Combined Speciation Analysis by X-ray Absorption Near-Edge

Dec 23, 2010 - Sub-Department of Environmental Technology, Wageningen University, 6700 EV Wageningen, The Netherlands, Institute for Ecopreneurship, ...
0 downloads 0 Views 1MB Size
Download PDF
Environ. Sci. Technol. 2011, 45, 1067–1073

Combined Speciation Analysis by X-ray Absorption Near-Edge Structure Spectroscopy, Ion Chromatography, and Solid-Phase Microextraction Gas Chromatography-Mass Spectrometry To Evaluate Biotreatment of Concentrated Selenium Wastewaters M A R K U S L E N Z , * ,†,‡ E R I C D . V A N H U L L E B U S C H , †,§ FRANC ¸ O I S F A R G E S , |,⊥ SERGEI NIKITENKO,# PHILIPPE F. X. CORVINI,‡ AND P I E T N . L . L E N S †,∇ Sub-Department of Environmental Technology, Wageningen University, 6700 EV Wageningen, The Netherlands, Institute for Ecopreneurship, University of Applied Sciences Northwestern Switzerland (FHNW), Gru ¨ ndenstrasse 40, 4132 Muttenz, Switzerland, Laboratoire Ge´omate´riaux et Environnement (LGE), Universite´ Paris-Est, EA 4508, 5 bd Descartes, 77454 Marne la Valle´e Cedex 2, France, Laboratoire de mine´ralogie et de cosmochimie du Muse´um (LMCM) and UMR CNRS 7202, Muse´um National d’Histoire Naturelle, 61 rue Buffon, 75005 Paris, France, Department of Geological and Environmental Sciences, Stanford University, Stanford, California 94305, United States, DUBBLE at European Synchrotron Radiation Facility (ESRF), Netherlands Organization for Scientific Research (NWO), BP 220, 38043 Grenoble Cedex 9, France, and UNESCO-IHE Institute for Water Education, Westvest 7, 2611 AX Delft, The Netherlands

Received July 9, 2010. Revised manuscript received November 23, 2010. Accepted November 30, 2010.

In this study we evaluate the potential of anaerobic granular sludge as an inoculum for the bioremediation of seleniumcontaminated waters using species-specific analytical methods. Solid species formed by microbial reduction were investigated using X-ray absorption near-edge structure (XANES) spectroscopy at the selenium K-edge. Furthermore, dissolved selenium species were specifically determined by ion chromatography (IC) and solid-phase microextraction gas chromatography-mass spectrometry (SPME-GC-MS). Least-squares linear combination of the XANES spectra for samples incubated with the highest

* Corresponding author e-mail: [email protected]; phone: +41 614 674 791; fax: + 41 614 674 290. † Wageningen University. ‡ University of Applied Sciences Northwestern Switzerland (FHNW). § Universite´ Paris-Est. | Muse´um National d’Histoire Naturelle. ⊥ Stanford University. # Netherlands Organization for Scientific Research. ∇ UNESCO-IHE Institute for Water Education. 10.1021/es1022619

 2011 American Chemical Society

Published on Web 12/23/2010

selenate/selenite concentrations (10-3 M) show the predominance of elemental selenium and a Se(-I) selenide, such as ferroselite, the thermodynamically most stable iron selenide. In contrast, elemental selenium and Se(-II) selenides are the main species detected at the lower selenate/selenite concentrations. In each repeated fed batch incubation, most aqueous selenite anions were converted into solid selenium species, regardless of the type of electron donor used (acetate or H2/CO2) and the selenium concentration applied. On the other hand, at higher concentrations of selenate (10-4 and 10-3 M), significant amounts of the oxyanion remained unconverted after consecutive incubations. SPME-GC-MS demonstrated selenium alkylation withbothelectrondonorsinvestigated,asdimethylselenide(DMSe) and dimethyl diselenide (DMDSe). Selenite was even more alkylated in the presence of H2/CO2 (maximum 2156 µg of Se/L of DMSe + DMDSe) as compared to acetate (maximum 50 µg of Se/L). In contrast, selenate was less alkylated using both electron donors (maximum 166 and 3 µg of Se/L, respectively). The high alkylation potential for selenite limits its bioremediation in selenium laden waters involving H2/CO2 as the electron donor despite the fact that nontoxic elemental selenium and thermodynamically stable metal selenide species are formed.

