Environ. Sci. Technol. 2010, 44, 3772–3778
Evaluating Environmental Influences on AsIII Oxidation Kinetics by a Poorly Crystalline Mn-Oxide S A N J A I J . P A R I K H , * ,† BRANDON J. LAFFERTY,‡ TERRY G. MEADE,‡ AND DONALD L. SPARKS‡ Department of Land, Air and Water Resources, The University of California, One Shields Avenue, Davis, California 95616, and Department of Plant and Soil Sciences, Delaware Environmental Institute, The University of Delaware, 152 Townsend Hall, Newark, Delaware 19716
Received November 9, 2009. Revised manuscript received March 17, 2010. Accepted April 1, 2010.
The oxidation of arsenite (AsIII) via Mn-oxides is an important process for natural arsenic (As) cycling and for developing in situ strategies for remediation of As-contaminated waters. In this study, the influence of goethite (R-FeOOH), phosphate, and bacteria/biopolymer coatings on the initial AsIII oxidation kinetics by a hydrous Mn-oxide (δ-MnO2) is examined via both batch experiments and rapid scan ATR-spectroscopy. Under natural conditions the presence of various mineral surfaces, bacteria, organic matter, and ions in solution can block Mn-oxide reaction sites, alter reaction rates, and thus inhibit AsIII oxidation. Previous studies of As-Mn systems demonstrate rapid oxidation of AsIII, catalyzed by Mn-oxides, producing less toxic and mobile arsenate (AsV). Subsequent to oxidation, reaction products from reductive dissolution of δ-MnO2 by AsIII, bind to and passivate the mineral surface. This study demonstrates enhanced passivation through interaction with phosphate and bacteria. Increased As oxidation with high concentrations of goethite is observed, attributed to AsV sorption to R-FeOOH and diminished surface passivation of δ-MnO2. Specific competition between phosphate and AsV for δ-MnO2 was confirmed through diminished As sorption and decreased AsV production when oxidation occurred in the presence of phosphate. Kinetic experiments reveal that the extent of initial AsIII oxidation in the presence of low phosphate and R-FeOOH concentration is reduced; however, initial reaction rates are generally not affected. Reaction rates are reduced when bacterial adhesion and high phosphate concentrations strongly passivate δ-MnO2 and reduce AsIII interactions with the mineral surface. The data presented in this study highlight the importance of considering natural heterogeneity when investigating reaction mechanisms and initial reaction kinetics.
Introduction Inorganic arsenic (As) contamination in soils, sediments, and water from natural and anthropogenic sources pose environmental and human health risks. The predominate species of As in soil and aquatic environments are arsenite (AsIII) and * Corresponding author e-mail:
[email protected]. † The University of California. ‡ The University of Delaware. 3772
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arsenate (AsV) (1), with AsV being both less toxic and less mobile than AsIII (2). Oxidation of AsIII in soil and aquatic systems can be carried out via both abiotic (3) and biotic pathways (4). Manganese oxides are widespread in the natural environment and readily serve as electron acceptors in the abiotic oxidation of AsIII (5, 6). Biotic oxidation and reduction of As have been observed in a wide range of bacteria isolated from soil and natural waters (4). Kinetic investigations of AsIII oxidation by Mn-oxides have revealed rapid AsIII depletion rates (5-9), with equilibrium reached on a scale of minutes to hours. During this rapid reaction, sorption of AsIII to the Mn-oxide surface is believed to be a necessary step for oxidation (5, 6). Subsequent to AsIII oxidation, the retention of AsV on Mn-oxides surfaces has been documented experimentally (5, 8-10) and via density functional theory calculations (11). Binding of AsV on Mnoxide surfaces passivates the mineral surface, as AsIII binding sites are blocked and oxidation is inhibited. It is expected that similar passivation will occur in heterogeneous environments where bacteria, biopolymers, and ions in solution interact with Mn-oxide binding sites, thus influencing the