Continuous Feed Microbial Fuel Cell Using An Air Cathode and A

The use of granules led to a better treatment of the wastewater but did not .... ion chromatograph with an AS40 automated sampler and with an IonPac A...
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Energy Fuels 2009, 23, 5707–5716 Published on Web 10/19/2009

: DOI:10.1021/ef9005934

Continuous Feed Microbial Fuel Cell Using An Air Cathode and A Disc Anode Stack for Wastewater Treatment Mirella Di Lorenzo,*,‡ Keith Scott,‡ Tom P. Curtis,† Krishna P. Katuri,‡ and Ian M. Head† †

School of Civil Engineering and Geosciences, ‡School of Chemical Engineering and Advanced Materials, Newcastle University, Newcastle upon Tyne, NE1 7RU United Kingdom Received June 10, 2009. Revised Manuscript Received September 16, 2009

The performance of a single-chamber microbial fuel cell (SCMFC), with air cathodes surrounding a series of graphite discs anodes, is reported. The materials used in the MFC are low-cost options for its construction. The air cathode, made from an activated carbon, was supported on a low-cost polypropylene/silica composite membrane. The system was operated in continuous mode and fed with wastewater from the primary clarifier of a wastewater treatment plant. The optimal external load was 100 Ω, with a current output of 2.2 mA and a power density of 50 mW m-2, defined with regard to the anode surface area. In the treatment of the wastewater, the chemical oxygen demand (COD) loading rate was a key factor in the performance of the SCMFC: lower organic loadings gave higher Coulombic efficiency with a maximum of 63.4 ( 4.2% when the system was fed with 0.055 kg COD m-3 d-1, meaning that the electro-active biofilm was responsible for the majority of the COD removal. The performance was compared with an alternative anode configuration made of graphite granules. The use of granules led to a better treatment of the wastewater but did not improve the performance of the SCMFC with regard to the current and power output. In particular, the power output was approximately three times lower compared to the graphite disk anode (0.17 mW vs 0.484 mW), and the maximum Coulombic efficiency was only 28%.

In comparison with conventional aerobic treatment, the main advantages of AWT are: lower treatment costs; high flexibility; high loading rate operation; smaller volume of waste sludge; and finally, anaerobic organisms can be preserved unfed for long periods of time.1 The UASB (upflow anaerobic sludge blanket) technology, developed about 30 year ago, is the most common among all the anaerobic treatment systems, and approximately 60% of the anaerobic full-scale treatment facilities worldwide are now based on the UASB design.2 Recently, in addition to anaerobic digestion, microbial fuel cell (MFC) technology has attracted increasing attention from both the academics and the public as a novel biotechnology to treat wastewater and harvest energy from dissolved organic carbon. MFCs rely on the ability of certain species of microorganisms to transfer electrons from the inside of the cell to an electrode (anode) while they are oxidizing, and therefore removing, the organic materials in wastewater.3 In contrast to chemical fuel cells, in an MFC microorganisms act as biocatalyst at the anode. A recent review compared MFC performance to conventional AWT.4 MFCs have the great advantages of producing electricity from organic waste in a direct way, and therefore use energy much more efficiently than standard combustion engines that are limited by the Carnot cycle. Also, there is no need for gas treatment, which is required with traditional anaerobic digestion.

Introduction Industrial processes, as well as municipal wastewater collection, almost always result in waste or side-products that require further treatment. Environmentally benign low-cost processes are needed by the end users of water pollution control equipment. Microbe-based biological methods continue to be the prime choice for efficient and sustainable wastewater processing in conjunction with chemical and physical treatment. In particular, biological treatment methods clearly dominate the secondary wastewater treatment sector as it is the most effective and eco-friendly option currently available. In recent years, a combination of tighter restrictions on sludge disposal site location, air pollution, hazardous waste disposal, and odor control, has had substantial impact on the applicability of aerobic treatment of industrial wastewater.1 Moreover, the urgent global demand for alternative energy sources, less energy intensive processes, and the emerging drive toward a more sustainable society, has led to an increasing interest in technologies that consider wastewater as a renewable source of energy. In this context, anaerobic wastewater treatment (AWT) is becoming increasingly popular worldwide and up to now represents the only technology proven to be capable of extracting energy from wastewater on a commercial scale.2 *To whom correspondence should be addressed. Phone: þ39 0832298120. Fax: þ39 0832298146. E-mail: [email protected]. (1) Lema, J. M.; Omil, F. Water Sci. Technol. 2001, 44 (8), 133–140. (2) Angenent, L. T.; Karim, K.; Al-Dahlam, M.; Wrenn, B. A.; Domiguez-Espinosa, R. Trends Biotechnol. 2004, 22 (9), 477–485. r 2009 American Chemical Society

(3) Rozendal, R. A.; Hamelers, H. V. M.; Rabaey, K.; Keller, J.; Buisman, C. J. N. Trends Biotechnol. 2008, 26 (8), 450–459. (4) Pham, T. H.; Rabaey, K.; Aelterman, P.; Clauwaert, P.; De Schamphelaire, L.; Boon, N.; Verstraete, W. Eng. Life Sci. 2006, 6 (3), 285–292.

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Theoretically, MFCs can convert 1 kg of chemical oxygen demand (COD) to 4 kW, whereas with anaerobic digestion 1 kg of COD could be converted to roughly 1 kW.11 MFCs can operate at low temperatures of operation (below 20 °C) and low COD concentration, where AWT generally would fail due to low reaction rates. Nitrogen removal in MFCs has also been demonstrated.5,6 In the past few years, the configuration of MFCs has been continuously improved, and the performance increased 10-fold since the first application on a laboratory-scale with two-chamber MFCs.7 However, the maximum current generated with MFCs is only around 0.1 A, and the average power density of MFCs is around 40 W m-3.8 These peak values refer strictly to the utilization of a synthetic effluent, characterized by easily biodegradable compounds, and to operation in batch mode. The electrical performances in general decrease when real wastewater is used and/or the MFC is operated with continuous flow.8 The biggest barriers for practical applications of this novel technology in a wastewater treatment plant, are related to difficulties in scaling-up the process and to their capital costs. So far, MFCs have been operated only at a small-scale from a few milliliters to several liters at most. It has been recently estimated that the capital costs of a fullscale MFC system would be orders of magnitude higher than those of conventional wastewater treatment systems. These costs are particularly affected by the price of the cathode catalyst, which is platinum in most cases, and the price of the proton exchange membrane (PEM), with an impact in the total price compared to conventional aerobic treatment systems of approximately 47 and 38% respectively.3 Recently, many studies have focused on alternative cathode catalysts. Cotetra-methyl phenylporphyrin (CoTMPP), iron phthalocyanine (FePc), and manganese oxide have recently been shown to be suitable alternatives to Pt in MFCs, however they still need further investigation.9-12 System using bacteria as catalyst at the cathode (biocathodes) have been also investigated.13,14 To overcome the high price of the PEM, membraneless MFCs have been tested. However, due to substantial oxygen diffusion into the anode chamber, the Coulombic efficiencies decreased.15 In this study we analyzed the performance of a singlechamber microbial fuel cell (SCMFC) with activated carbon air cathodes surrounding a series of graphite discs anodes. The