1. Introduction Selenium has been referred to as the “essential toxin” due to its essential nature and toxic effects on living organisms in a narrow concentration range (1). The environmental fate and the toxicity of selenium strongly depend on its complex chemical speciation (2). In the past, water-soluble selenium oxyanions (i.e., selenite and selenate) have been related to severe harmful effects on aquatic life in a number of cases (1, 3), most prominently in the western U.S. Kesterson Reservoir National Wildlife Refuge (4). Diverse physical and/or chemical (filtration, adsorption, precipitation, reduction) treatment options have been investigated to tackle the problem of selenium contamination in aquatic environments (5). A grave limitation of filtrationor adsorption-based techniques is, however, that selenium oxyanions become strongly concentrated in retentates (e.g., during reverse osmosis membrane filtration) or in eluates (e.g., during ion exchange treatment), respectively (6, 7). The safe disposal of such selenium-laden watersscurrently considered as an industrial waste by environmental authorities such as the U.S. EPA (8)ssignificantly contributes to the high operational costs associated with these technologies, since simple disposal in, e.g., open evaporation basins raises concerns of selenium toxicity to wildlife (9). Anaerobic granular sludge (aggregates of microorganisms and an inorganic matrix used in anaerobic wastewater treatment) is a potent inoculum for the bioremediation of waters low in selenium concentration (µg of Se/L), since it harbors selenium-respiring microorganisms that convert selenium oxyanions to elemental selenium (10, 11). Such elemental selenium is considered poorly bioavailable due to its low solubility. In this investigation we study the applicability of anaerobic granular sludge not only to treat waters low in selenium concentration, but also to convert highly concentrated solutions of selenate and selenite to elemental selenium. For this, two different electron donors, i.e., acetate and hydrogen/carbon dioxide (H2/CO2) were evaluated. The removal of dissolved selenium species from the liquid phase was assessed by ion chromatography (IC) and solid-phase microextraction gas chromatography-mass VOL. 45, NO. 3, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1067

spectrometry (SPME-GC-MS). To evaluate the treatment success in terms of the stable solid end product of microbial transformation, i.e., elemental selenium, metal selenides, or organoselenides (compare 5), nondestructive X-ray absorption near-edge structure (XANES) spectroscopy at the selenium K-edge was applied.

