, we propose that both one- and two-electron transfer are feasible mechanisms for the reduction of O2 to H2O2; following this reduction, sediment Fe(II) causes the decomposition of H2O2 to •OH through the Fenton mechanism.17−19 Sustainability of •OH Production. To evaluate the sustainability of •OH production from sediment oxygenation in subsurface redox fluctuation cycles, the surface sediment that produced minimal •OH was reduced biologically. Upon oxygenation of the reduced surface sediment, the cumulative concentration of •OH reached a maximum of 35 μM •OH (Figure 3a), approaching the concentration produced in the 5m depth sediment (Figure 1). Biological reduction increased the Fe(II) concentration from 0.53 to 0.88 g/kg (Table S3), which was almost the same concentration as that in the sediment following chemical reduction (0.92 g/kg) and after sequential oxidation−reduction (0.89 g/kg). However, the total Fe concentration in the sediments following biological reduction (4.19 g/kg) was much higher than the concentrations that occurred following chemical reduction (1.71 g/kg) and sequential oxidation−reduction (1.80 g/kg), indicating that a lower fraction of reactive Fe(II) was present in the sediments following biological reduction. The normalized yield of •OH from the oxygenation of the sediment following biological reduction is 1273 μM •OH per g Fe(II). This yield is close to that produced from the sediment after chemical reduction since both reduction reactions regenerated the reactive Fe(II) in phyllosilicates. In natural processes, Fe(II) and Fe(III) in phyllosilicates can be cycled by microorganisms under changing redox conditions.44 We therefore suggest that •OH production from sediment oxygenation is sustainable under periodically fluctuating redox conditions. •OH Production from Oxygenation of an Aquifer in the Field. To explicitly demonstrate the production of •OH in subsurface environments, we carried out an injection-extraction experiment in the Jianghan Plain. Results demonstrate that

Figure 4. Production of •OH upon oxygenation of an aquifer at 23-m depth.

with the variations in Cl− concentrations, further implying that •OH was produced as a result of the injection of oxygenated water. The sharp decrease in DO concentration (Figure S9) demonstrates that the injected O2 was depleted from the aquifer. The concentrations of •OH are lower than those produced in the lab because of the limited amount of O2 in the aquifer. From these findings, we infer that more •OH can be produced by recharging more oxygenated water until the sediment Fe(II) is depleted. To highlight the importance of aquifer sediments in •OH production, we extracted the aquifer groundwater and measured •OH production upon groundwater oxygenation. The concentrations of •OH produced were less than 2 μM, which are much lower than those produced in the aquifer. This difference is consistent with the aforementioned finding that sediment solids contribute predominantly to •OH production. It should be noted that the concentrations of •OH produced from groundwater oxygenation are still on the same order of magnitude as those reported following oxygenation of surface waters and arctic tundra soil pore water.8,27 This implies that exposure of groundwater to air is also a source of •OH production, for example, during the discharge or abstraction of groundwater. Environmental Impact. The environmental impact of •OH produced from oxygenating sediments was evaluated with respect to the oxidation of redox-active contaminants. Both arsenic and antibiotics are of worldwide concern and exist in the groundwater of the Jianghan Plain.30,45−47 The oxygenation of a 5-m depth sediment that intrinsically contains arsenic resulted in the oxidation of As(III) to the less toxic As(V) (Figure 5a).48,49 The predominant role of •OH in As(III) oxidation was confirmed by the dramatic decrease in the efficiency caused by the addition of scavengers (Figure 5a). A similar oxidation reaction was observed in the presence of tetracycline (Figure 5b). We hypothesize that other redoxactive substances with similar rate constants can also be oxidized. Thus, the sediment oxygenation process can induce the oxidation of redox-active substances by •OH under fluctuating redox conditions. We further evaluated the significance of •OH in CO2 emissions because organic carbon is a large sink of •OH in natural environments.4,6,8 The •OH produced from sediment oxygenation contributes to the emission of 4.62 g CO2 m−2 d−1 E

