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Improved Hydrogen Production in the Microbial Electrolysis Cell by Inhibiting Methanogenesis Using Ultraviolet Irradiation Yanping Hou, Haiping Luo,* Guangli Liu,* Renduo Zhang, Jiayi Li, and Shiyu Fu Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou 510275, China ABSTRACT: Methanogenesis inhibition is essential for the improvement of hydrogen (H2) yield and energy recovery in the microbial electrolysis cell (MEC). In this study, ultraviolet (UV) irradiation was proposed as an efficient method for methanogenesis control in a single chamber MEC. With 30 cycles of operation with UV irradiation in the MEC, high H2 concentrations (>91%) were maintained, while without UV irradiation, CH4 concentrations increased significantly and reached up to 94%. In the MEC, H2 yields ranged from 2.87 ± 0.03 to 3.70 ± 0.11 mol H2/mol acetate with UV irradiation and from 3.78 ± 0.12 to 0.03 ± 0.004 mol H2/mol acetate without UV irradiation. Average energy efficiencies from the UVirradiated MEC were 1.5 times of those without UV irradiation. Energy production from the MEC without UV irradiation was a negative energy yield process because of large amount of CH4 produced over time, which was mainly attributable to cathodic hydrogenotrophic methanogenesis. Our results clearly showed that UV irradiation could effectively inhibit methanogenesis and improve MEC performance to produce H2.

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INTRODUCTION Compared to the conventional fermentative hydrogen (H2) production methods, the microbial electrolysis cell (MEC) has attracted considerable attention over the past several years as a promising technology for higher H2 yield from organic matter.1,2 The MEC has shown advantages of efficient biomass conversion to biohydrogen gas and high Coulombic efficiencies (CE).3,4 However, methane (CH4) production is commonly observed in the MEC fed with acetate or other complex substrates, such as glucose and organic wastewater.5−8 After a period of operation, biogas production is dominated by CH4 instead of H2 in the membrane-less MEC. Rader and Logan showed that only CH4 gas was produced after running for 17 days in the multielectrode continuous flow MEC fed with acetate.9 Cusick et al. demonstrated that 86% of the produced gas was CH4 in a pilot-scale continuous flow MEC fed with winery wasterwater after 40 days operation.10 Methane production is one of the most critical causes of low H2 yield in the MEC.11 Moreover, CH4 has lower energy and economic values per unit of mass than H2, resulting in a negative energy balance in methanogenic MECs.1,12 Therefore, methanogenesis inhibition is essential to improve H2 yield and energy recovery in the MEC. To enhance H2 production, several approaches have been developed to inhibit methanogenesis in the MEC, such as intermittently exposing electrodes to air,6 heat shocking or lowering pH,13 reducing hydraulic retention time (HRT),14 operating at low temperature (4−9 °C),11 eliminating bicarbonate from the medium,15 using methanogen inhibitors such as 2-bromoethanesulfonate (BES),5 and controling the anode potential.16 However, most of these methods are ineffective in terms of long-term performance and even caused © 2014 American Chemical Society

other problems. For example, the method to expose electrodes to air cannot effectively control methanogens.9 Reduction of HRT may reduce hydraulic loading and COD removal. The approach to use chemical inhibitors is expensive and toxic for field applications.11 Therefore, more effective and practical methods should be developed to inhibit methanogenesis in the MEC. In a single-chamber MEC, CH4 may be generated by methanogenesis in the solution, on the electrodes or the wall of the reactor. As the solution is replaced after each batch cycle, only methanogenesis on the electrodes or the wall of the reactor is responsible for CH4 production.14 The effect of biofilm on the reactor wall can be negligible due to low surface area and affinitiy for bateria on the wall. Thus, the CH4 production should be mainly from the methanogenesis on the anode or cathode in the MEC. Lee et al. demonstrated that the acetoclastic methanogens were inferior to the exoelectrogens to grow in the anode biofilm of acetate-fed MEC.17 Hence, anodic methanogenesis is not the main source of CH4 production in the MEC. Cheng et al. revealed that CH4 production increased considerably when the cathode potential was set lower than −0.8 V (vs Ag/AgCl) in the MEC with methanogenic biocathode.18 Since methanogens have higher metabolic activity on the cathode with lower potential, the cathode with more negative potential as compared with the anode should be a desired place for methanogen growth. Received: Revised: Accepted: Published: 10482