rate and amount of AsIII oxidized. This has been observed for AsIII oxidation by manganite in the presence of phosphate where the extent and rate of oxidation was reduced (12). Bacterially catalyzed oxidation of AsIII is typically slower than oxidation via Mn-oxides. For example, AsIII half-lives (t1/2) during logarithmic growth have been measured at 12 (Variovorax paradoxus), 7.2 (Agrobacterium tumefaciens), and 4.8 h (Pseudomonas fluorescens) (13). Upon reaction with Mn-oxides, t1/2 for AsIII can be as rapid as less than 1 min (7, 8) to 0.15 h (6); however, longer values for t1/2 (37 h) have also been reported (14), with differences attributed to Mnoxide crystallinity, Mn:As ratio, and sorption processes. Attenuated total reflectance (ATR) Fourier transform infrared (FTIR) spectroscopy is an established technique for studying sorption (15, 16) and redox processes (17, 18), providing bonding mechanisms and, under certain reaction conditions, kinetic data (8, 17). Rapid-scan ATR-FTIR was previously used to collect rapid in situ kinetic data, providing molecular scale data, to examine the initial oxidation of arsenite (AsIII) via hydrous Mn-oxide (δ-MnO2) (8). Through observation and analysis of IR bands corresponding to arsenate (AsV), rapid AsIII oxidation was observed (initial pH 6-9) with 50% of the reaction occurring within the first minute. The primary objective of this paper is to examine the initial oxidation kinetics of AsIII via poorly crystalline Mnoxides in the presence of competing ions, mineral surfaces, and bacteria/biopolymer coatings. It has been previously shown that ion competition influences AsV sorption processes to a range of soil minerals (19-21), and only one study has examined the effect of ion competition on Mn-oxide catalyzed As oxidation kinetics (12). In that study, reactions with a crystalline MnIII-oxide (manganite) are slower than what has been observed for AsIII oxidation via poorly crystalline MnIVoxides (7, 8). Additionally, research on the initial oxidation kinetics of As via Mn-oxides in the presence of competing mineral surfaces and bacterial films has not been presented. This current study focuses on the initial moments of reaction and probes the effects of competition on the first minutes of As oxidation by δ-MnO2, whose poorly crystalline structure approaches that of Mn-oxides found in soil and sediment (22). While studies that investigate pure two-reactant systems are helpful for elucidating reaction mechanisms (10, 23, 24) and studies using soils and sediments (25-27) are useful to evaluate reaction rates and concentrations under natural 10.1021/es903408g
2010 American Chemical Society
Published on Web 04/19/2010
conditions, this study serves as a bridge by examining the initial oxidation kinetics of a relatively simple system and increasing its complexity under controlled conditions. The research presented here focuses on how additional environmentally relevant reactants influence the initial AsIII oxidation reaction via δ-MnO2 through use of rapid-scan ATR-FTIR spectroscopy.
Experimental Procedures An abbreviated description of experimental procedures is given here; for details regarding methods please see the Supporting Information. Materials. Synthesis of δ-MnO2 was performed using methods described in previous publications (8, 28) to give a mineral phase representative of natural Mn-oxides. δ-MnO2 was stored at 4 °C for less than 2 weeks prior to use in experiments. Goethite was synthesized using KOH and Fe(NO3)3 following the methods of Cornell and Schwertmann (29). Sodium arsenite (Fisher Scientific, >99%), sodium hydrogen arsenate heptahydrate (Alfa Aesar, 98-102%), and sodium phosphate (Fisher Scientific, 100.2%) were used as sources of AsIII, AsV, and phosphate, respectively. AsIII oxidizing bacteria were isolated and used in previous studies (13, 30, 31). As-oxidizing bacteria were grown on R2A agar plates, followed by inoculation into growth media (13) until the late exponential phase. Batch Sorption Isotherms and As Oxidation Kinetic Experiments. δ-MnO2 was reacted for 0 to 1440 min with AsIII (5 mmol kg-1 