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aeration or riverbank filtration, groundwater recharging, and farming and construction activities. When the nutrients (i.e., C, N, S, etc.) and substances/contaminants coexist or are transported across the oxic/anoxic interface in these processes, transformations caused by •OH-induced oxidation must be taken into account aside from the well recognized biogeochemical processes. Evidence of •OH production resulting from the oxidation of Fe(II) by O2 provides fundamentals for the associated oxidation of contaminants.25,26 Our findings may also open up new areas for environmental remediation activities. For example, the oxidation of contaminants by •OH can be achieved through periodically manipulating the redox conditions of iron-containing minerals or sediments. An alternative process is the periodical injection of O2 into the aquifer or in situ production of O2 from groundwater electrolysis34 for remediation. The operation mode of existing water treatment units such as constructed wetland and riverbank filtration can be modified to produce •OH for degrading refractory organic contaminants.

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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.est.5b04323. Sections S1−S5, sediment sampling, analysis, oxygenation, steady state, and CO2 emission; Figures S1−S9, sampling locations, ESR evidence, variations of iron content, effect of BPY on •OH, XRD patterns, production of •OH, H2O2, and variations of DO and Eh; Tables S1−S4, summarized results and characteristics, ferrous and total iron content, and sediment mineral composition; and additional references (PDF)

Figure 5. Oxidation of (a) As(III) and (b) tetracycline by •OH produced from sediment oxygenation. Note that the concentrations of As and tetracycline refer to the sum of the dissolved and adsorbed fractions. Ethanol at 100 mM was added as the scavenger of •OH. Similar inhibition is observed with addition of 10 mM benzoic, an •OH-specific scavenger.

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(Section S5), which is orders of magnitude higher than that reported for soil water oxygenation8 and on the same order of magnitude as that produced from soil respiration.50 This indicates that sediment oxygenation contributes to CO2 emission,, and its importance could be of particular significance in the regions such as the Jianghan Plain where redox conditions fluctuate frequently in the subsurface environment.30 Implications. We identify here a source of •OH production that has not previously reported from the oxygenation of subsurface environments, particularly those with Fe(II)containing sediments. The steady-state concentrations of •OH produced are much higher than those reported for oxygenation and photolysis of surface waters. Iron is a ubiquitous element in soils (i.e., loess and red soil) and sediments resulting from its high abundance (∼5%) in the Earth’s crust. At an oxic/anoxic interface, the interaction of O2 with sediment Fe(II) produces •OH and Fe(III). •OH induces the oxidation of the redox-active substances that are transported through the interface. When O2 is depleted under fluctuating redox conditions, Fe(III) is biologically reduced back to Fe(II),51 leading to the sustainable production of •OH. This new source of •OH production could be significant because the interaction of O2 with sediments is common in many natural and artificial processes. Typical natural processes include the interaction of surface water (i.e., river, lake, and ocean) with groundwater,9−11 alternating wetting and drying caused by groundwater table fluctuations (e.g., in unsaturated zones and wetlands),52 and ocean circulation. Artificial processes include groundwater table fluctuations caused by water conservancy projects, drinking water treatment by in situ

AUTHOR INFORMATION

Corresponding Author

*Phone: +86-27-67848629; fax: +86-27-67883456; e-mail: [email protected] (S.Y.). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We appreciate the valuable suggestions and edits kindly given by Prof. Daniel Giammar at Washington University in St. Louis and Prof. Hongfu Yin, Zhongqiang Chen, Shucheng Xie, Chao Li, and Hailiang Dong at China University of Geosciences (Wuhan). This work was supported by the Natural Science Foundation of China (NSFC, No. 41522208, 41521001) and the Ministry of Education of China (No. 20130145110008).

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REFERENCES

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DOI: 10.1021/acs.est.5b04323 Environ. Sci. Technol. XXXX, XXX, XXX−XXX

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DOI: 10.1021/acs.est.5b04323 Environ. Sci. Technol. XXXX, XXX, XXX−XXX