Environ. Sci. Technol. 2004, 38, 6618-6624
Interaction of Inorganic Arsenic with Biogenic Manganese Oxide Produced by a Mn-Oxidizing Fungus, Strain KR21-2 Y U K I N O R I T A N I , * ,† N A O Y U K I M I Y A T A , † MAIKO OHASHI,† TOSHIHIKO OHNUKI,‡ HARUHIKO SEYAMA,§ KEISUKE IWAHORI,† AND MITSUYUKI SOMA† Institute for Environmental Sciences, University of Shizuoka, 52-1 Yada, Shizuoka 422-8526, Japan, Japan Atomic Energy Research Institute, Tokai, Ibaraki 319-1195, Japan, and National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba 305-8506, Japan
In batch culture experiments we examined oxidation of As(III) and adsorption of As(III/V) by biogenic manganese oxide formed by a manganese oxide-depositing fungus, strain KR21-2. We expected to gain insight into the applicability of Mn-depositing microorganisms for biological treatment of As-contaminated waters. In cultures containing Mn2+ and As(V), the solid Mn phase was rich in bound Mn2+ (molar ratio, ∼30%) and showed a transiently high accumulation of As(V) during the early stage of manganese oxide formation. As manganese oxide formation progressed, a large proportion of adsorbed As(V) was subsequently released. The high proportion of bound Mn2+ may suppress a charge repulsion between As(V) and the manganese oxide surface, which has structural negative charges, promoting complex formation. In cultures containing Mn2+ and As(III), As(III) started to be oxidized to As(V) after manganese oxide formation was mostly completed. In suspensions of the biogenic manganese oxides with dissolved Mn2+, As(III) oxidation rates decreased with increasing dissolved Mn2+. These results indicate that biogenic manganese oxide with a high proportion of bound Mn2+ oxidizes As(III) less effectively than with a low proportion of bound Mn2+. Coexisting Zn2+, Ni2+, and Co2+ also showed similar effects to different extents. The present study demonstrates characteristic features of oxidation and adsorption of As by biogenic manganese oxides and suggests possibilities of developing a microbial treatment system for water contaminated with As that is suited to the actual situation of contamination.
Introduction Contamination of drinking water by inorganic arsenic is one of the important environmental problems worldwide (1, 2). Inorganic arsenate and arsenite generally dominate arsenic species in surface and groundwaters. At neutral pH, As(V) * Corresponding author phone/fax: +81-54-264-5728; e-mail:
[email protected]. † University of Shizuoka. ‡ Japan Atomic Energy Research Institute. § National Institute for Environmental Studies. 6618
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exists as anionic species, H2AsO4- and HAsO42- (pKa1 ) 2.24, pKa2 ) 6.94, and pKa3 ) 12.19 (3)), while As(III) is electronically neutral (pKa1 ) 9.29 (3)). Since As(III) is less effectively removed than As(V) by most treatment technologies, preoxidation of As(III) is generally required (4). Various types of chemically synthesized manganese oxides effectively oxidize As(III) to As(V). These manganese oxide minerals include birnessite (5-9), cryptomelane (10), pyrolusite (10), and manganite (11). It appears that manganese oxide surfaces contribute to As(III) oxidation in natural systems (3). Manning et al. (12), using EXAFS, demonstrated the formation of As(V) adsorption complexes with an As(V)-Mn interatomic distance of 3.22 Å on abiotically synthesized birnessite. A XANES study also showed that As(III) is oxidized and subsequently adsorbed as As(V) on the birnessite (12). In natural environments, the formation of manganese(III/IV) oxides from soluble Mn2+ is