In-situ Cr(VI) reduction with electrogenerated hydrogen peroxide driven by iron-reducing bacteria

Bioresource Technology 102 (2011) 2468–2473

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In-situ Cr(VI) reduction with electrogenerated hydrogen peroxide driven by iron-reducing bacteria Liang Liu a,b,d, Yong Yuan a, Fang-bai Li a,⇑, Chun-hua Feng c a

Guangdong Key Laboratory of Agricultural Environment Pollution Integrated Control, Guangdong Institute of Eco-Environmental and Soil Sciences, Guangzhou 510650, China Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China c School of Chemistry and Chemical Engineering, South China University of Technology, Guangzhou 510640, China d Graduate University of Chinese Academy of Sciences, Beijing 100039, China b

a r t i c l e

i n f o

Article history: Received 2 September 2010 Received in revised form 1 November 2010 Accepted 3 November 2010 Available online 12 November 2010 Keywords: Cr(VI) reduction Electrogenerated hydrogen peroxide Iron-reducing bacteria Microbial fuel cell

a b s t r a c t Cr(VI) was reduced in-situ at a carbon felt cathode in an air–cathode dual-chamber microbial fuel cell (MFC). The reduction of Cr(VI) was proven to be strongly associated with the electrogenerated H2O2 at the cathode driven by iron-reducing bacteria. At pH 2.0, only 42.5% of Cr(VI) was reduced after 12 h in the nitrogen-bubbling-cathode MFC, while complete reduction of Cr(VI) was achieved in 4 h in the airbubbling-cathode MFC in which the reduction of oxygen to H2O2 was confirmed. Conditions that affected the efficiency of the reduction of Cr(VI) were evaluated experimentally, including the cathodic electrolyte pH, the type of iron-reducing species, and the addition of redox mediators. The results showed that the efficient reduction of Cr(VI) could be achieved with an air-bubbling-cathode MFC. Ó 2010 Elsevier Ltd. All rights reserved.

1. Introduction Hexavalent chromium (Cr(VI)) contamination is a serious environmental concern due to its high toxicity and corrosiveness (Dupont and Guillon, 2003; Rodriguez et al., 2005). Therefore, it is necessary to remove the Cr(VI) that is abundant in the wastewaters of many industries (Park et al., 2008) such as electroplating, leather tanning, textile dyeing, metallurgy and wood preservation. The commonly used method to treat these wastewaters is chemical reduction of Cr(VI) to the less toxic Cr(III). This method is easy to implement but has disadvantages such as the requirement for a continuous feed of reducing reagents (FeSO4, NaHSO3 or FeCl2) and the production of considerable amounts of sludge (Singh et al., 2009; Erdem and Tumen, 2004; Schlautman and Han, 2001). Using H2O2 as the reductant is a much cleaner process because H2O2 is oxidized to oxygen (Reaction (1)) without the need for further recycling (van Niekerk et al., 2007; Pettine et al., 2002).

2HCrO4 þ 3H2 O2 þ 8Hþ ! 2Cr3þ þ 3O2 þ 8H2 O However, at the industrial level, the storage and transportation of H2O2 is inconvenient and expensive, especially for large quantities. It would be attractive if H2O2 were able to be generated in-situ and immediately used for Cr(VI)-contaminated wastewater ⇑ Corresponding author. Tel.: +86 20 87024721; fax: +86 20 87024123. E-mail address: [email protected] (F.-b. Li). 0960-8524/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2010.11.013

treatment. With this in mind, we attempted to manufacture H2O2 with a bioelectrochemical system (BES). A microbial fuel cell (MFC), which allows the recovery of bioenergy from organic wastes (Rozendal et al., 2008) with the aid of microorganisms, was used. This technology enables in-situ H2O2 generation without the need for any energy input. Briefly, in the anode compartment, oxidation of organic electron donors can occur in the presence of electrochemically active microorganisms which transfer the electrons generated to the solid anode. The electrons are then transported through an external circuit to the cathode compartment where air/O2 (electron acceptor) is available and H2O2 is electrochemically generated via the two-electron reaction of O2 reduction (Reaction 2).