air cathode was supported on a low-cost polyethylene/silica composite membrane. The performance was compared with an alternative anode configuration made of graphite granules and characterized by a higher surface area. In order to better simulate the operating condition in a treatment plant, the reactor was operated in continuous mode and fed with real wastewater. Material and Methods Microbial fuel cell. The microbial fuel cell (SCMFC) used in the experiments was of square cross-section and was placed between two glass tubes (QVF) as shown in Figure 1. The material of construction was polyacrylate. The MFC contained four cathodes (2 cm8 cm), one on each face of the quadrangle. The cathodes were exposed to air on one side and to the anodic compartment on the other. The cathode was produced by directly spraying an ultrasonically mixed carbon black (Ketjen black 300, Akzo Chemicals Ltd.), acetone, and 10% PTFE suspension onto a polypropylene/silicate composite membrane (RhinoHide Entek International, UK) to a loading of 0.1 mg cm-2 The anode, consisted of 10 graphite discs (2.6 cm diameter, 0.2 cm thickness) having 40 small holes (0.2 cm diameter) for flow of wastewater through the cell. The surface area per disk was 8.9 cm2, resulting in a total anode surface area of 89 cm2 (Figure 1). The graphite discs were supported on a titanium rod (0.5 cm diameter). The empty volume of the cube cell was 350 cm3. The total fluid volume (Vf) in the cell and connecting glassware was 1100 cm3, and a head space of 500 cm3 was maintained by using a U-tube for the outlet. To determine the effect of anode surface area on performance, an alternative anode configuration, using graphite granules (diameters between 0.2 and 0.6 cm, Carbon International, London, UK) was used. The granules were connected to the cell using the titanium rod with two graphite discs at the top of the rod, one disk at the bottom, and another one in the middle. The granules were packed in the spaces between the graphite discs and held in place with a titanium net to occupy the cylindrical space in between the four cathodes in the cube cell. The empty volume of the cube cell was reduced to 280 cm3, while the total fluid volume (Vf) was, in this case, 900 cm3. The total external surface area of the graphite granules (Sp) was calculated by approximating the area of a single pellet with the surface of a sphere having an average diameter of 0.4 cm and by multiplying the surface of one pellet into the total number of pellets introduced in the reactor. This approximation did not consider the contribution of the pellet roughness to the Sp. The total anode surface area (Satot) was estimated as 1496 cm2, by adding the surface areas of the four graphite discs to the pellet surface. Throughout the study the anode and cathode were connected through a voltmeter (Pico data logger) and an external resistance to polarize the cell and monitor the current variation under closed circuit conditions. The external resistance was controlled by utilizing a resistor substitution box (RS 500, 1% accuracy, Elenco electronics). In operation of the cell, wastewater was fed through the injection port, in up-flow mode, at flow rates in the range of 0.18-0.52 cm3 min-1 using a peristaltic pump (WatsonMarlow, 520S) equipped with Marprene II tubing (0.5 cm internal diameter). The effluent was collected from the outlet (E) for analysis. The MFC was operated at room temperature,

(5) Jia, Y.-H.; Tran, H.-T.; Kim, D.-H.; Oh, S.-J.; Park, D.-H.; Zhang, R.-H.; Ahn, D.-H. Bioprocess Biosyst. Eng. 2008, 31 (4), 315– 321. (6) Clauwaert, P.; Rabaey, K.; Aelterman, P.; De Schamphelaire, L.; Pham, T. H.; Boeckx, P.; Boon, N.; Verstraete, W. Environ. Sci. Technol. 2007, 41, 3354–3360. (7) Logan, B. E.; Regan, J. M. Trends Microbiol. 2006, 14 (12), 512– 518. (8) Logan, B. E. Microbial Fuel Cells; Wiley: New York, 2008. (9) Roche, I.; Katuri, K.; Scott, K. J. Appl. Electrochem. 2009, 39, 197–204. (10) Cheng, S.; Liu, H.; Logan, B. E. Environ. Sci. Technol. 2006, 40, 364–369. (11) Zhao, F.; Harnisch, F.; Schroder, U.; Scholz, F.; Bogdanoff, P.; Herrman, I. Electrochem. Commun. 2005, 7, 1405–1410. (12) Hao, Yu, E.; Cheng, S.; Scott, K.; Logan, B. E. J. Power Sources 2007, 171, 275–281. (13) Clauwaert, P.; Van der Ha, N.; Boon, N.; Verbeken, K.; Verhaege, M.; Rabaey, K.; Verstraete, W. Environ. Sci. Technol. 2007, 41, 3354–3360. (14) He, Z.; Angenent, L. T. Electroanalysis 2006, 18, 2009–2015. (15) Liu, H.; Logan, B. E. Environ. Sci. Technol. 2004, 38, 4040–4046.