believed to be a biologically controlled process in most freshwater bodies since abiotic oxidation of Mn2+ proceeds only at a limited rate under circumneutral conditions (13-16). Thus, interactions of biogenic manganese oxides with various elements, including arsenic, are of great interest for treatment of water contaminated with toxic elements (16-20). A variety of microorganisms, including bacteria and fungi (14, 16, 21-23), can oxidize Mn(II) to insoluble manganese oxide. In bacteria, multi-copper oxidases have been proposed to catalyze manganese oxide formation from soluble Mn(II). Besides Mn-oxidizing bacteria, an Acremonium-like hyphomycete fungus, strain KR21-2 (24), isolated from streambed pebbles encrusted with manganese oxide in the Kikukawa River system, Shizuoka Prefecture, Japan (25), was also shown to excrete an Mn-oxidizing enzyme, probably a class of multicopper oxidase. Strain KR21-2 is phylogenetically related to members of the order Hypocreales (24). Cephalosporium () Acremonium) is one of the Mn-depositing fungi isolated at the highest frequencies from soils and natural ferric and manganic sediments (26, 27). Other members of Hypocreales have also been isolated at high frequencies (26). From these observations, Acremonium and related Hypocreales are considered to be representative of Mn-depositing fungi ubiquitous in the environment. Strain KR21-2 may therefore be regarded as a model organism for studies of the contribution of Mn-depositing fungi to biogeochemical cycling of various elements (20, 24). This fungus deposits manganese oxide particles with an X-ray diffraction (XRD) pattern typical of vernadite (δ-MnO2), with a specific surface area of 12.3 m2 per mmol of Mn (113 m2 g-1 of manganese oxide) (20). Recent studies (18, 19) have demonstrated that biogenic manganese oxides have chemical and physical characteristics different from chemically synthesized ones. For example, biogenic manganese oxides produced by a sheathed bacterium, Leptothrix discophora SS-1, have a large capacity to adsorb Pb2+ ions as compared with the synthetic manganese oxides. The very high sorption efficiency results from both a higher surface area and a higher binding energy for Pb2+ per unit area of biogenic manganese oxides (19). Our previous study (20) showed sorption efficiencies of biogenic manganese oxides produced by stain KR21-2 for Co2+, Ni2+, and Zn2+ ions about 10-fold higher than chemically synthesized γ-MnO2 on the basis of unit weight and unit surface area (20). Kim et al. (28) recently demonstrated by microscopic and spectroscopic studies that Mn2+ oxidation products formed by L. discophora SP-6 are nanosized, todorokite-like, porous MnO2. Villalobos et al. (29) showed that biogenic manganese oxide produced by Pseudomonas putida MnB1 is composed purely of Mn(IV) with the significant amounts 10.1021/es049226i CCC: $27.50
2004 American Chemical Society Published on Web 10/27/2004
of charge-balancing alkali metal ions, suggesting that its negatively charges primarily arise from tetravalently charged vacancies in the crystal lattice. The aim of this study is to describe the interaction of inorganic arsenic, arsenate (As(V)), and arsenite (As(III)) with biogenic manganese oxides that were produced by a Mnoxidizing fungus, strain KR21-2. We show that the adsorption of As(V) and oxidation of As(III) during the formation of biogenic manganese oxide are strongly affected by the proportions of Mn2+ bound on manganese oxide particles. Effects of coexisting Zn2+, Ni2+, and Co2+ on As(III) oxidation and As adsorption by the biogenic manganese oxides are also examined.