O2 þ 2Hþ þ 2e ! 2H2 O2 Recently, several studies (Zhu and Ni, 2009; Rozendal et al., 2009) have demonstrated this concept of using an MFC to achieve cathodic production of H2O2 on the surfaces of carbon materials. This process may have important industrial applications. For example, some reports (Zhu and Ni, 2009; Feng et al., 2010; Zhuang et al., 2010) have shown the utilization of H2O2 produced in such a BES as a Fenton reagent (H2O2 and Fe2+) for the production of hydroxyl radicals, which are strong oxidants of organic pollutants in wastewaters. This study provides the first attempt to reduce Cr(VI) using H2O2 that is directly generated in the MFC cathode compartment.

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Because Cr(VI) can also function as the electron acceptor, as evidenced from previous MFC studies concerning Cr(VI) removal through either electrochemical (Li et al., 2008, 2009b; Wang et al., 2008) or bioelectrochemical methods (Tandukar et al., 2009), it is of interest to us to know whether the indirect Cr(VI) reduction proposed here exhibits a higher reaction rate than direct Cr(VI) reduction in the cathode compartment. Moreover, this study examines the impacts of different operational parameters on the accumulation of H2O2 that is considered to play a key role in Cr(VI) reduction. The factors investigated include pH of catholyte, types of bacteria and use of an external electron mediator.

2. Methods 2.1. Microorganisms and medium in the anode chamber Two pure cultures Shewanella decolorationis S12, Klebsiella pneumoniae (K. pneumoniae) L17 and one mixed culture were used as anodic inoculums. Culture of S. decolorationis S12 (Xu et al., 2005) was provided by the Guangdong Key Laboratory of Microbial Culture Collection and Application, Guangzhou, China. K. pneumoniae L17 was isolated from subterranean forest sediment by our group (Li et al., 2009a). The mixed culture was inoculated from an anaerobic activated sludge collected from Leide wastewater plant located in Guangzhou, China. Before being transferred to the MFC reactor, the frozen bacteria (1 mL) suspended in 100 mL of medium (10.0 g L1 peptone, 5.0 g L1 beef extract and 5.0 g L1 NaCl, pH = 7.0) were allowed to grow overnight (18 h) at 30 °C on an orbital shaker incubator at 150 rpm. Glucose (3 g L1) used as the energy source was added to the anode chamber and was anaerobically oxidized by the microorganism. The microbial growth medium (pH 7.0) in the anode chamber contained: 5.84 g L1 NaCl, 0.10 g L1 KCl, 0.25 g L1 NH4Cl, 12.00 g L1 Na2HPO412H2O, 2.57 g L1 NaH2PO42H2O, 10 mL vitamin solution and 10 mL mineral solution. The required vitamin and mineral solutions were prepared as previously described (Lovley and Phillips, 1988). Prior to use, the above medium was sterilized by autoclaving at 121 °C for 20 min.

2.2. MFC construction and operation The MFCs consisted of two identical chambers separated by a cation exchange membrane (ESC-7000, Electrolytica Corporation). Each cell chamber had an effective volume of 85 mL. Both electrodes were made of carbon felt (4.5  4.5 cm each, Panex 33 160 K, Zoltek) and Ti wire was inserted inside the carbon felt to connect the circuit. The electrode spacing was 2 cm. The cation exchange membrane was cleaned by boiling in H2O2 (3% V/V) solution and then soaking in deionized water for a day. To operate the MFC, the microorganism growth medium containing glucose (10% v/v; medium/anode reactor value) was added to the anode chamber and the catholyte containing K2CrO4 (initial Cr(VI) concentration of 10 mg/L) was added to the cathode chamber. The catholyte was continuously purged with N2 (90 ml/min) or air (90 ml/min) in different experimental arrays. To assess the impact of pH on the reduction rate of Cr(VI), precise control of the catholyte pH was achieved by manipulating the composition of H3PO4, NaH2PO4, and Na2HPO4 used. Open circuit experiments were conducted as control experiments. The purpose of these control experiments was to confirm that the reduction of Cr(VI) was not due to adsorption onto the electrode. All MFCs were operated in triplicate at a controlled temperature of 30 ± 1 °C in a constant temperature incubator (HPG-280H, China) for the entire experiment. Unless otherwise stated, a 500 X resistor was used as the external load for the MFC.