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Di Lorenzo et al. Table 1. Characteristic of the Wastewater Utilized parameter

value

pH alkalinity, ppm conductivitya, μS cm-1 COD, ppm BOD, ppm TOC, ppm NH3-N, ppm phosphate, ppm sulfate, ppm total suspended solids, ppm

7 46 ( 3 1570 ( 10 175 ( 50 88 ( 5 98 ( 2 21 ( 0.3 4.1 ( 0.9 49.4 ( 9 187 ( 18

a

At 20.7 °C.

to keep the WW conductivity constant and equal to the non diluted WW. The wastewaters were prefiltered over a woven cloth to remove suspended solids before addition to the reactor. Enrichment. The enrichment of the anode surface with electrochemically active bacteria was performed in continuous mode by feeding the reactor at a fixed flow rate of 0.353 cm3 min-1 with WW containing 1000 ppm of glucose. The COD loading rate, defined by considering the total fluid volume (Vf), was 0.55 kg COD m-3 d-1 (0.38 mg COD L-1 min-1) in the case of graphite discs, and of 0.67 kg COD m-3 d-1 in the case of graphite granules. Analyses. The COD was determined using a standard method with chromate as the oxidant as previously described.16 All samples were filtered through a 0.22 μm pore diameter membrane filter (VWR International) prior to COD measurements. The COD consumption rate was calculated, when steady state was reached, using the formula: Q  ðCODin - CODout Þ

ð1Þ

where Q (dm3 h-1) was the fuel flow rate, and CODin and CODout (mg dm-3) were the COD of the influent and the effluent, at the steady-state, respectively. Total suspended solids of the wastewater was determined as previously described.16 Sulfate and phosphate concentration in the real wastewater were determined using a Dionex ICS-1000 ion chromatograph with an AS40 automated sampler and with an IonPac AS14A, 4125 mm analytical column; 8 mM Na2CO3 solution was used as eluent at a flow rate of 1 cm3 min-1. A sample loop of 25 μL was used; the detector was an electrochemical conductivity detector. The Coulombic efficiency (fractional), at the steady-state was calculated with formula 2:

Figure 1. Single chamber microbial fuel cell utilized in this study. A: air cathode; B: inlet; C: outlet; D: polyacrylate plastic block containing the electrodes; E: anode configuration with graphite discs. The cross area of each cathode was of 16 cm2 for a total surface of 64 cm2.

εc ¼

MI  100% FzQΔCOD

ð2Þ

where F is Faraday’s constant (96 485 C mol-1); M=32 is the molecular weight of oxygen, I (A) is the current at the steadystate; z=4 is the number of electron exchanged per mole of oxygen, Q (dm3 s-1) is the flow rate through the system, and ΔCOD (g dm3) the difference in the influent and effluent COD. Conductivity measurements were performed with a conductivity meter provided by Hanna instruments. The internal cell resistance was measured by electrochemical

approximately 21 ( 2 °C. The feed solution was maintained at a temperature of 7 ( 2 °C in order to minimize bacterial growth. Nitrogen was purged into the feeding tank. Wastewater. The wastewater (WW) utilized during the experiments was collected from the primary clarifier of the treatment plant located in Cramlington (Northumbria Water, UK). It had a COD of 175 ( 50 ppm (mg dm-3) and other characteristics shown in Table 1. No inoculum was used. In some experiments the COD of the WW was increased by utilizing glucose as specified, or decreased by dilution with tap water. In this last case, an appropriate volume of phosphate buffer (5 M, pH 7) was added in order

(16) Greenberg, A.; Clesceri, L. S.; Eaton, A. D., Standard Methods for the Examination of Water and Wastewater, 18th ed.; American Public Health Association: Washington, 1992.

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Figure 3. Polarization and current density curves from the SCMFC. Current density refers to the area of the anode, 84 cm2 (8.4  10-3 m2). Power density refers to the anodic volume: 350 cm3. Anode material: graphite discs. The polarization curves were recorded using a potentiostat (Gillac, ACM Instruments) at a scan rate of 1 mV s-1 from an open circuit potential established after 4 h.

Figure 2. Electrochemically active bacteria enrichment of the SCMFC. The SCMFC was fed in continuous mode until a stable current output was obtained and the electrochemically active bacteria were considered to be enriched and stabilized at the anode site. Anode material: graphite discs. External resistance: 10 Ω. Feeding rate: 0.35 cm3 min-1. Loading rate: 0.55 kg COD m-3 d-1. Fuel: sewage wastewater containing 1000 ppm of glucose. Inlet COD: 1180 ( 70 ppm.

nucleic acid sequence database, were identified using the BLAST algorithm.18

impedance spectroscopy using a potentiostat (Gillac, ACM Instruments) with the cathode as the working electrode and the anode as counter electrode and reference electrode. Impedance measurements were conducted at open circuit voltage (OCV) over a frequency range of 104 down to 102 Hz with a sinusoidal perturbation of 15 mV amplitude. Polarization curves were recorded by means of a potentiostat (Gillac, ACM Instruments) at a scan rate of 1 mV s-1 after establishing stable behavior at an open circuit potential of over 4 h. The reference electrode was mercury/mecurous sulfate (MMS). The values of potentials reported are referred to the normal hydrogen electrode (NHE). Community Analysis. The bacterial community cells were fixed by dipping the anode in a 1:1 solution of pure ethanol and sodium phosphate buffer (50 mM, pH 7.5), followed by storage at -20 °C until analysis. Total DNA was extracted from the biofilm, from the suspension of sodium phosphate buffer, and from the influent wastewater. In particular, the biofilm was scratched from graphite discs placed at different height of the graphite rod: starting from the top, discs 2, 4, 6, 8, and 10 were considered. The 16S rRNA gene fragments from the bacterial populations were amplified using primers 1 and 3 as previously described,17 which were provided by Thermo Electron GmbH (Germany). The 16S rRNA gene fragments were subsequently analyzed by denaturing gradient gel electrophoresis (DGGE) and bands were cut out of the gel with a clean scalpel and added to 50 μL of PCR grade water. After 12 h of incubation at 4 °C, 1 μL of the solution was reamplified with the same primers and sent for sequencing. DNA sequencing of the fragments was carried out by Genevision T/A Geneius (INEX Business Centre, UK). The DNA sequences were analyzed and the closest-matching sequences in the National Centre for Biotechnology Information