NaAsO2) and AsIII-phosphate (5 mmol kg-1 NaAsO2 and 5 mmol kg-1 NaH2PO4) at pH 6 and 9 in 5 mmol kg-1 NaCl. Samples (including blanks) were mixed via a reciprocal shaker (100 rpm, 25 °C). To promote flocculation of δ-MnO2, 1 mL of 1.0 mol kg-1 NaCl was added to each sample before being centrifuged at 5500 rpm for 10 min. After centrifugation, supernatants were filtered (0.2 µm) prior to analysis. For sorption isotherm experiments, δ-MnO2 (∼40 g kg-1) was reacted with 1, 2.5, 5, 10, and 15 mmol kg-1 NaH2PO4, Na2AsO2, and Na2HAsO4 at pH 6 and 9 in 5 mmol kg-1 NaCl. Samples were placed on a reciprocal shaker (100 rpm, 25 °C) for 24 h. Samples were centrifuged at 5500 rpm for 10 min and supernatants filtered (0.2 µm) prior to analysis. Bacterially-Catalyzed As Oxidation Kinetics. Bacteria were grown in 25 mL of growth media with 75 µmol L-1 AsIII until the late exponential phase. Cells were centrifuged at 5500 rpm (10 min, 4 °C) and resuspended in growth media with no AsIII. Washed bacteria were spiked with AsIII (pH 6) at 0, 1, 5, 15, and 25 mmol kg-1 AsIII and placed on an oribital shaker (100 rpm, 23 ( 2 °C). Aliquots (0.1 mL) were taken from each of the flasks at specific time intervals and analyzed via LC-ICP/MS analysis. Following reaction with AsIII concentrations up to 25 mmol kg-1 P. fluorescens and A. faecalis were plated on R2A agar after 24 and 48 h; growth of bacteria colonies demonstrates the As levels used as nonlethal. ATR-FTIR Spectroscopy and Analysis. FTIR spectra were collected with a Thermo Nicolet Nexus spectrometer (Thermo; MCT/A) using a diamond single bounce ATR accessory (Smart Orbit, Thermo) and on a multibounce ZnSe horizontal ATR (HATR, Pike Technologies) using standard spectral collection techniques. FTIR spectra for experiments with R-FeOOH were collected on a Thermo Nicolet 6700 spectrometer (Thermo; MCT/A) using a diamond single bounce accessory (GladiATR, Pike Technologies). As Oxidation: Rapid-Scan FTIR Experiments. In situ FTIR experiments were carried out via single-bounce ATR. All experiments were conducted using 25 mmol kg-1 AsIII in 5 mmol kg-1 NaCl at pH 6. The accuracy/validity of this method has been previously addressed (8). The rapid-scan FTIR experiments conducted (pH 6, 25 mmol kg-1 AsIII) include the following: (i) varying δ-MnO2 concentrations at 7.5, 11, 15, and 22 g kg-1; (ii) with 15 g kg-1 δ-MnO2 and
varying phosphate at 4, 8, 12, and 25 mmol kg-1; (iii) with P. fluorescens and A. faecalis at steady state concentration (105 cells mL-1); (iv) with 8 g kg-1 R-FeOOH and mixtures of δ-MnO2 and R-FeOOH (8 g kg-1 R-FeOOH and 15 g kg-1 δ-MnO2, 15 g kg-1 R-FeOOH and 15 g kg-1 δ-MnO2; and (v) with bacteria after 24 h reaction with 15 g kg-1 δ-MnO2, 15 g kg-1 R-FeOOH, and 15 g kg-1 R-FeOOH and 15 g kg-1 δ-MnO2. Experiments with goethite were conducted on a different FTIR and with different batches of minerals, resulting in slightly different peak areas and corresponding AsV concentrations. A conservative approach has been used to compare rapidscan kinetic data. The amount of AsV produced (AsVmax) is estimated by calculating the average AsV peak area from 4 to 15 min. Linear regression analysis of the first 30 s of reaction was carried out to determine the initial slope of the reaction (m30s) to compare initial reaction rates. The amount of time required for half of AsVmax has been defined as t1/2 and was determined by using an exponential fit for the data (0 to 15 min) and calculated t for half of AsVmax. This approach is only required for reactions where t1/2 exceeds 30 s. For t1/2 less than 30 s calculation for t1/2 could also be made using the linear regression equation for the first 30 s of reaction. Examining Binding Mechanisms during Passivation of δ-MnO2. To explore As binding mechanisms during passivation of δ-MnO2 subsequent to reaction with AsIII, a series of ATR-FTIR spectra were acquired (ZnSe HATR). Spectra collected include 12 mmol kg-1 AsV, 15 g kg-1 δ-MnO2, 12 mmol kg-1 AsV plus 12 mmol MnII (MnCl2), 12 mmol kg-1 AsV plus 15 g kg-1 δ-MnO2, and 12 mmol kg-1 AsIII reacted with 15 g kg-1 δ-MnO2 at 20 and 60 min.