2. Experimental Section 2.1. Source of Biomass. Anaerobic granular sludge from a full-scale upflow anaerobic sludge bed (UASB) reactor treating paper mill wastewater (Industriewater Eerbeek B.V., Eerbeek, The Netherlands) was utilized for the experiments. This inoculum has been characterized microbially (12, 13) and regarding its (trace) metal content (14, 15) and has been previously described to be effective for selenate removal from low contaminated wastewaters (10, 16). 2.2. Selenium Removal Assays. Selenite and selenate removal from the liquid phase was studied in anaerobic batch assays (duplicate) using 0.5 g (wet weight) of anaerobic granular sludge in 50 mL of methanogenic medium as described previously (17, 18). Acetate was added by diluting a neutralized concentrated stock solution to 1.88 g L-1 (providing 2.5 × 10-1 M electrons/L of medium). Hydrogen was added by flushing the serum bottles with a H2/CO2 mixture (80/20, v/v) and adjusting the final headspace pressure to 1.7 bar (providing 1.5 × 10-1 M electrons/L of medium). The anaerobic granular sludge was incubated for 4 weeks in the presence of selenium oxyanions. Due to the faster consumption of the electron donor, the medium was renewed in weekly intervals when using H2/CO2, in contrast to biweekly intervals when acetate was fed. Note that both electron donors were provided in excess to allow for complete selenium oxyanion reduction. Selenium oxyanions were added from concentrated stock solutions (concentration verified by Inductively Coupled Plasma Optical Emission Spectroscopy, ICP-OES) to final concentrations of 10-5 to 10-3 M selenite and selenate. To study the release of alkylated species from biomass, a selenium-free medium was supplied twice subsequently to the incubation with selenium oxyanions. Upon termination of the experiment, aliquots of the anaerobic granular sludge were placed in a custom-made sample holder of poly(tetrafluoroethylene) using an anaerobic glovebox. Samples were sealed from ambient air by Kapton tape. The sample holders were stored (4 °C) under N2 in a wide-mouth bottle until the XANES measurements. 2.3. Selenium Liquid-Phase Speciation. Selenite and selenate were determined by IC as described previously (17) (details in the Supporting Information). Dimethyl selenide (DMSe) and dimethyl diselenide (DMDSe) were determined by SPME-GC-MS as previously described (16) (details in the Supporting Information). The amount of solid selenium formed (both suspended in the liquid phase and associated with the sludges) was defined as the difference between the selenium concentration fed initially and the sum of selenium determined as selenate, selenite, DMSe, and DMDSe measured at the end of the experiment (16). 2.4. Selenium Solid-State Speciation. Selenium K-edge (12.66 keV) XANES experiments were performed as described previously at the DUBBLE beamline (BM26, ESRF, Grenoble, France) (15). The energy calibration for both monochromators was achieved using gray, trigonal selenium placed between two ionization chambers (transmission mode) during all measurements. The main edge crest maximum for elemental trigonal selenium, located at 12 662.5 eV, was used throughout the study. XANES spectra were normalized using the X-ray absorption fine structure (XAFS) software package (19) using standard procedures (20). Least-squares linear combination XANES fittings were done using MS Excel SOLVER. Principal component analysis (PCA) using the normalized spectra was done with the XANES dactyloscope 1068

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 45, NO. 3, 2011

software (21). The following standards were used throughout this study: red R-monoclinic and gray trigonal as elemental selenium standards; penroseite, krutaite, and ferroselite as Se(-I) selenide standards; achavalite, klockmannite, stilleite, berzelianite, and sodium selenide as Se(-II) selenide standards; selenocysteine as Se(-II) organoselenide; sodium selenite and sodium selenate as oxidized selenium species. Model mineral compounds were verified using micro X-ray diffraction (µ-XRD) (15). During consecutive measurements, some samples showed beam-induced reduction due to the X-ray beam. In particular, incubations with the lowest concentrations (10-5 M) of both selenate and selenite showed sluggish evidence of radiation-induced reduction (beamreduced samples are marked by an asterisk, Table 1). Therefore, only one quick scan on a fresh spot was collected to minimize radiation-induced reduction effects. Hence, the collected spectra for those samples low in selenium concentration show undetectable evidence of radiation-induced reduction, because of its relatively low absorbance at 12 663 eV, which is where elemental selenium absorbs the most. Thus, their speciation modeling was computed on those first scans, solely. For the other samples, 3-5 consecutive scans were measured and averaged. Before averaging, all individual scans were carefully checked for any spectral inconsistency due to beam instability, beam damage, and any other experimental bias of any kind.

3. Results 3.1. Effect of the Electron Donor on Selenium Oxyanion Removal. Anaerobic granular sludge reduced both selenite and selenate from the liquid phase in repeated incubations (Figure 1). Generally, higher proportions of solid selenium were formed in the batches containing selenite (Figure 1A,C) compared to selenate (Figure 1B,D). Selenite was reduced to solid selenium by more than 93% during a period of 4 weeks with only one exception (72%, week 1, 10-4 M), independent of the type of electron donor used or the selenite concentration applied. The highest total amount of solid selenium (78 mg of Se/L) was formed from 10-3 M selenite (week 3, H2/ CO2). For selenate in contrast, the amount of solid selenium formed decreased during repeated batch incubation with 10-5 and 10-4 M oxyanion, respectively, using both H2/CO2 (Figure 1B) and acetate (Figure 1D) as electron donors. Only minor proportions (66 atom %), whereas those that received selenate were mostly converted to selenide(-II) species (such as achavalite, berzelianite, and stilleite). However, in all batches that received 10-5 M selenium oxyanions (which were subject to minimal beam-induced reduction), the modeled speciation was again mainly determined by Se(-II) selenides, i.e., berzelianite and achavalite (up to 69% and 58%, respectively) and elemental selenium (up to 38%) (Table 1).