Materials and Methods As(V/III) Adsorption and As(III) Oxidation Concurrent with Biogenic Manganese Oxide Formation. An Acremoniumlike hyphomycete fungus, strain KR21-2 (20, 24), capable of oxidizing Mn(II) to manganese oxides enzymatically, was used in this study. A total of 50 mL of HEPES-buffered AY (HAY) liquid medium (20, 24) with MnSO4 and either Na2HAsO4 or NaAsO2 was inoculated with a conidial suspension of strain KR21-2 (1 × 105 conidia mL-1) (24) and incubated at 25 °C on a reciprocal shaker (BR-40lF, TAITEC; 105 strokes min-1) for 72 h. The HAY contained 3 mM sodium acetate, 150 mg L-1 yeast extract, 200 µM MgSO4‚7H2O, 30 µM K2HPO4, 50 µM CaCl2‚2H2O, 80 µM H3BO3, 7.4 µM FeCl3‚6H2O, 3.0 µM ZnSO4‚7H2O, 2.4 µM Na2MoO4‚2H2O, and 0.04 µM CuSO4‚5H2O in 20 mM HEPES buffer (pH 7.0) (24). The liquid culture was sampled at appropriate time intervals and separated by centrifugation (11000g for 10 min). The supernatants were used for analyses of dissolved Mn2+ and arsenic species. The residual solids thus separated (manganese oxide particles and fungal mass) were treated with 20 mM CuSO4 solution (50 mL) for 12 h to extract bound, but not oxidized, Mn2+ (30, 31). After separation by centrifugation, the residue was rinsed with water and then treated with 10 mM hydroxylamine chloride solution for more than 4 h to dissolve oxidized Mn. The concentrations of Mn dissolved in the supernatants and extractants were measured with an atomic absorption spectrometer (Perkin-Elmer AAS 3300). These procedures are defined as a concurrent culture experiment in this study. An anion-exchange method (11, 32) was used for separation of As(III) and As(V) in the supernatants of the As(III)added systems. A 1 g portion of Dowex 1 × 8 100 anionexchange resin (Cl- form) was slurry-packed in a polypropylene column. The resin was treated by passage of 0.4 M HNO3 (4 mL × 2), Milli-Q water (4 mL × 2), and 1 M NaOH (4 mL × 2), followed by rinsing with Milli-Q water (4 mL × 2). The resin was further treated with 1 M acetic acid (4 mL × 2) and rinsed with Milli-Q water (4 mL × 2) to obtain the acetate form. The sample solutions (250 µL) were eluted through the resin with 10 mM acetate buffer (2 mL × 4, pH 4.5), where neutral As(III) was eluted while As(V) was retained. The combined eluate was acidified with 1 M HNO3, and Ge (final concentration 50 µg L-1) was added as an internal standard for ICP-MS measurements for As(III) determination. The total As concentration in the supernatant was measured by ICP-MS without the anion exchange separation procedure. As(V) was determined by subtracting As(III) from total As. Recovery of standard As(III) was more than 98%. Effects of Coexisting Cations on As(III) Oxidation and As Adsorption by Biogenic Manganese Oxide. To test the effects of the dissolved Mn2+ on As(III) oxidation kinetics and As adsorption by the biogenic manganese oxide, we conducted the following experiments. The biogenic manganese oxides were prepared in cultures of KR21-2 with initial Mn(II) at 1.0 mM for 72 h without any initially added As(III). At 72 h, 10 mM NaN3 was added to the culture to inactivate
FIGURE 1. As(V) adsorption and biogenic manganese oxide formation in liquid cultures of strain KR21-2 with 14.5 µM As(V) and 1.1 mM Mn2+. (A) As(V) dissolved and adsorbed and proportions of bound Mn2+ in solid Mn. (B) Mn dissolved, bound, and oxidized (n ) 2, error bars ( SD). the Mn-oxidizing enzyme of strain KR21-2. Then the cultures were supplemented with several concentrations of Mn2+ (0.2-1.0 mM) and allowed to incubate for 1 h to equilibrate with aqueous Mn2+ before As(III) was added at 15 µM. The supernatant was separated by centrifugation at appropriate time intervals and used for As(III) and As(V) determination described previously. The control experiments were also carried out without a subsequent addition of Mn2+. To examine the effects of Zn2+, Ni2+, or Co2+ on As(III) oxidation and on As adsorption by the biogenic manganese oxides, each of the metal ions was added at 0.5 mM. These procedures are defined as a post-culture experiment in this study. XANES (X-ray Absorption Near-Edge Structure) Spectra. A biogenic manganese oxide sample was prepared as in the post-culture experiment with additional Mn2+ at 1.0 mM and As(III) at 15 µM. At 24 h after the addition of As(III), the mixture was separated by centrifugation, and the supernatant was discarded. The residue was immediately frozen at -30 °C and kept until XANES analysis. The same procedure was also carried out using 15 µM As(V) instead of As(III), for comparison. The As K-edge XANES spectra were collected at the BL-27B station of the Photon Factory of the High Energy Accelerator Research Organization (Tsukuba, Japan) in fluorescence mode using a seven-element Ge semiconductor detector. Standards for As(III) and As(V) were 0.10 M aqueous solutions of NaAsO2 and Na3AsO4, respectively. The absorption energy was set to be 11874.0 eV (33, 34) at the inflection point in the XANES spectra of As in standard Na3AsO4.