Results and Discussion Batch AsIII-δ-MnO2 Experiments. Arsenic sorption by δ-MnO2 increased during AsIII oxidization compared to AsV sorption (Figure 1a), which is in agreement with the observations of previous studies using a synthetic birnessite (10). It is possible that reductive dissolution of δ-MnO2 by AsIII liberates MnII and may lead to increased binding sites for AsV and greater As retention. Although AsIII is more mobile than AsV (2), it is clear that chemical reactions influence transport in soil and subsurface environments. Since oxidation/ sorption can increase As retention, AsIII entering a system dominated by Mn-oxides may exhibit increased retention as compared to AsV entering the same system. The presence of phosphate during AsIII oxidation leads to decreased total As sorption to δ-MnO2 (Figure 1a). These data demonstrate competition between AsV and phosphate, resulting from similarity in chemical structure and reactivity (20, 32), and decreased retention of both anions (Figure 1). The reduced As sorption in the presence of phosphate is especially important for agricultural settings where animal waste containing As (and P) is land applied (33). A competitive ion effect has been demonstrated through addition of phosphate fertilizer to AsV contaminated soils, resulting in an increase of AsV leaching (34). Figure 2 shows the percent of initial As (AsIII and AsV) and phosphate in solution after reaction with δ-MnO2 as a function of time at pH 6 and 9. Increased AsIII oxidation rates via manganite have been previously observed with decreased pH (6.3 to 4.0); however, the current data, and our previous paper (8), reveal no significant effect of pH on the initial AsIII oxidation rate via δ-MnO2 (Figure 2). The figure reveals that the concentration of AsIII in solution rapidly drops to near zero, with full removal from solution occurring between 5 and 30 min. At 24 h, both phosphate and As concentrations are stable, and solution AsV concentrations are higher when phosphate is present. Increasing AsV concentrations from 5 to 960 min indicate that reactions are still occurring at the solid-liquid interface. High phosphate concentrations continue to exist in solution, indicating that As release is not due VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 1. Sorption isotherms from batch experiments at pH 6 (solid symbols) and 9 (open symbols) in 5 mmol kg-1 NaCl for a) As sorption to δ-MnO2 when added as AsV and AsIII (including oxidation) in the presence and absence of phosphate (P) and b) phosphate sorption to δ-MnO2 in the presence and absence of AsIII. to phosphate exchange reactions. Due to the similarity in chemical structure between phosphate and AsV, it follows that AsV sorption will not occur on these sites. It is our interpretation that AsIII is binding to δ-MnO2, oxidized, and AsV is subsequently released to solution with either the oxidation or desorption step occurring relatively slowly. It is well documented that during AsIII oxidation via Mn-oxides, MnIV can go through a MnIII intermediate before reducing to MnII (35). AsIII reaction with MnIII δ-MnO2 may lead to much slower AsIII oxidation rates and contribute to the release of AsV to solution between 30 and 960 min. Batch experiments alone cannot be used to determine reaction mechanisms; however, at high AsIII concentrations our previous FTIR study suggested AsIII binding to δ-MnO2 without the expected rapid oxidation (8). Although likely minimal in amount, density 3774
