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1 Applied Geochemistry 23 (2008) Contents lists available at ScienceDirect Applied Geochemistry journal homepage: Effect of indigenous bacteria on geochemical behavior of arsenic in aquifer sediments from the Hetao Basin, Inner Mongolia: Evidence from sediment incubations Huaming Guo *, Xiaohui Tang, Suzhen Yang, Zhaoli Shen School of Water Resources and Environment, China University of Geosciences, Beijing , PR China article info abstract Article history: Received 5 February 2008 Accepted 7 July 2008 Available online 15 July 2008 Editorial handling by D. Polya Incubation studies were carried out using 5 freshly collected sediments from shallow aquifers of the Hetao Basin, Inner Mongolia. The aquifer sediments covering a range of redox conditions, as indicated by their deep grey to yellow color were mixed with degassed artificial As solution or degassed deionized water at a ratio of solid to water of about 1:10 (wt./ wt.). Suspensions which were either amended with glucose or autoclaved, were incubated in parallel with unamended suspensions. Five microcosm cultures of unamended sediments gradually release the equivalent of lg/g As to the dissolved phase. The addition of glucose as a potential electron donor results in a marked stimulation in the mobilization of As ( lg/g) in the amended incubations for all sediments. The quantity of As released accounts for 60 70% of As bound to Fe/Mn oxides in the original sediments. The microbially mediated mobilization of As with the organic nutrient as an electron donor is strongly associated with the As bound to Fe/Mn oxides, as well as the exchangeable As. During the incubations amended with glucose, 2 4% of the sediment Fe is released. The results suggest that the introduction of labile dissolved organic C into the yellowish sediment aquifers with As-free groundwater would reduce a significant proportion of the Fe(III) oxyhydroxides mediated by anaerobic bacteria respiration and increase groundwater As concentrations. Ó 2008 Published by Elsevier Ltd. 1. Introduction High As groundwaters have been observed in aquifers from many parts of the world, including Bangladesh, India, Argentina, China, Mexico, Hungary, Vietnam, USA, Chile and Japan (Smedley and Kinniburgh, 2002). China has many provinces with high As groundwaters, including Inner Mongolia, Xinjiang, Shanxi, Jilin, Jiangsu, Anhui, Shandong, Henan, Hunan, Yunnan, as well as Taiwan (Guo et al., 2007). It has been estimated that about 2 3 million people are exposed to the potential risk of As toxicity (Jin et al., 2003; Shen et al., 2005). This is of great concern to both regulatory agencies and scientific institutes. * Corresponding author. Tel.: ; fax: addresses: hmguo@cugb.edu.cn, hm_guo@hotmail.com (H. Guo). The sources of As and mechanisms of its mobilization are the most important issues, since they help in understanding the geochemical behavior of As in aquifers and in developing proper technologies for remediating high As groundwater. The proposed mechanisms of As enrichment in groundwater include oxidation of As-bearing sulfides (Robertson, 1989; Peter et al., 1999), reductive dissolution of Fe(III) oxyhydroxides (Bhattacharya et al., 1997; Nickson et al., 1998), as well as dissimilatory reduction of As (Zobrist et al., 2000), microorganisms could mediate all of those processes. Many bacteria and archaea are capable of oxidizing As minerals (Ehrlich, 1964), which would catalyze the dissolution oxidation of minerals. Microbial reduction of Fe(III) in the Fe(hydr)oxide minerals may release Fe(II) and adsorbed As(V) or As(III) into solution (Cummings et al., 1999; Herbel and Fendorf, 2005). The most readily bioreducible Fe(III) (hydr)oxides are the high surface area, /$ - see front matter Ó 2008 Published by Elsevier Ltd. doi: /j.apgeochem
2 3268 H. Guo et al. / Applied Geochemistry 23 (2008) least thermodynamically stable phases such as ferrihydrite and lepidocrocite (Schwertmann and Taylor, 1989; Roden and Zachara, 1996). The Fe(III) reduction induces a transformation of ferrihydrite (or lepidocrocite) to more stable Fe(III) minerals, such as goethite (a-feooh), and mixed Fe(II) Fe(III) minerals, such as magnetite (Fe 3 O 4 )(Zachara et al., 2002), which universally decreases their capacity to retain As (Dixit and Hering, 2003). Microbial reduction of As(V) to As(III) may also improve As mobilization. Arsenic-respiring bacteria are not only capable of reducing soluble As(V) (Langner and Inskeep, 2000), but also adsorbed As(V) (Herbel and Fendorf, 2005) and As(V) within solids such as scorodite (Newman et al., 1997). Dissimilatory As(V) reduction has the potential to solubilize As, as As(III) is apparently more mobile than As(V) in the environment (Bissen and Frimmel, 2003). Bacteria that use As(V) as a terminal electron acceptor for degradation of organic matter to obtain energy for growth via dissimilatory As(V) reduction have been identified in As-rich aquatic environments, including Bacillus sp. (Afkar et al., 2003), Desulfitobacterium sp. (Niggemyer et al., 2001), Desulfotomaculum sp. (Newman et al., 1997), Sulfurospirillum sp. (Ahmann et al., 1997), and Desulfomicrobium sp. (Macy et al., 2000). High As groundwater has been recognized as a major cause for serious health problems in the Hetao Basin, where As concentrations ranged between 0.6 and 572 lg/ L, with a significant proportion (up to 90%) of the As being present as As(III) (Guo et al., 