4. Discussion 4.1. Selenium Oxyanion Reduction by Anaerobic Granular Sludge. Thanks to the direct, species-specific analyses, this study shows that anaerobic granular sludge can efficiently reduce both selenite and selenate to solid selenium species using H2/CO2 and acetate as electron donors (Figure 1). However, in the case of selenate, the biomass did not sustain the reductive efficiencies that were initially observed when selenate was fed repeatedly (10-4 and 10-3 M, Figure 1B, D). This constitutes a rather unexpected result, since the development of a selenate respiring population was previously observed in continuously operated bioreactors treating low selenate concentrations (10-5 M) using the same inoculum. Previously, this resulted in an increased removal capacity of the biomass at a higher selenate concentration of 10-4 M (10, 16). Although the experiments of the present study were conducted over 4 weeks, a slow growth of the selenate-reducing populations might explain the low removal efficiencies observed toward the end of the experiments. Accordingly, the higher removal efficiencies achieved in the first incubation with selenate (Figure 1D) can be explained by a cometabolic reduction by other microbial groups such as sulfate-reducing bacteria (10), present in the inoculum in a large diversity (12). However, since sulfate-reducing bacteria are strongly and irreversibly inhibited by high selenate concentrations (10, 22), their contribution to the removal of selenate upon prolonged exposure is expected to be rather small. The presence of the respiratory end product of sulfatereducing bacteria (i.e., sulfide) might also explain the higher removal efficiencies observed for selenite, in contrast to that for selenate (Figure 1A, D). This is due to the fact that dissolved sulfide and selenite react spontaneously and precipitate to elemental sulfur and elemental selenium (23). Although no VOL. 45, NO. 3, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1069

FIGURE 1. Influence of electron donors H2/CO2 (A, B) and acetate (C, D) on selenite (A, C) and selenate (B, D) conversion after 4 weeks of incubation: unreduced selenium oxyanions (gray bar), alkylated selenium species (dimethyl selenide plus dimethyl diselenide) (black bars), and solid selenium species (both suspended and in biomass, white bars).

FIGURE 2. Selenium bioalkylation products using H2/CO2 (A) and acetate (B) as the electron donor: dimethyl selenide (squares) and dimethyl diselenide (tilted squares) formed during an incubation with 10-4 M selenite (weeks 1-4) (open symbols) and selenate (filled symbols). The incubation between weeks 5 and 8 was done in the absence of selenium oxyanions (dashed line). sulfate was added to the batch incubations, endogenous sulfur is present in the inoculum at high amounts (24). The latter leads to the formation of dissolved sulfide (∼10-4 M (25)). As a consequence, the selenite removal efficiencies in sulfur-depleted, anaerobic granular sludges might be lower than the high efficiencies observed here. Clearly, the interaction of sulfate-reducing bacteria and their respiratory end product sulfide with selenium oxyanions needs further investigation to quantify their role in selenium oxyanion removal. 1070

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 45, NO. 3, 2011

4.2. Selenium Solid-Phase Speciation Assessed by XANES Spectroscopy. In this study we demonstrate that anaerobic granular sludge converts water-soluble, toxic selenium oxyanions to insoluble elemental selenium and metal selenides, with the formal oxidation state of the latter (-I/-II) being dependent on the concentration of the selenium oxyanion added in the batch medium. Whereas the speciation in batches incubated with the highest selenium oxyanion concentration is dominated by elemental selenium and selenides related to ferroselite (with a formal oxidation state