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Itech, China). The positive lead of the power source was connected to the anode. A resistor (10 Ω) was connected between the cathode and the negative lead of the power source. Voltage across the resistor was measured using a multimeter data acquisition system (model 2700, Keithley Instruments, Inc., Cleveland, OH) to calculate the current density. The MECs were operated in fed batch mode in duplicate. When reproducible maximum voltages across the resistor (80−90 mV) were obtained for at least three batch cycles, the anodes were considered fully acclimated. Before each cycle of operation, the reactor medium was sparged with pure N2 gas for 15 min. The medium was refreshed when the current decreased to 80%). The schematic diagram of the MEC reactor is shown in Figure 1. Each reactor

Figure 1. Schematic diagram of an MEC with UV irradiation.

was with outer diameter of 5.5 cm, height of 10 cm, and a working volume of 130 mL. The graphite brush anode was composed of 24 bunches of graphite fiber (12 K, Xinka Carbon Industries CO., LTD, Shanghai, China), each of which was with 40 mm length, and about 40 ± 5 mg. The anode was heated in a muffle furnace at 450 °C for 30 min and then placed on the bottom of reactor. The cathode was made of carbon cloth (woven fabric, Toray Industries, Inc. Japan) with a projected surface area of 7 cm2.14 After coating the Pt catalyst (0.5 mg/ cm2), the weight of the cathode was 280 ± 25 mg. The cathode was placed in the upper part of reactor (Figure 1). Average distance between the anode and the cathode was about 4 cm.6 Rubber stopper was placed firmly on the bottle-type reactor and sealed with epoxy resin. A sampling bag (0.15 L capacity, Shanghai ELOR Co., Ltd., China) was attached on the top of reactor to collect biogas. In total, four reactors were prepared for the experiments. Enrichment and Operation. The MECs were inoculated with a 50:50 mixture of primary clarifier overflow (from Liede Wastewater Treatment Plant, Guangzhou) and a sodium acetate medium. The medium contained (per liter): CH3COONa 1 g, Na2HPO4 4.58 g, NaH2PO4· H2O 2.45 g, NH4Cl 0.31 g, KCl 0.13 g, trace metals solution 12.5 mL, and vitamin solution 12.5 mL.22 A constant voltage of 0.8 V was applied to the circuit using the DC power source (IT6720, 10483

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immersion oil. Bacteria were counted using an epifluorescence microscope (DM5000B, Leica, Germany) with 1000-fold magnification. At least 40 randomly selected fields (114 × 85.8 μm2) were counted per slide. Biomass was evaluated on the basis of protein concentration and measured at the end of the second stage using the Coomassie Brilliant Blue method.24 To analyze the cathodic biofilm community, DNA extraction and quantitative real-time PCR targeting the 16S rRNA genes for acetoclastic methanogens (Methanosaetaceae and Methanosarcinaceae) and hydrogenotrophic methanogens (Methanomicrobiales and methanobacteriales) were performed following the methods of Lee et al.17 The quantitative PCR experiment was conducted in reactors running for 30 days. Calculations. The performance of the MECs was evaluated in terms of volumetric current density (IV, A/m3), CE (%), H2 yield (YH2, mol H2/mol acetate), and the energy efficiency (%).2,9 The volumetric current density was an average of the current production in the steady stage divided by the liquid volume. The CE was calculated as follows:

CE = 100%C P/C T

Figure 2. Biogas (H2, CO2 and CH4) concentrations of MECs in the four stages. The four stages were separated with the dash lines: stage 1: from cycles 1 to 10, stage 2: from cycles 11 to 35, stage 3: from cycles 36 to 39, and stage 4: from cycles 40 to 45. Solid arrows indicate the starting points for UV irradiation and the dash arrow indicates the replacement of the cathodes and chambers.