2008). Zhang et al. (2002) reported that the As was introduced by mineral practices in the Langshan Mountains with higher elevations and then transported downgradient into basin aquifers. However, it is believed that groundwater As comes from geogenic sources and has been released through natural processes (Li and Li, 1994; Tang et al., 1996; Guo et al., 2008). The reductive dissolution of Fe(III) oxyhydroxides caused by microbial oxidization of organic matter is presumed to be the predominant factor controlling As mobilization (Guo et al., 2008). However, very few laboratory-scale geomicrobial experiments have been carried out to investigate the role of bacteria in mobilizing As in sediments from the Hetao aquifers in the presence of organic matter. The main objectives of this study are to (1) investigate the dominant microbial group in intact sediment samples from the Hetao aquifers; (2) evaluate As mobilization in the aquifer materials under reducing conditions stimulated by dissolved organic matter; (3) provide insights into mechanisms of As release in the aquifers. 2. Methods and materials 2.1. Sediment sampling and analysis The Hetao basin is one of the Cenozoic rift basins, which is fault-bounded. Both paleo-climate and tectonic movement have affected the sedimentary environment, palaeo-geography and lithology. During the Tertiary period, red (or deep brown) sediments occurred in an oxidizing environment which became highly saline (minerals such as gypsum and calcite). In the Quaternary period, inland lacustrine fine-grained sediments were deposited locally and a thick Mid-Cenozoic sedimentary formation developed. The fluvial sediments of the old Yellow river were mainly deposited in the southern part of the basin, with alluvial and pluvial sediments in the northern part. The lacustrine sediments usually occur at depths between 10 and 40 m below land surface (BLS) in the NW and the east of the basin, which developed in a former lake at the early stage of the late Pleistocene (around 120 ka BP). Locally, the topmost part of the sedimentary sequence consists of lacustrine sediments of small lagoons separated from the former lake and alluvial deposits, preventing diffusion of atmospheric O 2 into the aquifers (Guo et al., 2008). Arsenic concentrations in shallow aquifers from the Hetao Basin vary between 0.6 and 572 lg/l, with the high concentrations mainly being located in five hotspots, including Shuangmiao-Sandaoqiao, Shahai-Manhui, Bainaobao-Langshan, Taerhu and Shengfeng (Guo et al., 2008). Three representative boreholes, including two in the As-affected areas (BH1 in Langshan and BH3 in Shahai) and one in an As-free area (BH2 in Shanba) (Fig. 1), were drilled to obtain sediment samples from different depths up to 23 m BLS (Guo et al., 2008). Sediments to be used for bacterium incubation were preserved in anaerobic boxes (Biomerieux, France), with an O 2 adsorbent (Anaero- Pack, Mitsubishi) and an anaerobic indicator (Oxoid, England), and transported to the laboratory. They were stored at 4 C for less than 1 month. Sediment subsamples were dried and disaggregated and milled for XRD analysis. An aliquot was subjected to a mixed acid (HNO 3 HClO 4 HF) digestion for determining total element contents prior to analysis of a range of trace elements. Since a shallow aquifer with high As groundwater was found to occur at a depth of about 20 m BLS, aquifer sediments taken from 22.8 m BLS at BH1, 17.5 m BLS at BH2 and 22.3 m BLS at BH3, were selected for this study. In order to investigate the effect of sediment lithology on As leaching, two other sediment samples (silty clay and clay sampled at 13.2 and 23.4 m BLS, respectively) from BH3 were also included. Sequential extractions for quantifying As speciation in different pools in sediments were also carried out according to a sequential extraction procedure developed by Tessier et al. (1979), with some modification. The detailed procedure was described by (Guo et al., 2008). The extracted solutions were analyzed for total As. The forms of As speciation in sediments include exchangeable (F1), carbonate bound (F2), Fe Mn oxide bound (F3), organic and sulfide bound (F4), and residual (F5). Related results are given in Guo et al. (2008). This information is crucial in indicating reactivity, bioavailability and toxicity Isolation and enumeration by most probable number (MPN) Estimates of bacterial population densities of SO 4 - respiring bacteria (SRB), iron-respiring bacteria (IRB), NO 3 -respiring bacteria (NRB) and CH 4 -producing bacteria (MPB) were performed using most probable number (MPN) culturing techniques. The lactate-based medium for culturing SRB was amended with yeast extract (1 g/l)