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2.3. Calculations and analyses To quantify the cell performance, the resulting voltage (V) throughout the experiments was recorded every 2 min using a data acquisition system (AD 8223 type voltage collector with 16 channels, Rui Bo Hua Technology Control Corporation of Beijing, China) with a PC. The current density (I) and power density (P) normalized to the projected surface area of the cathode were calculated according to I = V R1 and P = V2 R1, respectively, where R is the external resistance. A polarization curve was obtained by adjusting the external resistor from 20 to 50,000 X. At each fixed resistance, the voltage was measured after 10 min, when a pseudo-steady state was approached (Logan et al., 2006). The power densities were normalized to the projected cathode surface area. A saturated calomel electrode (SCE, +0.241 V vs. standard hydrogen electrode; SHE) was used as the reference electrode. Columbic efficiency (CE) was calculated as previously described by Huang et al. (2008). At each scheduled sampling interval, a sample (1.5 ml) was withdrawn from the cathode chamber for Cr(VI) analysis. The concentrations of Cr(VI) were determined via a colorimetric method using 1,5-diphenylcarbazide in acidic solution (Clesceri et al., 1998). The concentration of hydrogen peroxide (H2O2) was determined using a H2O2 colorimeter (LOVIBOND-ET8600, Germany) at 528 nm. For the determination of H2O2, separate experiments with the same reaction conditions were conducted (without Cr(VI)). At each time interval, 10 mL of reaction solution was sampled and immediately filtered through a 0.45 lm filter, followed at once by measurement of the concentration of H2O2 in the filtrate. All the experiments were carried out in triplicate and only the mean values were reported.

3. Results and discussion 3.1. Simultaneous Cr(VI) reduction and hydrogen peroxide generation Fig. 1a shows residual Cr(VI) (normalized to the initial concentration) as a function of time at pH 2.0 under various conditions with S12 as the anodic inoculum. The removal rate of Cr(VI) with the air-purged cathode in the MFC was substantially greater than that with the nitrogen purged one. The Cr(VI) was almost completely removed after 3.5 h with the air-bubbling-cathode, while only 42.5% of Cr(VI) was reduced to Cr(III) with the nitrogenpurged cathode after 12 h. Previous reports have documented the successful reduction process of Cr(VI) at the deoxygenated cathode of an MFC via either an electrochemical (Li et al., 2008, 2009b; Wang et al., 2008) or bioelectrochemical (Tandukar et al., 2009) method. A slow decrease of Cr(VI) was also found in our case when the cathode of the MFC was purged with nitrogen gas. However, the slope of the kinetic curve increased markedly when air purging was applied, indicating the enhancement of Cr(VI) reduction. The role of H2O2 in the reduction of Cr(VI) was confirmed by adding H2O2 to the nitrogen-purged cathode. As shown in Fig. 1b, Cr(VI) was only slightly reduced under the nitrogen purged condition, whereas the reduction was obviously accelerated by adding H2O2, demonstrating that the removal of Cr(VI) was primarily due to H2O2. In such a system, the formation of H2O2 was thermodynamically favored due to the lack of an efficient oxygen reduction catalyst (Rozendal et al., 2009) and the reduction of Cr(VI) by H2O2 was also thermodynamically favorable in the view of their standard electrode potentials that were +0.56 V vs. SHE for H2O2 oxidation and +1.08 V vs. SHE for the Cr(VI) reduction at pH 2.0, respectively (van Niekerk et al., 2007; Kotas´ and Stasicka, 2000). The removal efficiency of Cr(VI) was in accordance with

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(a)