Results and Discussion As(V) Adsorption during Manganese Oxide Formation by Strain KR21-2. Under the culture conditions used in this study, strain KR21-2 precipitates manganese oxide in HAY (pH. 7.0) containing Mn2+ after 42 h of incubation, when the fungal growth approaches the stationary phase (24). The presence of As(V) at an initial concentration of up to 15 µM did not influence the ability of strain KR21-2 to oxidize Mn2+ to manganese oxides. The concentration of As(V) in the aqueous phase decreased abruptly at the onset of manganese oxide formation (Figure 1). When KR21-2 was cultured in HAY containing no initial Mn2+, no decrease in dissolved As(V) was observed (data not shown). This indicates that VOL. 38, NO. 24, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 2. Apparent adsorption isotherms of As on biogenic manganese oxide formed by strain KR21-2 at different culture times (46 and 72 h). Concentrations of As(III) and As(V) added initially ranged up to 15 µM. The initial Mn2+ concentration was constant at 1.1 mM. As(V) adsorption on the hyphae is negligible. Thus, the adsorption of As(V) on the biogenic manganese oxide is responsible for the decrease in the concentration of dissolved As(V). Interestingly, the As(V) adsorption during the incubation did not parallel the formation of manganese oxide. Higher As(V) adsorption was observed temporarily between 42 and 54 h, while manganese oxide formation was ongoing. After 54 h of incubation, when dissolved Mn2+ had almost disappeared, a large part of the adsorbed As(V) was subsequently released into the solution. Owing to the transient adsorption, the amount of adsorbed As(V) per solid Mn at 46 h was about 10-fold higher than that at 72 h, irrespective of the initial concentrations of As(V) (Figure 2). Since dissolved Mn2+ and As(V) remained for at least 72 h in HAY medium that was not inoculated with strain KR21-2, the possibilities of the formation of a scarcely soluble salt of Mn2+ with arsenate (35) and of the precipitation of arsenate with any other constituents in the culture were excluded in our culture conditions. Two-step extraction showed that the bound (Cu2+exchangeable) Mn2+ accounted for about 30% of the solid Mn (molar basis) during the early stage of manganese oxide formation (46-50 h; Figure 1A). After this stage, as manganese oxide formation progressed, its proportion decreased to 15.9 ( 1.9%, 12.5 ( 0.7%, and 11.5 ( 2.4% (n ) 2, (SD) at 54, 60, and 72 h, respectively. This was consistent with a previous result (24). No significant amounts of the bound Mn2+ and the oxidized Mn were observed at 42 h, although the fungal growth approached then the stationary phase (Figure 1B). Thus, the bound Mn2+ was attributed mainly to the Mn2+ adsorbed on the manganese oxide rather than on the fungal cell surfaces. The higher proportion of the bound Mn2+ in the manganese oxide phase during manganese oxide formation may be due to both a high concentration of dissolved Mn2+ in the solution and the small amount of manganese oxide formed. The higher proportion of bound Mn2+ at the early stage of manganese oxide formation was also reported during bacterial manganese oxide formation by L. discophora SS-1 in batch culture experiments (31); it accounted for about 10% of total solid Mn. Bacterial manganese oxides produced by Bacillus sp. SG-1 contained 20-30% bound Mn2+ (30). In the concurrent culture experiments, addition of NaN3, an inhibitor of enzymatic Mn2+ oxidation (24), at 46 h, when the transient accumulation of As(V) occurred, suppressed the subsequent release of the adsorbed As(V) (Figure 3). When 10 mM NaN3 was added, further oxidation of Mn2+ was completely inhibited and a large part of the adsorbed As(V) was retained: the amount of adsorbed As(V) at 72 h was 11.4 µmol As per mmol of solid Mn, which was about 4 times the 6620