Results Enrichment. As shown in Figure 2, during enrichment with electro-active bacteria, the SCMFC with graphite disk anodes exhibited an initial lag phase with no substantial changes in the current generated, for approximately four days. This phase was due to the build up of biomass and its adaptation to the environment in the cell.19 An exponential increase in current followed and, after 9 days, a stable current output of 5 ( 0.6 mA was reached. The output power, measured with the 10 Ω resistor, was 0.25 mW and the Coulombic efficiency was 7.40 ( 0.16%. The internal resistance was 15 Ω. Figure 3 shows the polarization and power density curves obtained with the SCMFC after the stable current was achieved. The open circuit voltage was 0.46 V, and the cell voltage fell gradually with an increase of current density until a value of almost 0 V at a current density of approximately 350 mA m-2. Over the full range of polarization the anode potential contributed to approximately 250 mV of the potential loss, and the remainder was mainly due to Ohmic potential losses and cathode polarization (Figure 3). There are indications of some mass transfer limitations in the anode and cell polarizations curves. The maximum power output was approximately of 55 mW m-2 (1.4 W m-3) obtained at a current density of 202 mA m-2. Effect of the External Resistance. Once the performance of the SCMFC with graphite discs stabilized, the effect of the external resistance (Rext) on the power output was investigated. For this purpose, the SCMFC was connected to a series of external loads varying from 10 to 4000 Ω, with a constant organic loading rate of 0.55 kg COD m-3 d-1. Table 2 reports the current generated at each value of Rext. The current decreased by increasing the external resistance from 10 to 4000 Ω: the highest fall in current was observed when the resistance was changed from 10 Ω to 50 Ω, with a total current decrease of 40%. For higher values of Rext the effects on the output current were minor, and in particular

(17) Kowalchuck, G. A.; Stephen, J. R.; De Boer, W.; Prosser, J. I.; Embley, T. M.; Woldendorp, J. W. Appl. Environ. Microbiol. 1997, 63, 1489–1497. (18) Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Nucleic Acid Res. 1997, 25, 3389–3402.

(19) Rabaey, K.; Clauwaert, P.; Aelterman, P.; Verstraete, W. Environ. Sci. Technol. 2005, 39 (20), 8077–8082.

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Table 2. Effect of the External Resistance on the SCMFC Performancea Rext (Ω) 10 50 100 300 500 800 1000 2000 3000 4000

steady-state cell potential (mV)

steady-state current (mA)

50 ( 8.4 150 ( 17 220 ( 30 342 ( 38 400 ( 33 448 ( 57 355 ( 25 398 ( 71 456 ( 115 492 ( 85

5 ( 0. 6 3 ( 0.24 2.2 ( 0.21 1.14 ( 0.09 0.8 ( 0.047 0.56 ( 0.05 0.355 ( 0.018 0.199 ( 0.05 0.152 ( 0.027 0.123 ( 0.015

0.25 0.45 0.484 0.39 0.32 0.25 0.126 0.079 0.069 0.060

COD removal rate (mg COD min-1)

coulombic efficiency (%)

0.33 ( 0.03 0.26 ( 0.05 0.30 ( 0.03 0.32 ( 0.05 0.30 ( 0.03 0.30 ( 0.09 0.28 ( 0.03 0.31 ( 0.02 0.30 ( 0.04 0.32 ( 0.09

7.40 ( 0.16 6.27 ( 1.38 3.67 ( 0.04 1.76 ( 0.02 1.47 ( 0.03 0.92 ( 0.04 0.63 ( 0.05 0.32 ( 0.02 0.25 ( 0.02 0.19 ( 0.01

a Loading rate 0.55 kg COD m-3 d-1. Fuel: wastewater containing 1000 ppm of glucose. Inlet COD: 1180 ( 70 ppm. Anode material: graphite discs. Anode surface area: 89 cm2. The step changes of Rext were obtained with a resistor substitution box (RS 500, 1% accuracy, Elenco electronics). Measurements of COD removal rate and coulombic efficiency from three replicates.

Starting with fuel made from wastewater plus 1000 ppm of glucose (total inlet COD: 1180 ( 70 ppm), the glucose concentration was reduced until the point at which pure wastewater was utilized. Further COD reductions were obtained by diluting the wastewater with tap water, with phosphate buffer added to maintain the conductivity (see Table 3). The fuel loading rate interval, obtained in this way, varied from 0.04 kg COD m-3 d-1 to 0.55 kg COD m-3 d-1, corresponding to a wastewater dilution of 1:3.3, and to wastewater containing 1000 ppm of glucose respectively. As reported in Table 3, the power density increased with the loading rate until the value of 0.08 kg COD d-1 m-3; further increase in the loading rate did not lead to improvements in the power output. The Coulombic efficiency increased with the first increase in loading rate (i.e., from 0.037 to 0.055 kg COD d-1 m-3), reaching a maximum value of 63.4 ( 4.2%. Further increases in loading rate caused a decrease of the Coulombic efficiency until the value of 3.3 ( 0.38%, at the maximum COD loading rate (0.55 kg COD m-3 d-1). On the other hand, at a high COD loading rate, good COD removal was achieved (Table 3). For a loading rate of 0.55 kg COD m-3 d-1, 80% removal was observed, while low inlet CODs led to approximately half the values of percentage COD removal. The explanation of this behavior can be attributed to the nature of the fuel. The addition of glucose to the WW in fact, led to a high fraction of easily biodegradable COD in the influent, which would explain the very good removal efficiencies observed. Wastewaters, by contrast, are characterized by high amounts of complex substrates that require longer time for digestion. This behavior was confirmed when the effect of the flow rate on the system performance was investigated. The flow rate was in one case reduced to 0.18 cm3 min-1 and in another increased to 0.52 cm3 min-1, and the results were compared with the rate of 0.35 cm3 min-1 previously utilized (Table 4). At the lowest flow rate, the percentage COD removal increased by approximately 60% with respect to that at the rate of 0.35 cm3 min-1, due to an increase in the HRT. When the flow rate was increased a lower COD removal was reached. Analysis of Anode Microbial Communities. The anodic performance of an MFC is inextricably dependent on the nature and rate of electron transfer from the microbial cell to the anode. The composition of bacterial communities formed at the anode can be complex and may vary markedly according to the nature of the electrode and of the substrate utilized. Understanding the nature of the microbial community that develops on the anode and the mechanisms involved