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the power generation of the MFCs as shown in Fig. 2. The maximum power density of 52.1 mW/cm2 obtained from the MFC with the air-bubbling-cathode was much higher than that of 6.8 mW/ cm2 from the MFC with the nitrogen-bubbling-cathode (Fig. 2a). The difference in the removal efficiency of Cr(VI) and power densities between two cases can be essentially attributed to the different reactions involved at the cathodes. As shown in Fig. 2b, the anode potentials of the two MFCs are almost consistent while the cathode potentials vary. The cathode potential under air-bubbling was significantly greater over the entire current range. In the case of the nitrogen-purged cathode, the slow removal efficiency of Cr(VI) and low power density indicated that Cr(VI) was not an efficient electron acceptor at this cathode. However, the reduction of Cr(VI) could be accelerated and the power output could be enhanced when air purging was applied at the cathode. In this case, both O2 and Cr(VI) can react with the electrons produced at the anode, which results in a higher energy output. Moreover, the twoelectron reduction of O2 resulted in the formation of H2O2 which could be an efficient chemical reductant to further react with Cr(VI). The coulombic efficiencies (CE) of the S12 inoculated MFC was 8.3 ± 0.7% with the air-bubbling-cathode at pH 2.0. The efficiency of the current at ultimately reducing Cr(VI) was calculated to be 70.3 ± 1.3%. The Cr(VI) reduction rate was 2.78 g Cr(VI)/ m3 h in the air-bubbling-cathode at pH 2.0. Li et al. (2009b) reported a Cr(VI) reduction rate of 0.97 g/m3 h at rutile-catalyzed cathodes and Wang et al. (2008) reported a reduction rate of 0.5 g/m3 h at nitrogen-purged cathodes based on the direct electrochemical reduction in microbial fuel cells. The in-situ generation of H2O2 in the cathode compartment was confirmed by measuring its

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Current density ( mA m ) Fig. 2. Power densities (a) and individual electrode potentials (b) vs. current density curves for nitrogen-purged and air-purged cathodes (pH 2.0). Anodic inoculum: S12.

concentration over time. The measurement was conducted during a separate experiment without Cr(VI) because oxidizing agents interfere with the spectrophotometric detection of H2O2. As revealed in Fig. 3, when O2 was expelled from the catholyte, no H2O2 was detected. However, the presence of dissolved O2 in the cathode led to the formation of H2O2. The H2O2 concentration was negligible before the MFC was initiated and rapidly increased with time to a relatively stable concentration of 1.38 mg/L. This is

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Conc. of H2O2 (mg/L)

Fig. 1. Cr(VI) reduction as a function of time under open circuit and closed circuit (nitrogen-purged and air-purged cathode) conditions at a catholyte pH of 2.0 (a) and effect of H2O2 addition on Cr(VI) reduction in nitrogen-purged cathode (b). Adding 0.15 ml H2O2 (100 mg/L) every min. Anodic inoculum: S12.

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Time (h) Fig. 3. Concentration of electrogenerated H2O2 at the cathodes with nitrogen or airpurging (pH 2.0). Anodic inoculum: S12.

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consistent with other observations in a traditional electrochemical cell (Brillas and Casado, 2002), where a constant concentration was maintained because the rate of H2O2 generation was equal to the rate of H2O2 decomposition. 3.2. Enhancing Cr(VI) reduction with controlled anodic strains and electron shuttle Because the reduction of Cr(VI) took place at the cathode of the MFC by accepting the electrons transferred from the anode, the anodic biocatalysts can obviously affect the reaction rate of Cr(VI) reduction. Fig. 4a shows the effect of varying the inoculum (L17,