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functional theory calculations also suggest possible MnIII and AsIII accumulation on Mn-oxides (11). In Situ ATR-FTIR Investigations of AsV Binding Mechanisms. It is believed that AsIII initially binds to MnIV sites and is rapidly oxidized to AsV, while reductive dissolution of the mineral leads to MnII release (through an MnIII intermediate). MnIII on δ-MnO2 may permit limited AsIII binding without immediate oxidation. Assuming no sorption of reaction products, AsIII oxidation would continue until one of the reactants was no longer present. However, surface passivation of δ-MnO2 binding sites by AsV and/or MnII sorption inhibits complete oxidation (8, 11). It has previously been proposed that AsV binds directly to MnIV within Mnoxides (10) or through MnII bridging (5, 8, 9). FTIR data from this current study support both of these theories (Figure 3),
FIGURE 3. ATR-FTIR spectra (diamond IRE) of a) 12 mM AsV standard, b) 15 g L-1 δ-MnO2 standard, c) AsV reacted with MnII (MnCl2), d) AsV reacted with δ -MnO2, and 12 mM AsIII reacted with δ-MnO2 for e) 20 and f) 60 min.
FIGURE 2. Kinetic plots of batch experiments showing percent of initial As (5 mmol L-1 AsIII), as solution AsIII and AsV, and phosphate in solution during the course of reaction with δ-MnO2 at a) pH 9 and b) pH 6 in 5 mmol kg-1 NaCl. Insets are included to allow viewing of data within the first 60 min of reaction. Solid symbols correspond to experiments where δ-MnO2 was reacted with AsIII, and open symbols correspond to experiments where AsIII and phosphate were simultaneously reacted with δ-MnO2. as spectra of AsIII reacted with δ-MnO2 contain IR bands consistent with both AsV reacted with MnII and AsV reacted with δ-MnO2 (see the Supporting Information for specific peak assignments). It is not possible to examine AsIII binding with this approach as concentrations used are below the AsIII FTIR detection limit at pH 6 (8). Using the spectra of As standards, and working near the FTIR detection limits for AsV, interpretation of AsV binding to δ-MnO2 can be achieved. IR spectra of AsIII reacted with δ-MnO2 closely resemble the spectrum of AsV- δ-MnO2, and indicate that AsV is bound to MnIV. However, the peak at ∼790 cm-1 falls between standard peaks for AsV-MnII (767 cm-1) and AsV-MnIV (798 cm-1) and may represent a combination of both peaks. Although these data suggest that two different binding mechanisms are possible, our interpretation of the IR spectra is that most binding to δ-MnO2 is occurring between AsV and MnIV. As Oxidation Kinetics via Rapid-Scan ATR-FTIR: Abiotic Experiments. The presence of phosphate, R-FeOOH, and bacteria influence the amount of initial As oxidation and in some cases the initial reaction rates. For all reactions, the initial AsIII oxidation is carried out via reaction with δ-MnO. The primary factor influencing the amount of AsIII oxidized is limitation of MnIV binding sites. Increasing δ-MnO2 concentration leads to increased AsV production (Figure 4). The AsVmax, t1/2, and m30s for all reactions are given in Tables S1, S2, S3, and S4. The initial reaction rate is similar (m30s)
FIGURE 4. Rapid-scan ATR-FTIR plots of AsV IR peak area as a function of reaction time for 25 mmol kg-1 AsIII reacted with varying concentrations of δ-MnO2 suspensions at pH 6 in 5 mmol kg-1 NaCl. for the three highest δ-MnO2 concentrations but decreases when δ-MnO2 becomes limiting (7.5 g kg-1). Reactions rapidly approach completion with t1/2 ranging from 0.21 to 0.28 s. These initial reaction rates are not dependent on AsIII concentration, as nearly identical rates were observed for δ-MnO2 oxidation of 5 mmol kg-1 AsIII via batch and quickscanning X-ray absorption (Q-XAS) spectroscopy (7). In all cases the addition of phosphate reduces the total extent AsIII oxidation (Figure 5a, Table S2). The initial slope (m30s) and t1/2 are similar for all reactions, except for addition of 25 mmol kg-1 phosphate (m30s decreases and t1/2 increases). Although phosphate (and low R-FeOOH concentrations) reduces the amount of AsV produced, the initial oxidation rate is not affected. Since initial reaction rates are not strongly influenced by concentration of reactants, including other ions and surfaces, the reaction is not transport limited, and this implies primarily chemically controlled kinetics. The exception is observed at the high