3 H. Guo et al. / Applied Geochemistry 23 (2008) Fig. 1. Location of the Hetao Basin and sites of sediment sampling. and 8 mmol/l MgSO 4 as electron acceptors. The medium for culturing NRB, IRB and MPB was amended with glucose (1 g/l), yeast extract (0.5 g/l) and yeast extract (1 g/l), respectively (Yu et al., 1990). Anaerobic culture tubes containing 9 ml of medium were crimp-sealed under N 2 with silica gel stoppers. One-gram sediment samples from different sites were used to inoculate a decimal dilution series (highest dilution, 10 7 ) by syringe. Three tube MPNs were analyzed for each sample. Inoculated tubes were incubated at 28 C for 3 weeks and then scored. For scoring, Fe(NH 4 ) 2 (SO 4 ) 2 6H 2 O (0.1 g/l) was injected into the tubes for SRB, with Na 2 S 9H 2 O for IRB. Tubes scoring positive for both SO 4 reduction and Fe(III) reduction turned black due to the formation of ferrous sulfide. The tubes for NRB and MPB were subsampled for determination of NO 2 and CH 4 by ion chromatography (IC) and gas chromatography mass spectrometry (GC MS), respectively. The appearance of NO 2 in a given tube was used to indicate the presence of NRB at the particular dilution level, while CH 4 was used to indicate the presence of MPB. MPN in grams [wet weight] was calculated for each sample. All materials, except for sediment samples, were autoclaved at 121 C for 30 min Microcosm culture experiments The sediments for bacterium incubation provide an opportunity to assess the in situ conditions under which indigenous microbial communities exist. Microcosm culture experiments were carried out using 125 ml HDPE bottles (Nalgene) with or without addition of autoclaved nutrients (glucose) in a N 2 gas environment. Glucose served as an organic nutrient and an electron donor. Sterilized microcosm cultures were conducted after autoclaving the mixture of sediment, nutrients and aqueous solution. An artificial As solution with a similar chemical composition to local groundwater was used in the microcosm culture experiments (Table 1). The sediments and the solution were incubated together. The physical chemical characteristics of the sediments used in this study are listed in Table 2. To perform the incubation studies, 10.0 g of the selected sediment sample was transferred to the HDPE bottle containing 100 ml of artificial As solution (or deionized water) with or without addition of 2.0 g glucose (Table 3). Both artificial solution and deionized water were sterilized for 30 min at 121 C to eliminate the interference of exotic bacteria. To reduce the presence of O 2 in the system, a stream of N 2 was passed through the suspension in each vial for 5 min. After tightly sealing to minimize the intrusion of O 2, the bottles were placed in an anaerobic incubator filled with N 2 at 28 C. The sediment suspensions were sampled at regular intervals from the incubation experiments using a syringe and centrifuged at 5000 rpm for 30 min. The supernatant was decanted and filtered through a 0.45 lm cellulose acetate filter. The filtered solution was analyzed for As species, Fe and Mn Analytical methods Arsenic species in the suspensions were analyzed using a high performance liquid chromatograph (HPLC) coupled with an inductively coupled plasma mass spectrometer (ICP-MS). HPLC (1100 Series, Agilent) consisting of a system controller, a solvent delivery module, a column oven and a 6-port injection valve was used. A reversed-phase Table 1 Chemical composition of aqueous solution used in the batch culture experiments (in mg/l, except As(III) and As(V) in lg/l) No. Description ph Na + K + Mg 2+ Ca 2+ F Cl SO 2 4 HCO 3 As(III) As(V) Solution 2 Artificial water <
4 3270 H. Guo et al. / Applied Geochemistry 23 (2008) Table 2 Physical-chemical properties of the sediment samples used in the incubation studies (taken from Guo et al., 2008) Bore No. Sediment No. Depth (m) Lithology SiO 2 BH1 A 22.8 Dark grey silty sand BH2 B 17.5 Yellow silty fine sand C 13.2 Brown silty clay BH3 D 22.3 Dark grey fine sand E 23.4 Dark grey clay Al 2 O 3 Fe 2 O 3 MgO CaO Na 2 O K 2 O As Ba F Mn Mo P S Sr Table 3 Description of incubation experiments No. Sediment Nutrient Solution a Experimental conditions g sample A 100 ml Solution 2 Autoclaving the solution g sample A Glucose, 2.0 g 100 ml Solution 2 Autoclaving the mixture of nutrient and solution g sample A 100 ml Solution 2 Autoclaving the sediment and the solution g sample A Glucose, 2.0 g 100 ml Solution 2 Autoclaving the sediment and the mixture of nutrient and solution g sample A 100 ml deionized water Autoclaving the deionized water g sample A Glucose, 2.0 g 100 ml deionized water Autoclaving the mixture of nutrient and deionized water g sample B 100 ml deionized water Autoclaving the deionized water g sample B Glucose, 2.0 g 100 ml deionized water Autoclaving the mixture of nutrient and deionized water g sample C 100 ml Solution 2 Autoclaving the solution g sample C Glucose, 2.0 g 100 ml Solution 2 Autoclaving the mixture of nutrient and solution g sample C 100 ml Solution 2 Autoclaving the sediment and the solution g sample C Glucose, 2.0 g 100 ml Solution 2 Autoclaving the sediment and the mixture of nutrient and solution g sample C 100 ml deionized water Autoclaving the deionized water g sample C Glucose, 2.0 g 100 ml deionized water Autoclaving the mixture of nutrient and deionized water g sample D 100 ml Solution 2 Autoclaving the solution g sample D Glucose, 2.0 g 100 ml Solution 2 Autoclaving the mixture of nutrient and solution g sample D 100 ml Solution 2 Autoclaving the sediment and the solution g sample D Glucose, 2.0 g 100 ml Solution 2 Autoclaving the sediment and the mixture of nutrient and solution g sample D 100 ml deionized water Autoclaving the deionized water g sample D Glucose, 2.0 g 100 ml deionized water Autoclaving the mixture of nutrient and deionized water g sample E 100 ml Solution 2 Autoclaving the solution g sample E Glucose, 2.0 g 100 ml Solution 2 Autoclaving the mixture of nutrient and solution g sample E 100 ml Solution 2 Autoclaving the sediment and the solution g sample E Glucose, 2.0 g 100 ml Solution 2 Autoclaving the sediment and the mixture of nutrient and solution g sample E 100 ml deionized water Autoclaving deionized water g sample E Glucose, 2.0 g 100 ml deionized water Autoclaving the mixture of nutrient and deionized water indicates no addition of nutrient. a Chemical composition of aqueous solution is shown in Table 1. C18 column (Capcell, Pak, 250 mm 4.6 mm, 5 lm particle size) was used for separation of As species. ICP-MS (7500C, Agilent) was used as a detector. Concentrations of major cations and trace elements in solutions were determined by inductively coupled plasma optical emission spectrometry (ICP-OES, IRIS Intrepid II, Thermo) and inductively coupled plasma mass spectrometry (ICP-MS, X Series II, Thermo), respectively. 