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FIGURE 3. Effect of NaN3 addition on As(V) adsorption (A) and manganese oxide formation (B) by strain KR21-2. NaN3 was added at concentrations of 0 (control; open circles), 1.0 (shadowed triangles), and 10 mM (filled circles) at 46 h of incubation, indicated by the arrows. Inset shows amounts of adsorbed As(V) per solid Mn and bound Mn2+ in solid Mn at 72 h of incubation. Initial concentrations of As(V) and Mn2+ were 14.5 µM and 1.1 mM, respectively. amount of the control mixture (2.93 µmol As per mmol of solid Mn). Although a lower concentration of NaN3 (1 mM) was insufficient to prevent further oxidation of Mn2+, higher As(V) adsorption (6.56 µmol As per mmol of solid Mn at 72 h) was also observed. The amount of adsorbed As(V) in the solid Mn phase was clearly correlated with the proportions of the bound Mn2+ in the solid Mn phase (Figure 3 inset). Whereas Mn2+ corresponding to 11.5% of total solid Mn was extractable with Cu2+ (Figure 1A) at 72 h, only 0.4% of solid Mn was extracted with 0.1 M ammonium acetate solution, which may extract weakly bound cations on solids. This suggests an innersphere complex formation of Mn2+ at the biogenic manganese oxide surfaces. Manganese oxide minerals characteristically have negative structural charges because of the presence of some Mn(III) or vacant sites within the octahedral layers or mineral lattices (16, 36, 37). Villalobos et al. (29) indicated that biogenic manganese oxide produced by P. putida MnB1 contains structurally less Mn(III) with the significant amounts of charge-balancing alkali metal ions: thus, negative structural charges of biogenic manganese oxides primarily arise from tetravalently charged vacancies in the crystal lattice (29). Since the biogenic manganese oxide produced by strain KR21-2 (20) exhibits a XRD pattern similar to that from P. putida MnB1 (e.g. 2.4 and 1.4 Å d spacings with 001 and 002 XRD reflection weak or absent (29)), it is likely to have such a structural property. An EXAFS study (12) provided evidence for the formation of As(V) adsorption complexes with an As(V)-Mn interatomic distance of 3.22 Å on the manganese oxide surface; the most likely As(V)MnO2 complex is a bidentate, binuclear, corner-sharing (bridged) complex occurring at manganese oxide crystallite edges and interlayer domains (12). Therefore, we suggest that the innersphere complex formation of Mn2+ neutralizes the structural negative charges on the biogenic manganese oxide surfaces, subsequently reduces the charge repulsion between manganese oxide surfaces and As(V) (dominate species of which were H2AsO4- and HAsO42- at pH 7.0; pKa1
TABLE 1. Oxidation and Adsorption of As in the Liquid Cultures of Strain KR21-2 with Various Concentrations of Initial Mn2+ and As(III) (mean ( SD; n ) 2)a initial Mn2+ (mM)
initial As(III) (µM)
oxidized As(III) in solution (%)
As adsorbed (µM)
0 0.007 0.025 0.11 1.0 1.0 1.0 1.0 1.0
15 15 15 15 15 43 83 142 440c
ndb 46.3 ( 2.3 79.0 ( 2.6 98.3 ( 0.1 100 ( 0.0 99.3 ( 0.4 99.5 ( 0.02 99.6 ( 0.01 ndb
ndb ndb 0.026 ( 0.005 0.74 ( 0.08 3.0 ( 0.32 6.34 ( 0.20 9.00 ( 1.41 17.1 ( 1.83 ndb
a Incubated for 72 h. formed.