phosphate concentration VOL. 44, NO. 10, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 5. Rapid-scan ATR-FTIR plots of AsV IR peak area as a function of reaction time for 25 mmol kg-1 AsIII (pH 6, 5 mmol kg-1 NaCl) reacted with varying concentrations of a) phosphate (P) and b) r-FeOOH (experiments conducted on a different FTIR and with different batches of δ-MnO2 and r-FeOOH). where the reaction is slower. In this case we hypothesize that exchange/desorption of phosphate from δ-MnO2 permits prolonged reaction. This is in agreement with a previous study which reports a decrease in rate and extent of AsIII oxidation by manganite when phosphate concentrations were high, relative to AsIII (12). Reduced AsIII oxidation when reacted with phosphate is also observed in batch experiments (Figure 2); however, the rate of reaction does not seem to be affected. Under these conditions we propose that phosphate binding to δ-MnO2 blocks AsIII reaction sites, thus hindering oxidation. AsV forms inner-sphere complexes with Mn-oxides (10, 36) and sorption of AsV is favored over phosphate to numerous mineral surfaces, including Mn-oxides (19). Since phosphate and AsV have very similar structures and chemical reactivities (20), inner-sphere sorption of phosphate to δ-MnO2 is believed to be the reason for competition. Under certain conditions AsIII can be oxidized by Fe-oxides (37); however, no oxidation via R-FeOOH is observed within 15 min of reaction (Figure 5b). All experiments examining AsIII oxidation via δ-MnO2 in the presence of R-FeOOH were conducted at the University of California, Davis using a different spectrometer and batches of both δ-MnO2 and R-FeOOH (other experiments performed at the University of Delaware), and small differences in the amount of AsIII oxidized by δ-MnO2 are reflected in Figure 5 and Table S3. When δ-MnO2 is reacted with AsIII and 4 g kg-1 R-FeOOH the amount of AsV detected decreases. However, with increasing R-FeOOH concentration increased production of AsV is observed. At the highest R-FeOOH concentration the amount 3776
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FIGURE 6. Rapid-scan ATR-FTIR plots of AsV IR peak area as a function of reaction time for 25 mmol kg-1 AsIII (pH 6, 5 mmol kg-1 NaCl) reacted with a) P. fluorescens and b) A. faecalis suspensions (10 times steady state) with and without δ-MnO2 and r-FeOOH. of AsV produced exceeds what is observed for δ-MnO2 alone (Figure 5b). It is important to note that ATR-FTIR detects AsV both in solution and bound to mineral surfaces, thus an approximation of total AsV can be made. While binding of R-FeOOH to δ-MnO2 may be possible, we believe that the observed result arises from interactions between AsIII and AsV with the mineral surfaces and not from interaction between the two minerals. The sorption of AsIII and AsV to Fe-oxides has previously been demonstrated (38, 39), and it is proposed that reduced AsIII oxidation results from competition between δ-MnO2 and R-FeOOH for AsIII. Increasing R-FeOOH increases competition for AsV, and with high R-FeOOH concentrations some AsV released from δ-MnO2 during oxidation binds to R-FeOOH instead of δ-MnO2, thus passivation of δ-MnO2 is reduced. In this case, the Fe-oxide is serving to promote and hinder AsIII oxidation via δ-MnO2. This result was observed when AsIII was oxidized by birnessite, todorokite, and hausmannite in the presence of R-FeOOH (40). Analogous to the current study, the produced AsV binds to goethite and reduces passivation of the Mn-oxides. Another study observed an increase in As attenuation through simultaneous oxidation of AsIII and FeIII by Mn-oxides, whereby coprecipitation of FeIII-oxides with AsV serves to sequester arsenic and prevent Mn-oxide passivation (41). These results demonstrate a possible remediation strategy to achieve increased As oxidation and attenuation through addition of Mn- and Fe-oxides (or FeII) to As contaminated water.