FIGURE 3. Normalized Se K-edge XANES spectra (solid lines) and best fits by linear combination (×) for sludges reducing 10-5 to 10-3 M selenite (A, C) and selenate (B, D) with electron donors H2/CO2 (A, B) and acetate (C, D). Misfits are related to unidentified selenium species. of -I), the lower concentrated batches were rather dominated by Se(-II) selenides, i.e., as in achavalite, berzelianite, and stilleite (Table 1). Due to the chemical similarities between selenium and sulfur, it has been hypothesized that achavalite, FeSe, and ferroselite, FeSe2, can be formed in analogy to iron sulfides and pyrite (26). It was proposed that a primary reaction of iron oxyhydroxides and aqueous selenide forms achavalite. This reaction can be followed by a subsequent reaction of achavalite with either elemental selenium (1) or further aqueous selenide (2), both reactions forming ferroselite (formal oxidation numbers given as superscripts): FeSe-II + Se0 f FeSe-I2

(1)

FeSe-II + H2Se-II(aq) f FeSe-I2 + H02(g)

(2)

Elemental selenium was dominant in the selenium speciation for three out of four samples exposed to 10-4 M selenite/selenate. Thus, it seems implausible that reaction 1 explains the exclusive occurrence of ferroselite in 10-3 M samples. The apparent difference in the modeled speciation might thus imply that higher amounts of aqueous selenide were formed in the 10-3 M batches in contrast to the lower concentrated batches. This allows achavalite to further react to form ferroselite according to reaction 2. All incubations received electron donors in excess, allowing, in theory, a complete reduction of oxyanions to aqueous selenide. However, alternative electron-accepting reactions, e.g., methanogenesis and sulfate reduction, might have competed for the available electrons in the 10-4 and 10-5 M batches,

resulting in lower of amounts of aqueous selenide. Consequently, this leads to a different selenium solid speciation in the latter batches. Methanogenesis and sulfate reduction are indeed completely inhibited by 10-3 M concentrations of selenium oxyanions, yet can proceed with reduced activity at the lower concentrations tested here (10, 13). Since ferroselite is the most thermodynamically stable iron selenide (27), selenium is efficiently immobilized within iron-rich, highly reducing environments such as those prevailing for anaerobic granular sludge (14, 15). In other environments, metal and/or aqueous selenide concentrations might be too low to form ferroselite. Rather, it results in the formation of FeSe, as previously observed in selenium-impacted sediments (28). The minor deviations between the modeled and the experimental XANES spectra in some 10-4 and 10-5 M incubations might be due to the presence of alkylated selenium compounds associated with the sludge. Indeed most dissolved alkylated species were observed in these incubations (Figure 2). Alkylation in anaerobic granular sludge can occur from previously accumulated selenium sources (weeks 5-8, Figure 2B) such as selenocysteine (29). Depletion of the previously accumulated selenocysteine pool during the experiments of this study (Figure 2) by alkylation can thus explain the low contribution of selenocysteine to the modeled speciation. The speciation for batches incubated with 10-5 M selenium oxyanions is more delicate to interpret due to the beam induced reduction. However, on the basis of the observation that selenate but not selenite is reduced by radiation (30, 31), it can be carefully assessed that the unaltered speciation in selenite-containing batches was not determined by selenite itself, yet by other unknown species. This is of particular importance, since selenite is more toxic as compared to selenate to, e.g., aquatic invertebrates (1). The fact that the samples undoubtedly appeared red (compare 13) suggests the presence of this modification of elemental selenium, yet the modeled speciation revealed mostly a contribution of gray elemental selenium. Because red elemental selenium is only formed on the outside of the sludge granules, yet the XANES analysis also yields speciation information from the bulk granule, the contribution of significant amounts of gray, elemental, trigonal selenium can be explained. 4.3. Implications for Practice. By combination of different speciation methods, we show that anaerobic granular sludge has a limited applicability to the treatment of highly selenate contaminated waters, e.g., in glass and selenium processing industries (32) or other wastewaters concentrated in selenium (13). This is due, firstly, to the fact that the selenate removal efficiency initially observed at high (10-4 M or higher) selenate concentrations was not sustained during repeated batch incubations. Secondly, high concentrations of selenate are mainly converted to stable metal selenides, which interfere with a recovery of elemental selenium that is worth pursuing. However, anaerobic granular sludge can still be used to treat low selenate concentrations occurring in, e.g., agricultural or mine drainage waters (5), since there it can sustain high removal efficiencies for prolonged times (10, 16). In this study, we furthermore demonstrate that anaerobic granular sludge fed with either H2/CO2 or acetate is a promising inoculum to be applied in the treatment of highly concentrated selenite waters, such as membrane filtration retentates (7) or oil refinery effluents (33), since it can efficiently immobilize selenite into insoluble mineral phases. The fact that selenite is converted to mainly elemental selenium makes the use of this inoculum attractive for applications aiming at the recovery of selenium as a pure element (5). Nevertheless, the application of anaerobic granular sludge to selenite treatment is, however, limited by VOL. 45, NO. 3, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1071