3. Results 3.1. Characterization of sediments Chemical compositions of sediment samples are shown in Table 2. The SiO 2 concentrations range between 49.8 and 76.4 wt.%, with high concentrations in the sand samples and low concentrations in the silty clay samples. The Fe 2 O 3 concentrations lie in the range wt.%, which are close to the values in the sediments from the As-affected areas in Bangladesh (BGS and DPHE, 2001). The high concentrations are found in silty clay in BH1 and BH3, which should be from the lacustrine environment and enriched in organic matter. The dark grey sediments of the aquifers from BH1 and BH3 imply that they are from a moderate-strong reducing environment, while the yellow sediments from BH2 imply a weak oxidizing environment (Guo et al., 2008). Concentrations of different As forms in the selected sediments are shown in Table 4. Of the chemically active As forms (exchangeable, bound to carbonates, bound to Fe
5 H. Guo et al. / Applied Geochemistry 23 (2008) Table 4 Concentrations of different As forms in sediments (taken from Guo et al., 2008) a Sample No. F1 (lg/ F2 (lg/ F3 (lg/ F4 (lg/ F5 A B C D E a F1: exchangeable form; F2: carbonate bound form; F3: Fe Mn oxide bound form; F4: organic matter and sulfide bound form; F5: residual form. Mn oxides, bound to insoluble organics and sulfides), % is in the As bound to Fe Mn oxides (F3) of the sediments. The highest percentage is observed in the fine sand from BH2 due to the higher redox potential Most probable number of bacteria isolated from sediments Two sediment samples (Sample B and Sample E in Table 2) were used to estimate anaerobic bacterial population numbers. Enumeration of bacterial populations using MPN reveals that samples from both the As-affected area and the As-free area have >10 4 anaerobic bacteria per gram of sediment [wet wt.] (Table 5). All samples contain NRB (>10 3 per gram of sediment [wet wt.]), but only the sediment from the As-free site had culturable MPB (>10 4 per gram of sediment [wet wt.]). Large amounts of SRB were isolated from the Sample B (>10 3 per gram of sediment [wet wt.]), while more than 10 3 IRB per gram of sediment [wet wt.] were observed in Sample E. It was found that the dominant anaerobic microbes seemed to be the NRB in the sediments from the As-affected area, while the MPB were dominant in the Asfree area. It should be noted that although these counts are satisfactory for comparing the relative amounts of the organisms in the different sediments, MPN counts can underestimate cell numbers by several orders of magnitude Culture experiments Dissolved As in incubations without amendment Concentrations of As(III) and total As in the Sediment A suspensions generally declined over the duration of incubation without amendment (Fig. 2). In the As solution-pristine sediment suspensions (No.3), As(III) concentrations systematically decreased from 260 lg/l to around 20.0 lg/l within 3 days. In the heat-sterilized suspension (No.5), the decrease in concentrations generally occurred slowly. After 27 days, total As reached 22.1 lg/l. In the deionized water-pristine sediment suspensions (No. 7), both As(III) and As(V) were observed within 3 days, and reached a plateau at 6 days with peak concentrations of 6.5 and 16.2 lg/l, respectively (Fig. 2a). They decreased afterwards, and were comparable to those in other incubations after 27 days. During this incubation, the released As was equal to 0.09 lg/g. A similar behavior of As species was found in the suspension without amendment in the case of other sediments (with total dissolved As concentrations between 3 and 30 lg/l, corresponding to the lg/g of the released As, not shown) Dissolved As in suspensions amended with glucose Dissolved As concentrations measured in the amended suspensions increased with time (Fig. 3). In the case of sediment C, As(III) concentration rose from 0 to 296 lg/l within 9 days, and then remained relatively steady until 27 days. In contrast, release of As(III) was roughly in equilibrium from sediments A, B, D and E at 18 days of incubation. The highest concentration of dissolved As was found in the sediment C suspension, and the released As corresponds to 3.81 lg/g. The incubation also stimulated a release of As in the amended suspension of Sediment B sampled from the As-free aquifer. Total dissolved As was up to 173 lg/l, corresponding to 1.73 lg/g of As mobilized during the incubation. The lowest concentration of dissolved As was Fig. 2. Time series of As species and total As concentrations during the incubations of Sediment A-As solution without amendment. (a): Solid lines and dashed lines correspond to As(III) and As(V), respectively. Incubation Nos. 3, 5 and 7 conducted without amendment of glucose using suspensions of Sediment A and solution 2, sterilized Sediment A and solution 2, Sediment A and deionized water, respectively.
