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Water Research 39 (2005) 49614968 www.elsevier.com/locate/watres

Electricity generation from swine wastewater using microbial fuel cells

Booki Mina, JungRae Kima, SangEun Oha, John M. Regana,b, Bruce E. Logana,b,
a

Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, PA 16802, USA b The Penn State Hydrogen Energy (H2E) Center, The Pennsylvania State University, University Park, PA 16802, USA Received 27 June 2005; received in revised form 26 September 2005; accepted 28 September 2005

Abstract Microbial fuel cells (MFCs) represent a new method for treating animal wastewaters and simultaneously producing electricity. Preliminary tests using a two-chambered MFC with an aqueous cathode indicated that electricity could be generated from swine wastewater containing 83207190 mg/L of soluble chemical oxygen demand (SCOD) (maximum power density of 45 mW/m2). More extensive tests with a single-chambered air cathode MFC produced a maximum power density with the animal wastewater of 261 mW/m2 (200 O resistor), which was 79% larger than that previously obtained with the same system using domestic wastewater (14678 mW/m2) due to the higher concentration of organic matter in the swine wastewater. Power generation as a function of substrate concentration was modeled according to saturation kinetics, with a maximum power density of Pmax 225 mW=m2 (xed 1000 O resistor) and half-saturation concentration of K s 1512 mg=L (total COD). Ammonia was removed from 19871 to 3471 mg/L (83% removal). In order to try to increase power output and overall treatment efciency, diluted (1:10) wastewater was sonicated and autoclaved. This pretreated wastewater generated 16% more power after treatment (11074 mW/m2) than before treatment (9674 mW/m2). SCOD removal was increased from 88% to 92% by stirring diluted wastewater, although power output slightly decreased. These results demonstrate that animal wastewaters such as this swine wastewater can be used for power generation in MFCs while at the same time achieving wastewater treatment. r 2005 Elsevier Ltd. All rights reserved.
Keywords: Microbial fuel cell; Electricity; Swine wastewater; Animal wastewater; Power generation

1. Introduction Large volumes of high-strength wastewaters are produced annually from industrial and agriculture operations. For example, it is estimated that 5.8 107 tons of animal manures are generated each
Corresponding author. Department of Civil and Environ-

mental Engineering, The Pennsylvania State University, University Park, PA 16802, USA. Tel.: +1 814 863 7908. E-mail address: blogan@psu.edu (B.E. Logan).

year in the US alone (Dentel et al., 2004). The animal wastewater must be treated to meet discharge regulations prior to being released into the environment (Suzuki et al., 2002; Maekawa et al., 1995) to avoid water contamination and odor problems (Luo et al., 2002; Westerman et al., 2000). High concentrations of nitrate (NO) and phosphate in wastewater can also contribute 3 to water pollution through eutrophication of surface water (Luo et al., 2002; Ra et al., 2000). Many treatment techniques have been proposed to remove inorganic or organic pollutants from wastewater, but these processes