(1)

Here Cp is the total coulombs calculated by integrating the current over time and CT is the theoretical amount of coulombs and calculated by

C T = Fbsv /M

trations began to decrease and more CH4 was detected in the MECs with the increase of running cycles. From cycle 6 (day 12) to cycle 10 (day 20), H2 concentrations decreased from 93 ± 2.6% to 70 ± 9.2%, while CH4 concentrations increased from 5.5 ± 2.4% to 30 ± 5.4%. To examine the effect of using UV irradiation on methanogenesis inhibition, the second stage experiment (from cycles 11 to 35, days 24 to 74) was conducted. In the group with UV irradiation, high percentages of H2 (>95%) were maintained in the MECs from cycles 12 to 22 (days 25 to 48), and negligible CH4 was detected ( 100% indicated that H2 might recycle between the anode and cathode.9,24 Hydrogen oxidized by exoelectrogens on the anode can contribute to current generation in MEC system. It has been shown that H2 recycle accounted for 62%−76% of observed current density, resulting in observed CEs of 190%−310%.25 In stage 4, after replacing the cathodes, CEs increased slightly compared to those at the end of stage 2. Similar to current densities, CEs between the MECs with and without UV irradiation were not obviously different because of similar current generations and stable COD removals (data not shown) for all the MECs. Energy Efficiency. Energy efficiencies relative to the electrical input and overall energy efficiencies based on both electrical and substrate inputs are shown in Figure 5. In stage 1,

Figure 3. Hydrogen yield of MECs throughout the experiment. Solid arrows indicate the starting points for UV irradiation of the reactors without UV irradiation and the dash arrow indicates the replacement of the cathodes.

H2/mol acetate. In stage 2, H2 yields from the UV irradiated MECs ranged from 2.87 ± 0.03 to 3.70 ± 0.11 mol H2/mol acetate, whereas H2 yields from the MECs without UV irradiation decreased gradually from 2.25 ± 0.09 to 0.03 ± 0.004 mol H2/mol acetate. In stage 4, H2 yields increased sharply to a high level after replacing the cathodes. However, H2 yields from the MECs without UV irradiation dropped dramatically from 3.74 ± 0.14 to 0.60 ± 0.03 mol H2/mol acetate from cycles 40 to 45 (days 85 to 95). The H2 yield from the UV-irradiated MECs remained stable, ranging from 3.24 ± 0.10 to 3.76 ± 0.15 mol H2/mol acetate. Current Generation and Coulombic Efficiency. Current densities and CEs from the MECs in the four stages are shown in Figure 4. Current densities from the MECs with and without UV irradiation were similar, indicating that the UV irradiation did not affect the activities of exoelectrogens significantly. Current generation at the steady state (∼25 h) reached 8−9 mA, and the cycle time was also similar (∼48 h, data not

Figure 5. Energy efficiency (ηE) relative to electrical input and overall energy recovery (ηE+S) based on both electrical and substrate input. Squares and circles represent results of the MECs without and with UV irradiation.

the energy efficiencies relative to electrical inputs varied from 111 ± 7.2% to 148 ± 5.4%, while overall energy efficiencies ranged from 56 ± 6.0% to 68 ± 3.5%. In stage 2, there were greater differences in energy recoveries between the MECs with and without UV irradiation. Both energy efficiencies and overall energy efficiencies achieved in the MECs with UV irradiation were higher than those in MECs without UV irradiation, especially in the period of cycles 25−35 (days 54−74) (Figure 5). More specifically, energy efficiencies from UV irradiated

Figure 4. Volumetric current densities and Coulombic efficiencies of MECs. Triangles and squares represent the current density and Coulombic efficiency, respectively; open and filled symbols represent results of the MECs without and with UV irradiation, respectively. 10485

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and 6.44 × 108 /mg for the samples of 0−0.5, 0.5−1.0, and 1.0−1.5 cm, respectively. The UV irradiation might have little inhibition on bacteria at the region deeper than 1.0 cm. The results indicated that the bacterial inactivation by UV irradiation also occurred on the anode. However, because of high surface area of the anode in the MEC, sufficient exoelectrogens could survive even with the UV irradiation. Biomass was examined to reveal the difference of biofilm growth in the MECs with and without UV irradiation. Biomass on the cathode from the reactors without UV irradiation was significantly higher than that from the reactors with UV irradiation (0.51 ± 0.05 vs 0.06 ± 0.01 mg protein/mg cathode). The biomass result on the cathode was in accord with the number of bacteria of the DAPI analysis. However, the biomass on the anodes of MECs with and without UV irradiation was not substantially different (14.3 ± 0.6 vs 15.4 ± 0.7 mg protein/mg anode). The biomass on the anodes was much higher than that on the cathodes (15.4 ± 0.7 vs 0.51 ± 0.05 mg protein/mg for the reactors without UV irradiation, and 14.3 ± 0.6 vs 0.06 ± 0.01 mg protein/mg for the reactors with UV irradiation), which was likely attributable to the significantly larger surface area of the anodes. Based on the quantitative PCR analysis, only hydrogenotrophic methanogens and no acetoclastic methanogens were observed within the cathodic biofilm (data not shown). The result was consistent with those in the literature.17,26