6 3272 H. Guo et al. / Applied Geochemistry 23 (2008) Fig. 3. Time series of As species and total As concentrations during the incubations amended with glucose. (a): Solid lines and dashed lines correspond to As(III) and As(V), respectively. Incubation Nos. 8, 17, 23, 29 and 40 conducted using suspensions of Sediments A, B, C, D and E amended with glucose and deionized water, respectively. observed in the amended suspension of Sediment A obtained at a depth of 22.8 m in the As-affected BH1. The amendment of glucose in the incubation greatly increased dissolved As concentration in the suspension. In the case of sediment E, dissolved As concentrations of the suspension amended with the glucose (172 lg/l at the end of incubation) were about 10 times those of the suspension without amendment (17.8 lg/l at the end of incubation). This indicates that addition of glucose as a potential electron donor results in a marked stimulation in the release of As(III) and As(V). Although microbial activities occur in the incubation, no methylated As was detected in the amended suspension. In general, As(III) was preferentially released at the beginning of the incubation and initially reached the plateau, followed by As(V) (Fig. 3a). For example, dissolved As(III) concentration of the Sediment D suspension increased within the first 18 days, and generally remained constant after 18 days of incubation, while dissolved As(V) concentration kept increasing slightly until day 27. Although concentrations of As species were not measured in the suspensions within the first 3 days, the proportion of As(III) mostly falls in the range between 70% and 90%, broadly comparable with the ratio of As(III) to total As found in shallow groundwaters from As-affected aquifers of the Hetao Basin (Guo et al., 2008). Although the initial As species on the sediment particles is unknown, it appears that the addition of glucose may lead to the reduction of As(V) to As(III) and/or prevent a gradual oxidation of As(III) in solution Dissolved As in suspensions amended with glucose and As solution Artificial As solution was added in the suspensions to investigate As mobilization in the presence of solution As. For most of the sediments tested, As concentrations generally decreased within 3 days of incubation, and then remained steady until day 27, in the heat-sterilized suspensions amended with glucose (Fig. 4b,d,f), which were comparable to those in the suspensions without amendment. This indicates that As mobilization mediated by microbial respiration possibly occurs slowly in natural conditions with a relatively low concentration of organic C. In comparison with the suspensions without amendment, dissolved As concentrations are a little higher in the heat-sterilized incubations with the addition of glucose, suggesting that the existence of dissolved organic matter would lead to the release of As species in conditions of limited microbial activity. Bauer and Blodau (2006) proposed that competitive adsorption between As and dissolved organic matter would be a cause of As release. Concentrations of dissolved As(V) generally remained constant, with the ratio of As(III) to total As ranging between 30% and 60%. In contrast, total As concentrations decreased within the first 3 days, and then gradually increased until 27 days in the pristine sediment suspensions amended with glucose, except for Sediment E (Fig. 4b,d,f,h). The first decrease possibly arises from the physicochemical processes between solution As, the sediment and the glucose (including adsorption, complexation, coprecipitation) with the presence of limited microbial respiration. Addition of glucose stimulates the relatively fast release of As, although the increase in As concentrations relative to the heat-sterilized incubations is dependent on the specific sediment. The amount of As released from the amended suspensions was found to be largest in the case of Sediment C (Fig. 4d), followed by Sediment D and Sediment A. During the incubation, the quantity of As mobilized in the Sediment C suspension reached 4.0 lg/g of the sediment relative to the heat-sterilized incubation. Concentrations of dissolved total As increased by 152 lg/l (from 23.7 to 176 lg/l) and 175 lg/l (from 45.5 to 221 lg/l) within the last 18 days in the case of Sediment D (Fig. 4f) and Sediment A (Fig. 4b), respectively. Although As concentrations at the end of incubation were generally lower than the initial As concentrations in the case of Sediments A, D and E, they were 2 5 times those of the heat-sterilized suspension. The trend of an increase in As concentrations was mostly observed at the end of incubation, the higher amounts of As would be released with a longer time of incubation.