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S12 or anaerobic activated sludge) in the anodic compartment on the reduction of Cr(VI). The MFC inoculated with anaerobic activated sludge had the best performance, reducing 97% of Cr(VI) within 3 h, while the L17 and S12 inoculated MFCs required longer times to achieve this reduction. The electron transfer from the microbial cell to the fuel cell anode, a process that links microbiology and electrochemistry, represents a key factor defining the theoretical limits of the energy conversion (Schröder, 2007). Subsequently, the efficiency of microbial energy conversion influences the cathodic reduction reactions because the electrons involved in the reduction reactions are produced by the microbial oxidation of organics at the anode. In other words, the cathodic reactions in MFCs are actually driven by the electrochemically active microorganisms of the anode. Iron-reducing strains are presently the most common microorganisms used in MFCs to directly produce electricity. However, the efficiency of electron production and transfer towards the anode varies amongst different species. For this reason we examined the efficiency of Cr(VI) reduction with different iron-reducing species at the anodes. From our results for Cr(VI) reduction, the anaerobic activated sludge was a better inoculum for this purpose than the other two pure cultures – this is also in agreement with energy generation capability of MFCs reported in the literature (Rabaey et al., 2004; Rabaey et al., 2005). In addition, the rate of Cr(VI) reduction could be enhanced by adding electron shuttles to the anode chamber (Fig. 4b). The rate of Cr(VI) reduction was significantly increased when anthraquinone-2,6disulfonate (AQDS), a known electron transfer mediator, was added to the anode chamber, lowering the time for 97% Cr(VI) reduction to less than 2 h. Previous studies showed that the electron transfer between iron-reducing bacteria and an extracellular electron acceptor could be significantly accelerated in the presence of electron shuttles (Watanabe et al., 2009; Thygesen et al., 2009). For example, the addition of AQDS increased current production in MFCs by 24% (Bond et al., 2002). The addition of AQDS to the anode of the MFC also led to an increased rate of Cr(VI) reduction at the cathode. As mentioned above, the Cr(VI) was mainly reduced by the H2O2 produced in-situ in the MFCs. Varying the anodic biocatalysts and the addition of AQDS, results in variation in the amount of H2O2 produced in-situ, as shown in Fig. 4c. The activated sludge inoculated MFC produced the highest concentration of H2O2 of the three inoculums. When AQDS was added to the anode compartment, the concentration of H2O2 was as high as 2.0 mg/L, almost 1.5 times that in the absence of AQDS. Obviously, the higher amount of H2O2 produced, the faster the rate of Cr(VI) reduction achieved. This demonstrates that an optimum anode is important for the reduction of Cr(VI) in this bioelectrochemical system. 3.3. Dependence of Cr(VI) reduction on catholyte pH

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According to the Cr-Pourbaix diagram (Pourbaix, 1974), the reduction of Cr(VI) to Cr(III) is thermodynamically favored under acidic conditions due to an increase of its standard potential with proton ion concentration (Rodriguez et al., 2005). The effect of pH on the kinetics of Cr(VI) reduction at the cathode is shown in Fig. 5a. The pH has a strong influence on the Cr(VI) reduction rate in the range of pH 2.0–4.0. For example, at pH 2.0, Cr(VI) was completely reduced in 3.5 h in the air-bubbling-cathode MFC, while only 9.0% of Cr(VI) was reduced at pH 7.0 after 6 h. In addition, as shown in Eq. (1), seven H+ ions were consumed by the reduction of each mole of Cr(VI). This reaction was thus strongly pH dependent, i.e. lower pH might make the reaction more favorable. Moreover, the electrogeneration of hydrogen peroxide driven by iron-reducing bacteria is also strongly dependent on the pH of the catholyte. As depicted in Fig. 5b, at low pH the production of H2O2 was obviously favored. As the pH increased, the concentration of

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H2O2 continuously decreased. The concentration of H2O2 produced in-situ was up to 1.38 mg/L at pH 2.0, a factor of 23 times higher than the 0.06 mg/L at pH 7.0. In summary, acidic conditions in the catholyte benefited both the electrogeneration of H2O2 and the reduction reaction of Cr(VI), resulting in the fast removal rate of Cr(VI).