MECs remained stable within the range of 114 ± 3.6% to 137 ± 4.0%, which were similar to those obtained in stage 1. Energy efficiencies from the MECs without UV irradiation decreased to 91%) and relatively high H2 yields were maintained in the MEC over 30 cycles (about 60 days) of operation. On the contrary, without UV irradiation, H2 production decreased with time, which was consistent with previous observations,9,14 and the amount of CH4 reached up to 94% after 35 cycles (74 days) of operation. In the MEC fed with acetate, total biodegradation of 1 mol of acetate should produce 4 mol of H2 theoretically. If the amount of H2 is converted into CH4 by hydrogenotrophic methanogens, only 1 mol of CH4 is achieved. Although the combustion heat of CH4 is higher than that of H2 (890.31 vs 285.83 kJ/mol), 2 the conversion from H2 into CH4 results in an energy loss of 253 kJ/mol acetate. The conversion from H2 to CH4 also reduces the energy efficiency.12,25 The higher energy efficiencies with UV irradiation clearly showed that UV irradiation could effectively inhibit methanogenesis and improve the MEC performance. As far as we know, this is the first time to report that relatively high H2 concentration (>91%) can be maintained in single-chamber MECs during operation about 60 days. The UV irradiation was nonselective for the bacterial inactivation on both the cathode and anode. However, the cathodic methanogenesis was mainly responsible for the CH4 production in the MEC as shown by little CH4 production after immediately replacing the cathodes. The UV irradiation reduced the number of bacteria (including methanogens) and the biomass on the cathode by more than six times as those without UV irradiation. Therefore, the cathodic methanogenesis should be greatly affected by the UV irradiation. On the other hand, attributable to the significantly larger surface area of the anode, the biomass on the anodes of MECs with and without UV irradiation was not substantially different. The activities of exoelectrogens on the anode were not affected by the UV irradiation significantly.

irradiation, the number of bacteria on the cathode was 0.35 × 106/mg at cycle 4 (day 8) and increased to 1.56 × 106/mg at cycle 10 (i.e., at the end of stage 1, day 20). At cycle 35 (day 74), the number of bacteria reached 15.5 × 106/mg. However, with UV irradiation, the number of bacteria greatly decreased from 1.56 × 106/mg at cycle 10 to 0.41 × 106/mg at cycle 12 (day 24). After 35 cycles of operation, the number of bacteria with UV irradiation slightly increased to 2.04 × 106/mg, which was about 7 times lower than that without UV irradiation. The bacteria on the cathode were effectively inhibited by UV irradiation during the relatively long-term operation. After two cycles of UV irradiation for the reactors without UV irradiation for 35 cycles, the total number of bacteria on the cathode decreased to 5.71 × 108. Bacterial distributions along the radical direction of the anode were significantly different with and without UV irradiation (Table 2). Without UV irradiation, the cell numbers were 6.30 × 108, 6.66 × 108, 6.80 × 108 /mg for the samples of 0−0.5, 0.5−1.0, and 1.0−1.5 cm, respectively. With UV irradiation, the cell numbers were 2.02 × 108, 5.54 × 108, Table 2. Bacterial Counts on the Anode in the MEC at Different Radical Depths Without and With UV Irradiation in Cycle 35 radical depth (cm) 0.0−0.5 0.5−1.0 1.0−1.5 0.0−0.5 0.5−1.0 1.0−1.5

unit mass ( × 108/mg) Without UV 6.30 ± 0.6 6.66 ± 0.72 6.80 ± 0.52 With UV 2.02 ± 0.16 5.54 ± 0.42 6.44 ± 0.62

total ( × 1010) 3.02 ± 0.29 3.20 ± 0.35 3.26 ± 0.25 0.97 ± 0.08 2.66 ± 0.20 3.14 ± 0.30 10486