7 H. Guo et al. / Applied Geochemistry 23 (2008) Fig. 4. Time series of As species and total As concentrations during the incubations of pristine sediments or heat sterilized sediments amended with glucose and As solution. (a), (c), (e) and (g): Solid lines and dashed lines correspond to As(III) and As(V), respectively. Incubation Nos. 4, 19, 25, 36 conducted using suspensions of Sediments A, C, D, and E amended with glucose and Solution 2, respectively, while Nos. 6, 21, 27, 38 used sterilized suspensions of Sediments A, C, D and E amended with glucose and Solution 2, respectively.
8 3274 H. Guo et al. / Applied Geochemistry 23 (2008) The change of As(III) concentrations was comparable with that of total As in all suspensions (Fig. 4). Except for Sediment E, dissolved As(III) declined within the first 3 days, and then increased afterwards. Whereas, concentrations of dissolved As(V) generally decreased in the first 6 9 days, and then increased until 27 days of incubation, indicating that the release of As(V) lags that of As(III) (Fig. 4a, c and e). The first decrease in dissolved As(V) concentrations seems to attribute to the reduction of solution As(V), since it is coincident with the increase in concentrations of dissolved As(III). In general, dissolved As(V) concentrations within the last 18 days were higher than initial concentrations of As(V) in the case of all the sediments. The ratio of As(III) to total As is in the range between 70% and 90%, a little higher than that in the corresponding heat-sterilized suspensions. For Sediment E, concentrations of As(III) and total As typically decreased during 27-day incubation (Fig. 4g and h). Although the microbial activity was not tested, it appears that the microbe-related processes should be sufficiently active since a decrease in ph from 7.87 to 5.39 is observed within 27 days of incubation. However, bacterially induced reduction does not result in the increase in dissolved As concentrations. The mineralogical composition of the sediment is possibly a cause of the continuous decrease in As concentrations. The results of XRD analyses revealed that Sediment E contains 30% chlorite and 30% mica (Guo et al., 2008). The observed decrease in solution ph associated with the microbial processes would enhance the As adsorption capacity of the clay minerals (Lin and Puls, 2000; Goldberg, 2002; Doušová et al., 2006; Chakraborty et al., 2007), which are believed to readsorb As mobilized under anaerobic conditions. 4. Discussion 4.1. Role of microbes in As mobilisation It is suggested that microbial processes in the sediments rich in organic matter create a favorable reducing environment, facilitating mobilization of As in the aquifers of the Hetao Basin (Guo et al., 2008), which is commonly believed to play an important role in the mobilization of As in Bangladesh groundwater (Islam et al., 2004; van Geen et al., 2004; Anawar et al., 2006). Most probable number (MPN) indicates IRB, NRB and SRB are present in the As-affected aquifer. The IRB would stimulate the reductive dissolution of Fe(III) oxides/oxyhydroxides, and therefore the release of As. Abiotic dissolution of Fe(III) oxyhydroxides would proceed more slowly and be ineffective under environmental conditions (Cummings et al., 1999). At the end of incubation, high concentrations of dissolved Fe are found in the amended suspensions (up to 98.3 mg/l), again confirming that Fereducing bacteria are present in the original Hetao aquifer material. In addition to reductive dissolution of Fe(III) oxides/oxyhydroxides, IRB would stimulate the reduction of As(V) to As(III). Stolz et al. (1999) found that the microaerophile Sulfurospirillum barnesii strain SES-3 can also respire As(V), in addition to Se, Fe(III), S 2 O 2 3, elemental S, Mn(IV), NO 3 and NO 2, trimethylamine oxide and fumarate. There are many studies showing that both NO 3 reducers (NRB) and SO4 reducers (SRB) would also use As(V) as a terminal electron acceptor. Chrysiogenes arsenatis strain BAL- 1T can respire NO 3, which would also use As(V) as a terminal electron acceptor (Macy et al., 1996). Newman et al. (1997) found that Desulfotomaculum auripigmentum strain OREX-4 has the ability to simultaneously reduce SO 2 4 and As(V), and produces the As sulfide mineral orpiment both in intra- and extracellular environments. Although they would not directly convert the related As-hosting oxide minerals (such as Fe oxides and Mn oxides), they may catalytically reduce As(V) to As(III), which would cause reductive desorption of As because the adsorption affinity of oxide minerals for As(III) at near-neutral ph is known to be substantially less than that for As(V) (Dzombak and Morel, 1990). Therefore, the black box remains to be opened for the purpose of revealing whether the microbially driven conversion of Fe(III) oxides/oxyhydroxides to Fe(II) or the reduction of As may be important for the mobilization of As. The inhibition of As release during the heat-sterilized incubation of the sediments is a strong indication that microorganisms play an important role in As mobilization. It is speculated that the reduction of a surface coating of ferrihydrite enriched in As by dissimilatory Fe-reducing bacteria was perhaps prohibited. For all incubations with the addition of As solution, the decrease in As concentrations was observed within 3 days, reflecting that the physicochemical re-equilibration between solid and