the fact that alkylated selenium species are formed, as demonstrated here. Although, on a relative basis, alkylated selenium species were formed to a minor extent only (Figure 1), a maximum of more than 2000 µg of Se/L was alkylated to dimethyl selenide and dimethyl diselenide. Consequently, dissolved selenium concentrations still have to be considered high regarding bioremediation applications, since the current U.S. maximum contaminant level for drinking water is 50 µg/L (34). Adverse effects on fish can arise even at total dissolved selenium concentrations of 5 µg/L (based on total selenium concentrations) (1). A precise control of the operational conditions (temperature, pH) can efficiently prevent alkylation during treatment (16), yet further measures such as gas stripping have to be applied to lower effluent selenium values sufficiently to achieve total maximum daily loads given by some legislators (35). A simple dilution of these species to the atmosphere in, e.g., post-treatment ponds is disputable, due to the malodorous character of alkylated species in trace concentrations (36) and their largely unknown chronic toxicity. When H2/CO2 was provided as the electron donor in comparison to acetate, alkylation was significantly higher (Figure 2); thus, its use is not recommended in order to limit alkylation. The fact that selenium alkylation continues from selenium sources previously accumulated in the biomass (Figure 2B) should be considered when excess biomass from biotreatment processes is harvested, stored, and disposed.

Acknowledgments This work was supported by the European Union within the Marie Curie Excellence TEAM Grant “Novel biogeological engineering processes for heavy metal removal and recovery” (MEXT-CT-2003-509567). The work was further supported by The Netherlands Organization for Scientific Research (Nederlandse Organisatie voor Wetenschappelijk Onderzoek, NWO), financing the stays at ESRF. The work was also further supported by the Swiss National Science Foundation (Grant Number SNF 200021_126899).

Supporting Information Available Analytical methods applied in this study. This material is available free of charge via the Internet at http://pubs.acs.org.

(10)

(11)

(12)

(13)

(14)

(15)

(16)

(17)

(18)

(19) (20)

(21) (22)

(23)