Figure 4. Effect of the external resistance on current, voltage, and power output. The reactor was continuously fed with wastewater containing 1000 ppm of glucose for a total inlet COD concentration of 1180 ( 70 ppm and a loading rate of 0.55 kg COD m-3 d-1. Anode material: graphite discs.

the higher the value of Rext the lower the current step decrease, with a reduction of less than 20% for a change from 3 kΩ to 4 kΩ. Table 2 reports the reactor performance also in terms of power generated at the steady-state, COD removal, and maximum Coulombic efficiency, that is, that measured for current at the steady-state and based on the variation of CODin - CODout at the steady-state. The Coulombic efficiency was a function of the steady-state current and therefore increased by decreasing the external resistance as the current increased. The external resistance therefore did not have a major influence on the COD removal rate, which was approximately constant at 0.3 ( 0.06 mg COD min-1, corresponding to approximately 72% of COD removal. The maximum value of the Coulombic efficiency, obtained at a Rext of 10 Ω, was 7.4 ( 0.16%, demonstrating that, even in the case of the highest current production, a high percentage of the COD removed did not contribute to electricity production. The highest power output was of 52.7 mW m-2 (defined with regard to the anode surface area), as confirmed from the polarization curve in Figure 3, and was reached at a Rext of 100 Ω (see Table 2 and Figure 4). For this reason, 100 Ω was chosen as Rext for all the following experiments. Effect of Organic Loading Rate. The effect of the loading rate on the system performance was analyzed by considering several input COD concentrations, at a constant flow rate, 0.35 cm3 min-1, and, therefore, at a constant hydraulic retention time (HRT), which was approximately 17 h. 5711

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Table 3. Effect of the Loading Rate on the SCMFC Performancea influent

COD loading rate (kg COD m-3 d-1)

current (mA)

COD removal (%)

Coulombic efficiency (%)

power density (mW m-2)

WW diluted 1:3.3 WW diluted 1:2 WW diluted 1:1.3 WW WW þ 100 ppm of glucose WW þ 300 ppm of glucose WW þ 600 ppm of glucose WW þ 1000 ppm of glucose

0.04 0.05 0.07 0.08 0.13 0.22 0.35 0.55

1.48 ( 0.08 2.01 ( 0.02 1.90 ( 0.04 2.27 ( 0.04 2.23 ( 0.06 2.21 ( 0.06 2.18 ( 0.09 2.21 ( 0.08

45 ( 1.2 41 ( 9.2 46 ( 1.1 48 ( 1.5 49 ( 5 78 ( 1.7 81 ( 1.2 80 ( 2

58 ( 2.2 63.4 ( 4.2 40 ( 1.2 37.1 ( 1.4 22.1 ( 3.2 8.24 ( 0.2 4.9 ( 0.0736 3.3 ( 0.38

24.7 ( 3.7 38.0 ( 1.2 39.3 ( 2.3 57.9 ( 3.2 55.4 ( 4.6 54.9 ( 4.1 53.4 ( 6.4 54.9 ( 5.8

a Rext 100 Ω. Fuel: wastewater characterized by several input CODs. Power density referred to the anode surface area: 89 cm2. Anode material: graphite discs.

Table 4. Effect of the HRTa COD loading rate flow rate 3 -1 (cm min ) (kg COD m-3 d-1) 0.18 0.35 0.52

0.028 0.055 0.081

current output (mA)

COD Coulombic removal efficiency (%) (%)

1.47 ( 0.05 65 ( 5.0 57 ( 5.8 2.01 ( 0.02 41 ( 9.2 63.4 ( 4.2 2.4 ( 0.1 31.2 ( 1.7 64.1 ( 3.3

a Anode material: graphite discs. Fuel: sewage wastewater diluted 1:2. Inlet COD: 120 ppm. Loading rate: 0.055 kg COD m-3 d-1.

is fundamental to optimising the overall system and has been the subject of several reviews.20,21 In this study, the bioelectrocatalysis was achieved by the interaction of a mixed community of bacteria, usually referred to as the “electrochemically active bacterial consortium”. The bacterial community composition of the biofilm formed on the graphite discs was investigated (Figure 5). In order to estimate the influence of the position of the graphite discs in the reactor on the consortium composition, we analyzed the biofilm formed on discs placed at different height on the titanium rod (Figure 5). DGGE analysis of 16S rRNA gene fragments showed only small differences in biofilm community composition between graphite discs at different locations in the reactor. The microbial community on the anodes was distinct from the community in the influent wastewater and, in particular, two bands were predominant. Comparative analysis of partial 16S rRNA gene sequences of from the most intense bands in the DGGE profiles showed high similarity with the 16S rRNA from Chlorobium spp. (95% identity over 154 bp) and Mesorhizobium species (99% identity over 136 bp). Chlorobium spp. are anoxygenic photosynthetic bacteria and its predominance could be explained by the fact that the reactor was open to the light. Chlorobium spp. normally grow in environments rich in hydrogen sulphide, which they use as electron donor to generate reducing power for biosynthesis and produce elemental sulfur as a product of sulfide oxidation. In addition, they can photo-oxidize hydrogen as well as other sulfur compounds such as sulphide, polysulfide, and thiosulfate.22,23 Fermentation of organic matter and sulfate reduction are potential sources of methane in the MFC, however the sulfate concentrations were approximately 0.5 mM and were unlikely to sustain high levels of sulfide

Figure 5. DGGE analysis of 16S rRNA gene fragments from the microbial communities in the SCMFC. Anode material: graphite discs. 1: influent wastewater; 2: biofilm from disk 2; 3: biofilm from disk 4; 4: biofilm from disk 6; 5: biomass from the 1:1 ethanol/ sodium phosphate buffer solution used to store the anode; 6: biofilm from disk 8; 7: biofilm from disk 10. The bands which were cut out and sequenced are indicated with the arrows. A: similarity with Chlorobium sp, B: similarity with Mesorhizobium sp.

generation. Fermentation of organic matter may therefore be the most likely source of sulfide in the MFC system. Hydrogen produced as an intermediate in organic matter fermentation may also have supported the growth of Chlorobium spp. Mesorhizobium spp. are Alphaproteobacteria and include organisms that enter into symbiotic relationships with plants where the bacteria perform nitrogen fixation. The genus also contains nonsymbiotic organisms. Many studies have regarded MFCs operated with specific axenic cultures, such as Shewanella sp., Pseudomonas aeruginosa,

(20) Schroder, U. Phys. Chem. Chem. Phys. 2007, 9, 2619–2629. (21) Logan, B. E.; Regan, J. M. Trends Biotechnol. 2006, 14 (12), 512– 518. (22) Cork, D.; Mathers, J.; Maka, A.; Srnak, A. Appl. Environ. Microbiol. 1985, 49 (2), 269–272. (23) Eisen, J. A.; Nelson, K. E.; Paulsen, I. T.; Heldelberg, J. F.; Wu, M.; Dodson, R. J.; Fraser, C. M. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (14), 9509–9514.