Bacterially-Catalyzed As Oxidation. Analysis of solution AsIII and AsV concentrations during the 48 h reaction period reveal that the bacteria completely oxidize 1 mmol kg-1 AsIII in approximately 24 h (Figure S1). Additionally, the results show that these bacteria oxidize a maximum of ∼5 mmol kg-1 AsIII within 48 h, with the highest oxidation rate after 24 h of reaction. Rapid-scan ATR-FTIR experiments do not show detectable AsIII oxidation by either P. fluorescens or A. faecalis alone during the 15 min reaction time (Figure 6) and rapid AsIII oxidation is observed only when δ-MnO2 is present. When bacteria are bound to only R-FeOOH no AsV is detected; however, if δ-MnO2 is present with bacteria, a small IR peak corresponding to AsV is observed. The AsVmax for P. fluorescens with δ-MnO2 is 3.05 mmol kg-1 and 4.41 mmol kg-1 for A. faecalis with δ-MnO2; with R-FeOOH also present these values drop to 0.79 and 2.14, respectively (Table S4). The t1/2 values are less than δ-MnO2 reacted with AsIII alone, with values ranging from 0.64 to 0.88; however, m30s values are much less with a value of 0.01. Reaction of bacteria with minerals prior to reaction with AsIII results in binding between bacterial surface proteins and/or phosphate groups to both δ-MnO2 and R-FeOOH (see the Supporting Information). Bacterial adhesion to minerals blocks access to MnIV and reduces AsVmax. Bacteria bound to δ-MnO2 hinder AsV production much more than reaction with phosphate or R-FeOOH. Reaction rates are significantly reduced, based on t1/2 (0.98-2.81) and m30s (0.01) values (Table S4), and indicate that the reaction is transport limited. Exchange of bacteria or biopolymers for AsIII at MnIV sites is not likely; rather, it is believed that AsIII diffusion and transport through bacteria extracellular material (biofilm) retards AsIII oxidation. Water in the biopolymer matrix is organized in structured channels allowing transport into the biofilm (42). Oxidation of As by δ-MnO2 is reduced; however, AsIII may still be transported within channels thus delaying the oxidation reaction. In natural environments coatings of organic materials exist on mineral surfaces, and similar effects are expected. In a study where humic acid was preadsorbed onto Fe-Mn nodules, a decrease in both oxidation and sorption of As was observed due to reduced binding sites for AsIII (43). Examination of initial AsIII oxidation kinetics by Mn-oxides in the presence of environmental factors improves our understanding of their potential influence on reaction rates and amounts. This study demonstrates that competing factors generally reduce, or inhibit, the forward direction of the initial reaction, and their presence should be considered when trying to determine the fate of As in natural settings. Additional work is needed to look at long-term reaction rates for As-oxidizing bacteria bound to Mn-oxide surfaces, as increased time may permit abiotic and biotic reactions to work simultaneously and oxidize large amounts of As. Also, the observation of Fe-oxides to bind reaction products and enhance the extent of AsIII oxidation should be further explored. Fe-oxides are ubiquitous in soils and subsurface environments, and their presence at levels greater than Mnoxides may serve to reduce surface passivation and permit greater As oxidation and subsequent sequestration.
Acknowledgments We thank William P. Inskeep, Richard E. Macur, and Russ Hille for generously providing the bacterial strains used in this research. This project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2005-3510716105, and the National Science Foundation, grant number EAR-0544246.
Supporting Information Available Details regarding methodology and further discussion of results. This material is available free of charge via the Internet at http://pubs.acs.org.
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