b
Not detectable. c Manganese oxide was not
) 2.24, pKa2 ) 6.94, and pKa3 ) 12.19 (3)), and promotes the formation of such an As(V)-MnO2 complex. The structural negative charge densities of the manganese oxide surface increase as the proportion of the bound Mn2+ in solid Mn decreases by its oxidation. This may cause the subsequent release of adsorbed As(V) after the early stage of manganese oxide formation in the concurrent culture experiments (Figures 1 and 3). Besides Mn2+, other transition metal ions such as Zn2+, Co2+, and Ni2+ are expected to exhibit a similar effect on promoting As(V) adsorption since manganese oxides have high affinity for these metal ions (see next section). Takamatsu et al. (38) found that the addition of the divalent cations Mn2+, Sr2+, Ba2+, and Ni2+ enhanced As(V) adsorption on synthetic δ-MnO2. As(III) Oxidation and Adsorption Concurrent with Manganese Oxide Formation. In the liquid cultures of strain KR21-2 with Mn2+ and As(III), As(III) was oxidized to As(V) during the production of biogenic manganese oxide. When As(III) was added at 440 µM, strain KR21-2 did not precipitate manganese oxide or oxidize As(III) (Table 1), although fungal growth was observed (data not shown). The dependence of oxidation of As(III) on the initial Mn2+ concentration (Table 1) revealed that As(III) is indirectly oxidized to As(V) by KR21-2 through the formation of manganese oxides: no oxidation of As(III) was observed in the culture without initial Mn2+ (Table 1). On the other hand, the addition of the initial Mn2+ at concentrations (7-25 µM) comparable to that of the initial As(III) (15 µM) promoted the oxidation of As(III) to As(V) (Table 1), although the As adsorption was very small. The amount of adsorbed As increased with increasing initial Mn2+ and As(III) concentrations. In the cultures where As(III) was initially added, an apparent isotherm nearly identical to that for As(V) (Figure 2) was observed at 72 h of incubation. This result, along with the predominance of As(V) in the aqueous phase at 72 h (Figure 1A), suggests that As(V) dominated the adsorbed As at the end of the concurrent culture experiment with initial As(III). The culture experiments with the initial concentrations of Mn2+ and As(III) at 1.1 mM and 14.7 µM, respectively, showed that As adsorption started at the onset of the manganese oxide formation (Figure 4). Transient adsorption of As was not observed, in contrast to the case where added As species was As(V) (Figure 1A). Interestingly, the oxidative product As(V) did not appear in the solution until the dissolved Mn2+ had mostly disappeared (Figures 4 and 5). Effects of Dissolved Mn2+ on As(III) Oxidation and Adsorption. To test the effect of the dissolved Mn2+ on As(III) oxidation and adsorption by the biogenic manganese oxides, we conducted the post-culture experiments using the biogenic manganese oxide suspension with further
FIGURE 4. As(III) oxidation and adsorption and biogenic manganese oxide formation in liquid culture of strain KR21-2 with 14.7 µM As(III) and 1.1 mM Mn2+. (A) As(III) and As(V) dissolved, and As adsorbed. (B) Mn dissolved, bound, and oxidized (n ) 2, error bars ( SD).
FIGURE 5. Relationship between As(V) proportion in solution and biogenic manganese oxide formation (oxidized and bound) during 42-58 h incubation of strain KR21-2 in HAY medium with initial concentrations of 14.7 µM As(III) and 1.1 mM Mn2+. Quadruplicated experiments were conducted. addition of Mn2+ at 0.2-1.0 mM (see Materials and Methods), followed by the addition of As(III) at 15 µM. At the end of these experiments (24 h after addition of As(III)), K-edge XANES spectra confirmed that adsorbed As was found mostly as As(V) (Figure 6), even in the presence of the highest added Mn2+ (1.0 mM), where the decrease in dissolved As(III) was the slowest and As(III) still accounted for half of the total As in the solution (Table 2). This indicates a very small contribution of adsorbed As(III) to total adsorbed As and is consistent with the results of Manning et al. (12), who, using XANES spectroscopy, found that the adsorbed As species on As(III)-treated birnessite is As(V). Thus, the decrease in aqueous-phase As(III) resulted from its conversion into As(V) rather than direct adsorption of As(III). The As(III) oxidation rate apparently followed first-order kinetics with R2 >0.93 in all cases (Table 2). Several researchers have reported apparent first-order kinetics for depletion VOL. 38, NO. 24, 2004 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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structural Mn(III/IV) to Mn(II) or Mn(III) by aqueous As(III) provide new adsorption sites for the oxidative product, As(V) (10, 12). Our results suggest that the binding of Mn2+ produced upon reduction of manganese oxide with As(III) also partly contributes to a higher adsorption of As in synthetic manganese oxide suspensions reacted with As(III).