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Figure 7. Electrochemically active bacteria enrichment of the SCMFC with graphite granules as anode. The SCMFC was fed in continuous mode until a stable current output was obtained, and the electrochemically active bacteria were considered to be enriched and stabilized at the anode. Anode material: graphite granules. External resistance: 10 Ω. Feeding rate: 0.35 cm3 min-1. Loading rate: 0.67 kg COD m-3d-1. Fuel: sewage wastewater containing 1000 ppm of glucose. Inlet COD: 1180 ( 70 ppm.

Figure 6. Long-term stability of the SCMFC. Steady state current obtained during each month of the SCMFC operation. The SCMFC was fed in continuous mode with sewage wastewater after primary clarify. Inlet COD: 180 ppm. COD loading rate: 0.083 kg m-3 d-1. External load: 100 Ω. Anode material: graphite discs.

Geobacter sp., Rhodoferax ferrireducens, Bacillus licheniformis and Bacillus thermoglucosidasius.24-28 However, MFCs operated with mixed culture have previously demonstrated high stability in the face of perturbations, larger substrate versatility, and also higher power output when compared to MFCs using pure cultures.4,29 Chlorobium and Mesorhizobium species have not previously been identified as electro-active bacteria. However, on the basis of the DGGE profiles they constitute a large proportion of the anodic biomass. Given the high Coulombic efficiencies observed (64%, obtained shortly before the anodes were sampled) it would seem likely that one or both of these organisms have some role to play in anodic electron transfer. Stability. Figure 6 reports the current output generated by the SCMFC fed with a COD loading rate of 0.083 kg COD d-1 m-3 over a period of 5 months, during which the present study was conducted. As shown, during the first three months of operation the current output was very stable, with minimum variance (less than 0.04%). From the fourth month a decrease in current occurred, with a maximum reduction in the output current, after the fifth month, of approximately 22% with respect to the initial value. A gradual decrease in the performance of an MFC operating with wastewater in continuous mode was reported previously.30 This may result from clogging of the electrode and/or the PEM membrane. The reduced performance of the SCMFC could also be due to bacterial growth observed at the cathode side of the MFC from the fourth month of operation reducing mass transfer of oxygen to the cathode surface.

Figure 8. Polarization and current density curves from the SCMFC with a graphite granule anode. Anode material: graphite granules. Current density refers to the anode surface area: 1496 cm2 (0.15 m2). Power density refers to the anodic volume: 280 cm3. The polarization curves were recorded at a scan rate of 1 mV s-1 and a prior open circuit potential of over 4 h.

Effect of Anode Surface Area. In order to test the effect of anode surface area on the performance of the SCMFC, an alternative anode configuration was considered, which was obtained by using graphite granules. The granules increased the theoretical anode surface, from 89 to 1496 cm2 As shown in Figure 7, enrichment of the anode with electro-active bacteria required a much longer period than for the graphite discs. The lag characterized by minimal current lasted 18 days. An exponential increase of the output current followed and finally, after 20 days, the current output stabilized at 1.91 ( 0.029 mA, with a power density of 0.243 mW m-2 (130 mW m-3) and a Coulombic efficiency of 2.7 ( 1.12. The internal resistance was 10 Ω. The performances of the SCMFC with graphite granules was lower than that with the disk anode. After enrichment, the output current was 62% lower with respect to graphite discs, and the power was 86% lower.

(24) Biffinger, J. C.; Pietron, J.; Ray, R.; Little, B.; Ringeisen, B. R. Biosens. Bioelectron. 2007, 22, 1672–1679. (25) Kim, H. J.; Park, H. S.; Hyun, M. S.; Chang, I. S.; Kim, M.; Kim, B. H. Enzyme Microb. Technol. 2002, 30, 145–152. (26) Kim, B. H.; Kim, H. J.; Hyun, M. S.; Park, H. S. J. Mol. Microbiol. Biotechnol. 1999, 9, 127–131. (27) Rabaey, K.; Boon, N.; Siciliano, S. D.; Verhaege, M.; Verstraete, W. Appl. Environ. Microbiol. 2004, 70, 5373–5382. (28) Choi, Y.; Jung, E.; Park, H.; Paik, S. R.; Jung, S.; Kim, S. Bull. Kor. Chem. Soc. 2004, 25, 813–818. (29) Rabaey, K.; Lissens, G.; Siciliano, S. D.; Verstraete, W. Biotechnol. Lett. 2003, 25, 1531–1535. (30) Kim, M.; Youn, S. M.; Shin, S. H.; Jang, J. G.; Han, S. H.; Hyun, M. S.; Gadd, G. M.; Kim, H. J. J. Environ. Monitor. 2003, 5, 640–643.