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We have demonstrated the concept of utilizing Cr(VI) as the electron acceptor for anaerobic respiration in MFC technology. The electrons donated through the respiration of an iron-reducing microorganism can be successfully transferred to Cr(VI), leading to the reduction of Cr(VI). Fig. 6a describes the mechanism of electron transfer for the reduction of Cr(VI). In such an MFC, there are three types of reactions available in the process for electron production, transfer and consumption – bioelectrochemical, electrochemical and chemical reactions. The bioelectrochemical reactions occurred in the anode chamber, where the electrons were produced during microbial metabolism. Subsequently, the electrons collected in the anode pass through an external load and arrive at the cathode chamber where the electrochemical reactions happen. The electrochemical reactions include the electrochemical reduction of dissolved oxygen to H2O or H2O2 and direct electrochemical reduction of Cr(VI). The chemical reaction that is the reduction of Cr(VI) by electrogenerated H2O2 also occurs in the cathode compartment. Thus, the actual reduction of Cr(VI) was achieved by two different pathways: direct electrochemical reduction at the cathode and indirect chemical reduction through the in-situ generated hydrogen peroxide as shown in Fig. 6b. As mentioned above, the fact that the reduction rate of Cr(VI) with the air-bubbling-cathode MFC was much faster than that with the nitrogen-bubbling-cathode MFC indicates that the reduction of Cr(VI) by the in-situ generated hydrogen peroxide is more favorable than the direct electrochemical reduction. Furthermore, under both pathways, the reduction of

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Fig. 6. Possible electron transfer pathways for the reduction of Cr(VI) (a) and the reactions involved at both anode and cathode (b).

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Cr(VI) could apparently be accelerated by adding extracellular mediators, such as AQDS, into the anode of the MFC. This increase is largely as a result of an increase in the electron transfer rate between iron-reducing microorganism and electrode in the presence of AQDS. In such an MFC, the oxidized AQDS is first reduced by electrons from microorganisms, and then reoxidized at the electrode to convey the electrons. Subsequently, the electrons were transferred to the cathode via the external circuit and Cr(VI) directly or indirectly accepted the electrons to be reduced to Cr(III). Since the iron-reducing microorganism is capable of recovering electrons directly from various wastes, the MFC is expected to be capable of treating two wastewaters at the same time, in which the iron-reducing microorganisms break down the organics in wastewaters and the cathode reduces Cr(VI) to Cr(III). Meanwhile, the MFC technique might also be expected to treat other contaminants that could react with H2O2 to decrease their toxicity. 4. Conclusions In this study, a significant acceleration of Cr(VI) reduction was observed when the catholyte was purged with air rather than nitrogen in an dual-chamber MFC. By monitoring the accumulation and consumption of H2O2 at the cathode, it was suggested that Cr(VI) was mostly reduced to the less toxic Cr(III) by electrogenerated H2O2 at the carbon felt cathode of the MFC. The efficiency of Cr(VI) reduction was strongly related to the catholyte pH, the anodic iron-reducing species, and the addition of extracellular mediators. This study demonstrated that the MFC technology with an aerated cathode was promising for Cr(VI)-contaminated wastewater treatment. Acknowledgements The authors appreciate the financial support of the National Science Foundation of China (No. 40771105) and the Guangdong Innovative Technique Foundation (No. 2006A36703003, 2007B080401019 and 2008A080401008). References Bond, D.R., Holmes, D.E., Tender, L.M., Lovley, D.R., 2002. Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483– 485. Brillas, E., Casado, J., 2002. Aniline degradation by Electro-FentonÒ and peroxicoagulation processes using a flow reactor for wastewater treatment. Chemosphere 47, 241–248. Clesceri, L.S., Greenberg, A.E., Eaton, A.D., 1998. Standard Methods for the Examination of Water and Wastewaters, 20th ed. American Public Health Association, Washington, DC. Dupont, L., Guillon, E., 2003. Removal of hexavalent chromium with a lignocellulosic substrate extracted from wheat bran. Environ. Sci. Technol. 37, 4235–4241. Erdem, M., Tumen, F., 2004. Chromium removal from aqueous solution by the ferrite process. J. Hazard. Mater. B109, 71–77. Feng, C.H., Li, F.B., Mai, H.J., Li, X.Z., 2010. Bio-electro-fenton process driven by microbial fuel cell for wastewater treatment. Environ. Sci. Technol. 44, 1875– 1880. Huang, L.P., Zeng, R.J., Angelidaki, I., 2008. Electricity production from xylose using a mediator-less microbial fuel cell. Bioresour. Technol. 99, 4178–4184.

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