FIGURE 6. As K-edge XANES spectra of As(V)- and As(III)-treated biogenic manganese oxides produced by strain KR21-2. Standards for As(III) and As(V) were 0.10 M aqueous solutions of NaAsO2 and Na3AsO4. The absorption energy was set to be 11874.0 eV at the inflection point in the XANES spectra of As in standard Na3AsO4. (combined of oxidation and adsorption) of As(III) in suspensions of synthetic manganese oxides (9, 10, 12). In this study, the first-order rate constants for As(III) oxidation decreased from 2.69 ( 0.08 to 0.057 ( 0.004 h-1 (n ) 2; (SD) with increasing additional Mn2+ concentration from 0 to 1.0 mM. The two-step extraction procedure showed that As(III) oxidation rates were negatively correlated with the proportions of the bound Mn2+ in the solid manganese oxide phases (Table 2): manganese oxides with smaller bound Mn2+ oxidized As(III) faster. This result was consistent with the slower oxidation of As(III), and smaller subsequent release of As(V), until completion of the manganese oxide formation in the concurrent culture experiments (Figures 4 and 5). The bound Mn2+ with the innersphere complexation on the manganese oxide surfaces may prevent As(III) from approaching the structural Mn(III/IV) that oxidizes As(III). Scott and Morgan (8) found that the addition of Mn2+ to an arsenic(III)-manganese oxide suspension caused a greater decrease in the rate of release of the oxidative product As(V). Thus, they proposed that the added Mn2+ binds to manganese oxides and consequently blocks the adsorption and oxidation of As(III) (8). While the addition of Mn2+ greatly lowered the oxidation rates of As(III), it caused a higher adsorption of total As with increasing added Mn2+ concentrations (Table 2). This is consistent with the observation that the bound Mn2+ enhanced As(V) adsorption since the As(V) dominated the adsorbed As on the manganese oxides even when incubated in As(III). Several researchers have found higher adsorptions of total As when As(III), rather than As(V), was initially added to suspensions of synthetic manganese oxides (9, 10, 12). It has been suggested that surface alterations by reduction of
In aquatic environments where the Mn2+ supply exceeds the oxidation activity of the Mn-oxidizing microorganisms that mediate manganese oxide formation, the resultant biogenic manganese oxides may contain a higher proportion of bound Mn2+ and consequently exhibit a higher capacity for As(V) adsorption and a slower oxidation rate of As(III). Elevated levels of dissolved Mn2+ in waters are frequently caused by anthropogenic activities: for example, up to 1.5 mM dissolved Mn was contained in the groundwater receiving the impact from mining activity (Pinel Creek, Arizona) (39). Kay et al. (39), using a five-step sequential extraction procedure, reported that adsorbed Mn, along with Mn associated with carbonate, primarily accounted for more than 14% of total Mn in the sediments of this stream. On the other hand, biogenic manganese oxides with smaller proportions of bound Mn2+ would have a higher ability to oxidize As(III) when the microbial activity for manganese oxide formation exceeds the Mn2+ supply. Some studies with different Mn-oxidizing microorganisms showed that biogenic manganese oxides contain different proportions of bound Mn2+ among the mediating microorganisms. L. discophora SS-1 generally produces manganese oxides with much less bound Mn2+ (10% of Mn in solid phase (20). These results would be partly due to the differences in the affinities of Mn-oxidizing