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Table 5. Effect of the External Resistance on the SCMFC Performance with Graphite Granules As Anodea Rext (Ω)

steady-state voltage (mV)

steady-state current (mA)

steady-state power (mW)

COD removal rate (mg COD min-1)

Coulombic efficiency (%)

10 50 100 500 1000

19.1 ( 0.3 70 ( 0.99 132 ( 0.42 195 ( 1.88 270 ( 1.54

1.91 ( 0. 029 1.5 ( 0.014 1.32 ( 0.004 0.39 ( 0.0038 0.27 ( 0.0016

0.036 0.105 0.174 0.076 0.073

0.35 ( 0.02 0.3 ( 0.008 0.33 ( 0.012 0.31 ( 0.02 0.33 ( 0.04

2.7 ( 1.12 1.87 ( 0.13 1.61 ( 1.4 0.63 ( 0.08 0.35 ( 0.009

Loading rate: 0.55 kg COD m-3 d-1. Fuel: wastewater containing 1000 ppm of glucose. Inlet COD: 1180 ( 70 ppm. Anode surface area: 1496 cm2. Measurements of COD removal rate and coulombic efficiency from three replicates. a

Table 6. Effect of the Loading Rate on the SCMFC Performance with Graphite Granules As Anodea influent

COD loading rate (kg COD m-3 d-1)

current (mA)

COD removal (%)

Coulombic efficiency (%)

Power density (mW m-2)

WW diluted 1:2 WW WW þ 600 ppm of glucose WW þ 1000 ppm of glucose

0.07 0.099 0.43 0.67

1.4 ( 0.009 1.4 ( 0.05 1.34 ( 0.006 1.32 ( 0.004

58 ( 2.2 61 ( 3.0 80 ( 0.9 83 ( 3.3

28 ( 3 17.7 ( 0.8 3.06 ( 1.1 1.61 ( 1.4

1.31 1.31 1.20 1.16

a

Rext = 100 Ω. Fuel: wastewater (WW) characterized by several input CODs. Power density referred to the anode surface area (0.15 m2).

The reduced performance of the SCMFC with graphite granules was confirmed by the polarization and power density curves reported in Figure 8. The peak power density was, in fact, of 1.36 mW m-2 (730 mW m-3), approximately 40 times lower than the case of graphite discs. The OCV was of around 0.46 V, very similar to that with the graphite discs. The cell voltage variation (Vcell, Figure 8) in the SCMFC with the graphite pellet anode exhibited a typical fuel cell polarization curve with a relatively rapid voltage loss at low current density, followed by a second phase of linear voltage drop. Consequently, the anode voltage was characterized by a rapid increase at low current density as opposed to a slow initial increase of Van in the case of graphite discs. The change in the cathode potential over the current density range was similar for both MFCs using either graphite discs or granules. The polarization behavior of the cathode in the cells using both anodes was effectively the same. The graphite granule packed bed gave currents approximately half those obtained with the disk stack cell. The major difference in performance was caused by the different anode configurations; noting that the internal resistance with the graphite granule packed bed anode was lower than that with the disk anode. The effect of external resistance on the performance of the SCMFC with graphite granules was investigated (Table 5). The external load was changed from 10 to 1000 Ω, and the current output evaluated. With the graphite granules the highest power of 0.17 mW was reached at an external load of 100 Ω, which compares with 0.484 mW for the graphite disk cell. The COD removal rate did not change with the external load and therefore the Coulombic efficiency decreased with the current, that is, higher external resistance corresponded to lower Coulombic efficiency, as observed for the graphite discs anode. The values of Coulombic efficiencies were in general very low, meaning that a large amount of COD removed did not contribute to energy production. These values were lower than values obtained with graphite discs at the corresponding external load. The effect of the organic loading rate was also investigated (Table 6). Lower COD loading rates led to higher Coulombic efficiency, and the highest value was 28 ( 3%. On the other hand, COD removal was improved: at 100 Ω and for a WW

dilution of 1:2, the COD removal increased by approximately 42% for the anode made with graphite discs. However the best removal was still reached when the system was fed with easily biodegradable organic matter, that is, glucose. Discussion The water treatment business is fairly mature in the developed world. Europe represents around one-third of the world’s environmental market and is driven by the European Union (EU) environmental regulations that are among the toughest in the world. The total European municipal water and wastewater treatment market has a compound annual growth rate of 4.1% per year and is estimated to reach a value of $ 3.09 billion in 2010. It is estimated that wastewater treatment is growing at about 7% globally per year, and every day it requires large amounts of energy. Most of the plants rely on biological methods for secondary treatment, and these are generally based on aerobic processes. Considering a standard organic loading rate in the range of 0.07-0.22 kg BOD m-3 d-1, aerobic treatments require approximately (2-4)103 kWh m-3 every day with BOD removal efficiencies in the range of 80-90%.31 As supplies of fossil fuels dwindle and concerns about anthropogenic contributions of carbon dioxide to the atmosphere intensify, there is an increasing trend toward the use of new sources of energy from renewable carbon-neutral sources with minimal negative environmental impact. In addition to conventional anaerobic treatments, microbial fuel cells represent a potential, alternative, low energy wastewater treatment system. Yet, to enhance their practical applicability in wastewater treatment, it is important to focus on implementing systems that can be easily scaled up, work in continuous mode, and are fed with real wastewater instead of pure compounds. In this study we analyzed the performance of an up-flow SCMFC fed with real wastewater after primary clarification. Although platinum was still used as a catalyst at the cathode, we tested a very cost-effective polypropylene/silicate membrane, which is usually used as a separator in lead acid batteries. The performance of the MFC was analyzed in terms (31) Metcalf, L.; Eddy, H. P., Wastewater Engineering: Treatment and Reuse, fourth ed.; MacGraw-Hill Companies: New York, 2003.