Literature Cited (1) Hamilton, S. J. Review of selenium toxicity in the aquatic food chain. Sci. Total Environ. 2004, 326 (1-3), 1–31. (2) Yu, R.; Coffman, J. P.; Van Fleet Stalder, V.; Chasteen, T. G. Toxicity of oxyanions of selenium and of a proposed bioremediation intermediate, dimethyl selenone. Environ. Toxicol. Chem. 1997, 16 (2), 140–145. (3) Wu, L. Review of 15 years of research on ecotoxicology and remediation of land contaminated by agricultural drainage sediment rich in selenium. Ecotoxicol. Environ. Saf. 2004, 57 (3), 257–269. (4) Forecasting selenium discharges to the San Francisco Bay-delta estuary: Ecological effects of a proposed San Luis Drain extension. http://pubs.usgs.gov/pp/p1646/pdf/pp1646.pdf. (5) Lenz, M.; Lens, P. N. L. The essential toxin: The changing perception of selenium in environmental sciences. Sci. Total Environ. 2009, 407 (12), 3620–3633. (6) Frankenberger, W. T.; Amrhein, C.; Fan, T. W. M.; Flaschi, D.; Glater, J.; Kartinen, E.; Kovac, K.; Lee, E.; Ohlendorf, H. M.; Owens, L.; Terry, N.; Toto, A. Advanced treatment technologies in the remediation of seleniferous drainage waters and sediments. Irrig. Drain. Syst. 2004, 18 (1), 19–42. (7) Marinas, B. J.; Selleck, R. E. Reverse osmosis treatment of multicomponent electrolyte solutions. J. Membr. Sci. 1992, 72 (3), 211–229. (8) NSMP identification and assessment of selenium and nitrogen treatment technologies and best management practices. http:// www.ocnsmp.com/library.asp. (9) Gao, S.; Tanji, K. K.; Dahlgren, R. A.; Ryu, J.; Herbel, M. J.; Higashi, R. M. Chemical status of selenium in evaporation basins for 1072

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 45, NO. 3, 2011

(24)

(25)

(26)

(27)

(28)

(29)

(30)

(31)