enzymes for Mn2+ among microorganisms. The affinity of the Mn-oxidizing enzyme from L. discophora SS-1 (Km ) 6 µM) (40) seems to be much higher than that of strain KR21-2 (Km ) 650 µM) (24). The characteristics of Mn-oxidizing microorganisms that contribute to manganese oxide formation would also affect As cycling in nature. Effects of Dissolved Zn2+, Ni2+, and Co2+ on As(III) Oxidation and Adsorption. Besides Mn2+, the addition of Zn2+, Ni2+, or Co2+ to the suspension of the biogenic manganese oxide lowered the As(III) oxidation and enhanced As adsorption, as compared with the control experiment (Table 2). The inhibitory effect of these cations at 0.5 mM on As(III) oxidation rate decreased in the order of Mn2+ > Co2+ ≈ Ni2+ > Zn2+. This seems to be responsible for the variation of As(III) removal efficiencies among these metal ions at the termination of the experiments (24 h after As(III) addition). Notably, total As adsorption was enhanced by Zn2+ addition more than by Ni2+, Co2+, or Mn2+. The additions of Ni2+ and Co2+ showed efficiencies for As adsorption almost similar to that of Mn2+. These variations in both As(III) oxidation and
TABLE 2. Effects of Dissolved Mn2+, Zn2+, Ni2+, and Co2+ on As(III) Oxidation and Adsorption by Biogenic Manganese Oxides (mean ( SD; n ) 2)a,b
metal ions
first-order rate constant for As(III) oxidation (h-1) (data points, n; R 2)c
oxidized As(III) (%)d
total As adsorbed (%)d
bound Mn2+ in solid Mn (mol %)d
no metal ions 0.2 mM Mn2+ 0.5 mM Mn2+ 1.0 mM Mn2+ 0.5 mM Zn2+ 0.5 mM Ni2+ 0.5 mM Co2+
2.69 ( 0.08 (10; 0.9908) 0.161 ( 0.014 (7; 0.9453) 0.071 ( 0.004 (6; 0.9359) 0.057 ( 0.004 (8; 0.9740) 0.215 ( 0.008 (6; 0.9908) 0.128 ( 0.010 (6; 0.9643) 0.091 ( 0.008 (6; 0.9493)
99.8 ( 0.0 98.9 ( 0.0 81.2 ( 2.6 73.7 ( 0.5 97.1 ( 0.3 95.7 ( 2.4 91.0 ( 7.9
4.3 ( 3.9 16.1 ( 0.2 25.9 ( 1.5 47.4 ( 2.3 99.5 ( 0.1 38.3 ( 0.7 39.5 ( 1.5
11.5 ( 2.4 16.4 ( 2.2 18.1 ( 4.6 19.5 ( 4.2 nme nme nme
a As(III) was added at 15 µM. measured.
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Biogenic manganese oxide was 1 mM. c 0-24 h after addition of As(III).
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d
24 h after addition of As(III). e Not
As adsorption may arise from different affinities and sorption characteristics among these metal ions. Our previous investigation demonstrated different affinities and extractabilities among these metal ions when they were sorbed on biogenic manganese oxide produced by strain KR21-2 (20): the order of sorption efficiency on the biogenic manganese oxide produced by strain KR21-2 was Co2+ > Zn2+ > Ni2+ ions, while that on the chemically synthesized γ-MnO2 was Zn2+ > Co2+ > Ni2+. Interestingly, extraction procedure using 10 mM CuSO4 solution showed higher irreversibility of Co2+ and Ni2+ sorption on the biogenic manganese oxide while Zn2+ sorption was mostly reversible (Cu2+-exchangeable) (20). Sorption of Co2+, Ni2+, and Zn2+on γ-MnO2 was, however, found to be mostly reversible (20). Such complex characters of metal sorption on the biogenic manganese oxides requires more detailed studies to clarify the roles of the coexisting metal ions on As(III) oxidation rate and As adsorption by the biogenic manganese oxides.
Acknowledgments This work was partly supported by a Grant-in-Aid for Young Scientists (B) (16710052) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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Received for review May 25, 2004. Revised manuscript received September 7, 2004. Accepted September 14, 2004. ES049226I