dissolved phase dominates the As behavior with the presence of weak microbial respiration at the beginning of the incubation. It also implies that the microbial activities are considerably enhanced after 3 days of incubation, during which significant stimulation in As release occurs with the respiration of organic matter. The relatively constant of As(III) and As(V) concentrations during the last 20-day incubation of the heat-sterilized sediments indicates that the reduction of As was also inhibited. The reduction of As(V) to As(III) observed at the initial stage (6 9 days) of incubations amended with glucose suggests that a process of dissimilatory microbial reduction is stimulated by the addition of substrate. The bacteria SRB, NRB and IRB would be involved in this process (Macy et al., 1996; Oremland et al., 2000, 2002; Zobrist et al., 2000). It is therefore speculated that the release of As is triggered by reduction to As(III) at an early stage of microbially mediated redox processes (Stüben et al., 2003). The increase in As(V) concentrations is concomitant with that of As(III) concentrations in the amended suspensions during the later stage of the incubation, suggesting that the reduction of Fe(III) oxyhydroxides as well as the reduction of As simultaneously results in the mobilization of As at relatively low redox conditions. The dissolved As is predominately in the As(III) form, which is consistent with As species in groundwater from the shallow aquifers of the Hetao Basin, Inner Mongolia Decoupling between the reduction of Fe/Mn oxides and the release of As In addition to the dissimilatory reduction of Fe(III) oxyhydroxides, the reduction of Mn oxides is another impor-
9 H. Guo et al. / Applied Geochemistry 23 (2008) tant cause for mobilization of As. At the early stages of organic material degradation, slightly reducing conditions would mobilize As bound to Mn phases due to reduction of Mn 4+ to Mn 2+ (Stüben et al., 2003). Although the mobilized As can be readsorbed on the Fe(III) oxyhydroxides, it would be remobilized as long as the reduction of Fe(III) oxides takes place in the continuously anaerobic incubation. At the end of the incubation, the mobilized As in the suspension amended with glucose is positively well-correlated with the As bound to Fe/Mn oxides of the original sediment (Fig. 5). The amount of As released accounts for about 60 70% of As bound to Fe/Mn oxides. However, the amount of As released from the Sediment C suspensions is a little greater than that of As bound to Fe/Mn oxides. There must be other processes responsible for the release of As, in addition to the reduction of Fe/Mn oxides. The solution ph continuously decreases over the course of the incubation due to the microbial degradation of organic substance, and reaches 5.36 at 27 days. The low solution ph would cause the dissolution of carbonate minerals, and subsequently give rise to mobilization of As bound to carbonates (Calmano et al., 1993). The XRD results show that Sediment C contains a higher concentration of calcite (20%) in comparison with the other samples (15%). Therefore, the microbially mediated mobilization of As with the organic nutrient as an electron donor is strongly associated with the As bound to Fe/Mn oxides and the labile As, possibly as well as the As bound to carbonates. The rate of dissolution of Fe oxyhydroxides in the suspensions amended with glucose is probably considerably higher than in the natural environment. It is worth noting that the fraction of Fe mobilized by the suspensions amended with glucose corresponds to only 2 4% of the total amount of Fe in the sediment. Therefore, the small fraction of Fe released may indicate that the short-term incubations with glucose have led to the reduction of poorly crystallized phases, such as ferrihydrite, and not the reduction of goethite or hematite (Zachara et al., 2002). It implies that the reduction of the small fraction Fig. 5. The plot of As bound to Fe/Mn oxides (F3) of the original sediments versus the mobilized As in the corresponding sediment suspensions amended with glucose. The mobilized As for Sediments A, B, C, D and E corresponds to concentrations of dissolved As observed in the incubations Nos. 8, 17, 23, 29 and 40 as defined in Fig. 3, respectively. of Fe oxides (about 2 4%) as poorly crystallized phases would release 60 70% of As bound to Fe/Mn oxides, confirming that the poorly crystallized Fe(III) oxides are great scavengers for As by adsorption (Richmond et al., 2004) Implication for As distribution in groundwater Less As is mobilized from both the dark grey sediments sampled in the boreholes of the As-affected areas and the yellow sediment sampled in the borehole of the As-free area in the incubations without amendment (less than 30 lg/l). The reduction of Fe(III) oxyhydroxides is believed not to be involved in the released of As, since the quantity of released As roughly corresponds to that of exchangeable As (F1) in the original sediments (Table 4). The Fe oxyhydroxide coatings universally exist in the shallow aquifers with the presence of As-free groundwater. These aquifers are naturally poor in organic matter, and not covered by an impermeable clay layer (Guo et al., 2008). Low groundwater As concentration in such shallow aquifers is consistent with the retention of As during the incubations of the aquifer sediment without amendment. The mobilization of As is observed