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consumption (9.19 kWh/m3 H2). If 12 mW/cm2 of UV intensity with 20 s of exposure time per running cycle, for example, is used in the MEC, the energy consumption is only 0.13 kWh/m3 H2. Since the UV irradiation is a nonselective method for bacterial inhibition, the UV lamps should be installed as closely as possible to the cathode surface (including adding water tight UV lamps in the reactor) in a continuous MEC system to effectively inhibit the methanogenesis on the cathode. To keep the exoelectrogens be active, larger specific surface area of anode electrode should be used in the scale-up MEC system. The effect of UV irradiation on the methanogenesis inhibition in the MECs with real wastewaters will be examined in further study.

Our experimental results showed that CH4 production was attributable to the cathodic methanogenesis and mainly through hydrogenotrophic methanogenesis. After replacing the cathode with biofilm by a new one in the MEC, CH4 production was undetectable, implying that except on the cathode, negligible methanogenesis existed in the system. In single-chamber MEC, change of the solution redox potential was rather small based on the Nernst equation estimation. Instead, cathode potential should affect the metabolic activity of methanogens. Higher CH4 production can be achieved at more negative cathode potentials in a methanogenic bioelectrochemical system.27 In our system, with an applied voltage of 0.8 V, the cathode potential of the steady stage was about −1.0 V (vs saturated calomel electrode, SCE), which was much lower than the anode potential (about −0.2 V vs SCE). Undetectable CH4 production in the open circuit MEC indicated that acetoclastic methanogenesis was negligible on the cathode, which was further supported by the quantitative PCR analysis, in which acetoclastic methanogens (Methanosaetaceae and Methanosarcinaceae) were not observed. Similar CEs for the MECs with and without UV irradiation, to some extent, also suggested that CH4 was produced by hydrogenotrophic methanogens rather than acetoclastic methanogens because acetoclastic methanogens should decrease CEs.11 The MEC with UV irradiation showed advantages over other methanogenesis inhibition methods. For example, compared to the MEC operated at low temperatures (4 °C),11 the MEC with UV irradiation produced higher H2 yield (2.87−3.70 vs 2.94 mol H2/mol acetate) and current density (62−75 vs 38 A/ m3). By adopting appropriate electrode structure, UV irradiation can effectively inhibit cathodic methanogenesis in the MEC without substantially reducing current generation. On the contrary, in the previously reported methods, either exposing the electrodes to air or lowering pH may severely damage both methanogens and exoelectrogens during the operation.6,13 The UV irradiation is easy to operate and will not cause any secondary pollutions, while the chemical inhibitor (BES) is toxic.11 Our results showed that once methanogenesis was well established, UV irradiation could not inhibit CH4 production effectively. This was possibly because some methanogens were still active within the cathode biofilm. To ensure high and relatively pure H2 production in the MEC, UV irradiation for methanogenesis inhibition should be employed at the beginning of the operation. Implication. Ultraviolet irradiation is a simple and efficient approach for methanogenesis inhibition in practice. The UV method has been widely used in water disinfection. Large amount of wastewater can be efficiently treated and continuously operated for many years using UV irradiation.28 Such experience of UV applications should be helpful to construct the MEC with UV irradiation in practice. Online monitoring can be used to improve the efficiency and to save energy of UV irradiation.29 The problem of biofouling or scaling on the quartz reactors can be resolved by several methods, such as the UV/electrolysis hybrid method.30 The energy consumption of UV irradiation in the MEC can be further optimized, including improvement of the UV absorbing materials and the UV absorbed effects of Pt on inactivation. In addition, application of high UV intensity with short exposure time should effectively inhibit bacteria with low energy consumption.20 In this study, a low UV intensity of 100 μW/ cm2 was used to avoid temperature increase on the reactor surface, resulting in long exposure time and high energy

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AUTHOR INFORMATION

Corresponding Authors

*Phone: +86 20 84110052; e-mail: [email protected]. *Phone: +86 20 84110052; e-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was partly supported by grants from the National Natural Science Foundation of China (Nos. 51278500, 51308557, and 51039007), the program of Guangzhou Science & Technology Department (No. 2012J4300115) and the Fundamental Research Funds for the Central Universities.

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