disposal of agricultural drainage. Chemosphere 2007, 69 (4), 585–594. Lenz, M.; van Hullebusch, E. D.; Hommes, G.; Corvini, P. F. X.; Lens, P. N. L. Selenate removal in methanogenic and sulfatereducing upflow anaerobic sludge bed reactors. Water Res. 2008, 42 (8-9), 2184–2194. Astratinei, V.; van Hullebusch, E. D.; Lens, P. N. L. Bioconversion of selenate in methanogenic anaerobic granular sludge. J. Environ. Qual. 2006, 35 (5), 1873–1883. Roest, K.; Heilig, H. G. H. J.; Smidt, H.; de Vos, W. M.; Stams, A. J. M.; Akkermans, A. D. L. Community analysis of a full-scale anaerobic bioreactor treating paper mill wastewater. Syst. Appl. Microbiol. 2005, 28 (2), 175–185. Lenz, M.; Janzen, N.; Lens, P. N. Selenium oxyanion inhibition of hydrogenotrophic and acetoclastic methanogenesis. Chemosphere 2008, 73 (3), 383–8. Zandvoort, M. H.; van Hullebusch, E. D.; Gieteling, J.; Lens, P. N. L. Granular sludge in full-scale anaerobic bioreactors: Trace element content and deficiencies. Enzyme Microb. Technol. 2006, 39 (2), 337–346. Lenz, M.; van Hullebusch, E. D.; Farges, F.; Nikitenko, S.; Borca, C. N.; Grolimund, D.; Lens, P. N. L. Selenium speciation assessed by X-ray absorption spectroscopy of sequentially extracted anaerobic biofilms. Environ. Sci. Technol. 2008, 42 (20), 7587– 7593. Lenz, M.; Smit, M.; Binder, P.; Van Aelst, A. C.; Lens, P. N. L. Biological alkylation and colloid formation of selenium in methanogenic UASB reactors. J. Environ. Qual. 2008, 37 (5), 1691–1700. Lenz, M.; Gmerek, A.; Lens, P. N. L. Selenium speciation in anaerobic granular sludge. Int. J. Environ. Anal. Chem. 2006, 86 (9), 615–627. Stams, A. J. M.; Grolle, K. C. F.; Frijters, C. T. M.; Van Lier, J. B. Enrichment of thermophilic propionate-oxidizing bacteria in syntrophy with Methanobacterium thermoautotrophicum or Methanobacterium thermoformicicum. Appl. Environ. Microbiol. 1992, 58 (1), 346–352. Winterer, M. XAFSsA data analysis program for materials science. J. Phys. IV 1997, 7 (2), C2.243C2.244. Farges, F.; Brown, G. E.; Petit, P.-E.; Munoz, M. Transition elements in water-bearing silicate glasses/melts. Part I. A highresolution and anharmonic analysis of Ni coordination environments in crystals, glasses, and melts. Geochim. Cosmochim. Acta 2001, 65 (10), 1665–1678. XANES dactyloscopesFreeware for windows. http://www.desy. de/∼klmn/xanda.html. Hockin, S.; Gadd, G. M. Removal of selenate from sulfatecontaining media by sulfate-reducing bacterial biofilms. Environ. Microbiol. 2006, 8 (5), 816–826. Hockin, S. L.; Gadd, G. M. Linked redox precipitation of sulfur and selenium under anaerobic conditions by sulfate-reducing bacterial biofilms. Appl. Environ. Microbiol. 2003, 69 (12), 7063– 7072. Osuna, M. B.; Van Hullebusch, E. D.; Zandvoort, M. H.; Iza, J.; Lens, P. N. L. Effect of cobalt sorption on metal fractionation in anaerobic granular sludge. J. Environ. Qual. 2004, 33 (4), 1256–1270. Manconi, I.; van der Maas, P.; Lens, P. N. L. Effect of sulfur compounds on biological reduction of nitric oxide in aqueous Fe(II)EDTA2- solutions. Nitric Oxide 2006, 15 (1), 40–49. Belzile, N.; Chen, Y. W.; Xu, R. Early diagenetic behaviour of selenium in freshwater sediments. Appl. Geochem. 2000, 15 (10), 1439–1454. Hatten Howard, J. Geochemistry of selenium: Formation of ferroselite and selenium behavior in the vicinity of oxidizing sulfide and uranium deposits. Geochim. Cosmochim. Acta 1977, 41 (11), 1665–1678. Herbel, M. J.; Blum, J. S.; Oremland, R. S.; Borglin, S. E. Reduction of elemental selenium to selenide: Experiments with anoxic sediments and bacteria that respire Se-oxyanions. Geomicrobiol. J. 2003, 20 (6), 587–602. Chasteen, T. G.; Bentley, R. Biomethylation of selenium and tellurium: Microorganisms and plants. Chem. Rev. 2003, 103 (1), 1–25. Ryser, A. L.; Strawn, D. G.; Marcus, M. A.; Fakra, S.; JohnsonMaynard, J. L.; Moller, G. Microscopically focused synchrotron X-ray investigation of selenium speciation in soils developing on reclaimed mine lands. Environ. Sci. Technol. 2006, 40 (2), 462–467. Pearce, C. I.; Coker, V. S.; Charnock, J. M.; Pattrick, R. A. D.; Mosselmans, J. F. W.; Law, N.; Beveridge, T. J.; Lloyd, J. R.

Microbial manufacture of chalcogenide-based nanoparticles via the reduction of selenite using Veillonella atypica: An in situ EXAFS study. Nanotechnology 2008, (15), 155603. (32) Fujita, M.; Ike, M.; Kashiwa, M.; Hashimoto, R.; Soda, S. Laboratory-scale continuous reactor for soluble selenium removal using selenate-reducing bacterium, Bacillus sp SF-1. Biotechnol. Bioeng. 2002, 80 (7), 755–761. (33) Lawson, S.; Macy, J. M. Bioremediation of selenite in oil refinery wastewater. Appl. Microbiol. Biotechnol. 1995, 43 (4), 762765.

(34) Basic information about selenium in drinking water. http:// water.epa.gov/drink/contaminants/basicinformation/selenium. cfm. (35) Lemly, A. A procedure for NEPA assessment of selenium hazards associated with mining. Environ. Monit. Assess. 2007, 125 (1), 361–375. (36) Schulz, S. S.; Dickschat, J. S. Bacterial volatiles: The smell of small organisms. Nat. Prod. Rep. 2007, 24 (4), 814–842.

ES1022619

VOL. 45, NO. 3, 2011 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

1073