from these sediments over the course of the glucose-amended incubation. The release of a significant fraction of As bound to Fe/Mn oxides from the same type of sediment with addition of an organic substance provides insight into the phenomenon that groundwater As concentrations are typically high in the shallow aquifers with closed semiclosed geochemical conditions, a relatively high content of organic substance and a slow groundwater flow. Guo et al. (2008) found that an argillaceous layer of lacustrine origin covering the shallow aquifer with high As groundwater restricts aquifer flushing, reduces the supply of oxidants such as O 2 and NO 3, and gradually results in an anaerobic environment. The reducing environment, together with the presence of abundant organic matter in the aquifer sediments, would promote the release of As, as shown in the incubations. The highly variable nature of fluvio-lacustrine deposits determining the accessibility of the oxidants and the availability of organic substance may help to explain the spatial variability of As concentrations in shallow aquifers. It also implies that groundwater As concentrations would increase if the leaching of labile dissolved organic C into those yellowish sediment aquifers produces the reduction of a large proportion of the Fe(III) oxyhydroxides mediated by anaerobic bacteria respiration. Therefore, it is particularly important to prevent anthropogenic organic contaminants from penetrating into the shallow As-free aquifers. In comparison with the natural aquifer, the rate of As release is much more significant in the incubation studies. For Sediment C, total dissolved As increases by 380 lg/l during 27 days of incubation amended with glucose, while groundwater As concentration is around 500 lg/l after Holocene aquifers have been flushed for thousands of years. One possible reason is that the large amount of dissolved organic substance (20 g/l glucose) in the suspensions would accelerate the respiratory process of anaerobic bacteria and therefore greatly catalyze the reduction of Fe(III) oxides. On the other hand, the
10 3276 H. Guo et al. / Applied Geochemistry 23 (2008) Table 5 Most probable number of bacteria isolated from sediments Sediment No. Sulfate reducers (cells/g) a Fe(III) reducers (cells/g) a Nitrate-reducers (cells/g) a Methanogenic bacteria (cells/g) a B 1.41 ( ) ( ) 9.20 ( ) ( ) 10 4 E 9 (1.0 36) 2.43 ( ) ( ) 10 4 n.d. a Values in parentheses indicate 95% confidence level interval. sediment/water ratios in the aquifer (8:1 wt./wt., Islam et al., 2004) are much higher than those in the incubation (1:10 wt./wt.). The process of As mobilization stimulated by microorganisms may be less pronounced at the higher sediment/water ratio of an actual aquifer (van Geen et al., 2004). 5. Conclusions Both dark grey sediments obtained from shallow aquifers of the As-affected areas and yellow sediments sampled from shallow aquifers of the As-free area contain different groups of anaerobic bacteria, including Fe(III) reducers, NO 3 reducers and SO 4 reducers, although the dominant microorganisms are categorized into different microbial groups. These microbes naturally present in the Hetao aquifers play an important role in mobilizing As in the incubations amended with glucose. Although total As concentrations decrease within the first 3 days of incubations amended with glucose and As solution, it is followed by the release of As. The release of As may be triggered by reduction to As(III) at the early stage of microbially mediated redox processes, and accelerated by the reduction of Fe(III) oxyhydroxides at the later stage of incubation with relatively low redox conditions. Comparison of the incubations and sequential extraction results suggests that the labile As (exchangeable As) and Fe/Mn oxides bound As should be readily mobilized during incubations amended with glucose as an electron donor. Although a small fraction of Fe present in the sediment is released, a significant proportion of As bound to Fe/ Mn oxides is mobilized. Since the organic substance and the anaerobic environment are believed to be the preliminary factors accelerating the microbially mediated release of As, the highly variable nature of fluvio-lacustrine deposits determining the accessibility of the oxidants and the availability of organic substance may help to explain the spatial variability of As concentrations in shallow aquifers of the Hetao Basin. It also implies that groundwater As concentrations would increase with the leaching of labile dissolved organic C into those yellowish sediment aquifers reducing a significant proportion of the Fe(III) oxyhydroxides mediated by anaerobic bacterial respiration. Acknowledgements This study was financially supported by the National Natural Science Foundation of China (No and ), the Program for New Century Excellent Talents in University (No. NCET ), and the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry. Dr. Fei Liu, Mr. Chao Wei, Mr. Ruopeng Liu, and Dr. Chunbo Hao are gratefully acknowledged for laboratory assistances. We thank the associate editor David Polya and two anonymous reviewers for their contributions to improve the manuscript. References Afkar, E., Lisak, J., Saltikov, C., Basu, P., Oremland, R.S., Stolz, J.F., The respiratory arsenate reductase from Bacillus selenitireducens strain MLS10. FEMS Microbiol. 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