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of COD removal, current and power output, and energy recovery. The maximal power density generated was 59 mW m-2, if defined with respect to the anode surface area, or 1.5 W m-3, if defined with respect to the anode chamber volume. Higher power outputs have been previously reported for an MFC.8 However, a direct comparison of the performance with previous studies is difficult because of differences in the anode configuration and reactor volume. The system used in this work has the advantage of being relatively easily scaled up, although the use of platinum as catalyst still represents a big obstacle. Recently, in our research group we have successfully tested manganese oxide as cathode catalyst in the MFC.9 A next step could be therefore to investigate the performance of the SCMFC of this study with manganese oxide as catalyst. Another attractive alternative to platinum catalysis of oxygen reduction at the cathode is the use of biocathodes.13,14 In the treatment of wastewater, the COD loading rate was a key factor in the performance of the SCMFC: lower organic loadings gave higher Coulombic efficiency with a maximum of 63.4 ( 4.2% when the system was fed with 0.055 kg COD m-3 d-1, meaning that the electro-active biofilm was responsible for the majority of the COD removal. Working at low external resistances has been shown to reduce methanogenesis,32 presumably by allowing more efficient oxidation of the organic carbon by the electrogenic bacteria, allowing them to out compete methanogens. However, it was also demonstrated that, even at low external resistances, at higher organic loading rates, the Coulombic efficiency was reduced; with organic carbon oxidation being channelled through methanogenesis possibly being responsible, aside from increased potential losses.19 High COD loadings, corresponding to highly saturated conditions with respect to anode surface area may lead to competition among bacteria involved in the electricity production and other types of bacteria, thus leading to greater amount of COD removal not related to current generation and, consequently, to low Coulombic efficiencies. When the fuel concentration decreased, the conditions became more restrictive for the other bacteria and the electrochemically active bacteria were at an advantage. The hypothesis of saturation conditions for high loading rates was supported by the fact that the current output did not decrease with the loading rate until a value of 0.08 kg COD m-3 d-1, or less, was used. Switching from pure wastewater to wastewater diluted 1.3 times caused a current decease of only 20%. Coulombic efficiencies as high as 89% have been reached with pure compounds such as glucose;29 but 63% is the highest efficiency reported so far for MFCs fed real wastewater.8 On the other hand, the percent COD removal was very low if compared, for example, with treatment performed with UASB reactors. By decreasing the flow rate to 0.18 cm3 min-1, the percent COD removal increased by 60%. This rate represents the best compromise between treatment efficiency and energy recovery (57% Coulombic efficiency), but implies a HRT of approximately 102 h. In contrast, with UASB reactors operating at loading rates one thousand-fold higher (12-20 kg COD m-3 d-1 compared to 0.028 kg COD m-3 d-1), HRTs as low as 4-8 h can be used.31 These HRTs can be further decreased when less than 90% COD removal and

higher-effluent TSS concentration are acceptable. This higher loading rate in the UASB reactor can only be applicable for high strength wastewater. For wastewater having COD less than 1000 mg/L, the loading generally used for this design is less than 3 kg COD/(m3 d) due to hydraulic loading limitations. The utilization of an alternative anode configuration based on graphite granules led to a better treatment of the wastewater but did not improve the performance of the SCMFC with regard to the current and power output. These parameters decreased, even though the surface area of the anode was markedly increased. The optimal external resistance was 100 Ω for both anode configurations, and the highest Coulombic efficiency was again found at low COD loading rates. Nevertheless, the power output was approximately three times lower with the graphite granule anode compared to the graphite disk anode (0.17 mW vs 0.484 mW), and the maximum Coulombic efficiency was only around 28%. One of the reasons for the difference in performance of the MFC with graphite granules compared with that for graphite discs was due to the variation in current distribution in the cell. It is known that in porous electrode structures, higher currents are experienced at the surface nearer to the cathode and the current densities fall as the distance increases from the cathode. Eventually, with relatively thick beds the current near to the current collector can be low and near zero. Thus, the actual effective area of the anode is not the actual surface area because of this nonuniform current distribution. The effective area that is used will tend to decrease as higher currents are imposed and will fall with a decrease in fluid ionic conductivity and with thicker granular beds. In comparison, the variation in the current density distribution on the disk anode surfaces would be smaller and thus most of the available surface area would be used.33 Thus, for granular porous electrodes or similar geometries there is in fact an “optimum” thickness beyond which little improvement in power performance can be achieved. Modeling current distribution in anodes with different configurations will be vital for the design of effective MFCs. Overall, the results obtained here may be due to a combination of the anode characteristics, bacterial activity and growth, and the effective surface area of the anode exposed to the feed. On one hand, the granules lead to a better contact between the biofilm and the bulk solution resulting in higher COD removal. On the other hand, the shape of granules and bed porosity allow only a small fraction of their total surface to be connected, resulting in lower current output. Our results demonstrated that even if graphite granules increase the surface area for anodic biofilm formation, they may not be suitable for implementation of the SCMFC in real wastewater treatment. On account of the high COD removal reached when glucose was added to the influent, pretreatment of wastewater prior to MFC treatment could be considered, in order to increase the concentration of easily biodegradable organic compounds. However, the total energy recovery and treatment efficiency should be able to justify the extra expenses related to the pretreatment. An interesting option would be to consider MFC and anaerobic digestion as two complementary technologies and integrate them in a treatment plant, as previously suggested.11

(32) Rabaey, K.; Boon, N.; Siciliano, S. D.; Verhaege, M.; Verstraete, W. Appl. Environ. Microbiol. 2004, 70, 5373–5382.

(33) Scott, K. Electrochemical Reaction Engineering; Elsevier Academic Press: London, 1991.

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The plant would include a prior anaerobic digestion to treat high COD effluent and a secondary treatment based on MFC to remove the residual organic carbon. Stacked microbial fuel cells could represent a good option to increase the anodic volume. It was recently shown that stacked configuration can lead to high current and power output.34

of the SCMFC: lower organic loadings gave higher Coulombic efficiency with a maximum of 63.4 ( 4.2% when the system was fed with 0.055 kg COD m-3 d-1, meaning that the electro-active biofilm was responsible for the majority of the COD removal. When an alternative anode configuration made of graphite granules was analyzed, a better treatment of the wastewater was reached, but the electro-chemical performance of the SCMFC decreased with a power output approximately three times lower compared to the graphite disk anode (0.17 mW vs 0.484 mW), and the maximum Coulombic efficiency was only of 28% .

Conclusions This study investigate the performance of a SCMFC, with air cathodes surrounding a series of graphite discs anodes. The air cathode was supported on a low-cost polypropylene/silica composite membrane. The system was operated in continuous mode and fed with wastewater from the primary clarifier of a wastewater treatment plant. In the treatment of the wastewater, the COD loading rate was a key factor in the performance

Acknowledgment. This work was supported by the European Union for Transfer of Knowledge award on biological fuel cells (contract MTKD-CT-2004-517215) and Northumbria Water. We thank Northumbria Water for providing anaerobic sludge and wastewater from the primary clarifier from Cramlington WWTP. We thank Entek for supply of the RhinoHide membrane.

(34) Aelterman, P.; Rabaey, K.; Pham, T. H.; Boon, N.; Verstraete, W. Environ. Sci. Technol. 2006, 40 (10), 3388–3394.

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