0043-1354/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2005.09.039

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entail high operational costs or large amounts of land for treatment (Sevrin-Reyssac, 1998). One approach to offset the costs of industrial and animal wastewater treatment is to generate useful amounts of bioenergy, such as hydrogen or methane gas, from the organic matter in the wastewater while at the same time accomplishing treatment (Logan, 2004; Angenent et al., 2004; Rabaey and Verstraete, 2005). Food processing wastewaters have been tested for biological hydrogen production using fermentative bacteria in several types of processes (Das and Veziroglu, 2001; Yu et al., 2002; Oh and Logan, 2005; Van Ginkel et al., 2005). However, these processes have not been widely used due to low energy recovery from the organic matter (1.42.5 mole of hydrogen per mole of hexose) and high operational costs (Logan, 2004; Angenent et al., 2004; Oh and Logan, 2005). Microbial fuel cells (MFC) have been developed that can generate electricity directly from marine sediments, anaerobically digested sludge, food wastewaters, and domestic wastewater. The amount of power produced varies depending on the type of reactor and the specic source of the organic matter. In laboratory and eld tests, 1025 mW/m2 (power normalized to the projected surface area of the anode) is produced with sediment fuel cells when the anode is placed into an anaerobic marine sediment and the cathode is in the overlying seawater containing dissolved oxygen (Reimers et al., 2001; Bond et al., 2002; Delong and Chandler, 2002; Tender et al., 2002). Using a single-chambered MFC conguration (Liu et al., 2004; Liu and Logan, 2004; Min and Logan, 2004), up to 26 mW/m2 (maximum power density) was generated using domestic wastewater (initial chemical oxygen demand (COD) of 200300 mg/ L) while at the same time removing up to 80% of the COD (Liu et al., 2004). A at plate MFC generated 7271 mW/m2, but under conditions that achieved only 42% COD removal (Min and Logan, 2004). Liu and Logan (2004) generated a maximum of 14678 mW/m2 using wastewater with a single-chambered air-cathode MFC operated in batch mode operation. In only a few cases has there been a direct comparison of a single wastewater with different types of MFCs. For example, it was shown using a food processing wastewater that power could be increased from 8177 to 371710 mW/ m2 by using a single-chambered MFC instead of a twochambered MFC (Oh and Logan, 2005). Animal wastewaters should provide a good source of organic matter for electricity production using an MFC, but so far this type of wastewater has not been examined for electricity production (Logan, 2004). Potential problems that could interfere with electricity generation in a MFC relate to those that can affect other anaerobic processes such as methane production: toxicity due to the high concentrations of ammonia in the wastewater or to volatile acids produced during hydrolysis and

fermentation of the substrates (Rittmann and McCarty, 2001). In this study, we demonstrate for the rst time that it is possible to produce electricity directly from swine wastewater using a MFC, while at the same time accomplishing wastewater treatment. Preliminary tests were conducted using an aqueous cathode, two-chambered MFC to demonstrate the feasibility of treatment and for comparison of power densities achieved using other substrates. More extensive tests were then conducted using an air-cathode, single-chambered MFC that is known to produce more power than the two-chambered system (Liu and Logan, 2004; Oh et al., 2004). Power output was examined as a function of circuit load (resistance), wastewater strength, and pretreatment by sonication of the wastewater. In addition, we examined ammonia and phosphate concentrations in the raw and treated wastewater.

2. Materials and methods 2.1. Animal wastewater Swine wastewater was collected from the Pennsylvania State University Swine Farm (University Park, PA) and kept in a refrigerator at 4 1C before use. The wastewater was used as the inoculum for all MFC tests without any modications such as pH adjustments or addition of nutrients or trace metals. Tests were conducted using full-strength wastewater, except as indicated, when the wastewater was diluted using ultrapure water (Milli-Q system; Millipore Corp., New Bedford, MA), autoclaved, or sonicated (Sonier 450; Branson Ultrasonic Co., CT; output control 7, duty cycle 40%). 2.2. MFC conguration and operation All experiments were conducted using MFCs operated in fed-batch mode in a temperature-controlled room (30 1C). A two-chambered MFC was used in initial tests that contained two electrodes (anode and cathode), each in a separate bottle (310 mL capacity, Corning Inc. NY, USA). Each bottle was lled to 250 mL with wastewater for the anode and phosphate buffer solution (pH 7; 2.75 g/L Na2HPO4+4.22 g/L NaH2PO4 H2O) for the cathode as previously described (Min et al., 2005). The two bottles were connected with a glass tube (total length 8 cm; inner diameter 1.3 cm) with a proton exchange membrane (NaonTM 117, Dupont Co., Delaware, USA) held by a clamp in the middle of the tube. The electrodes (2.5 4.5 cm each) were made of a carbon paper (E-Teck) and connected via an external circuit containing a single resistor (R 1000 O, except as noted). One side of the cathode was coated with a catalyst (0.35 mg-Pt/cm2). The cathode chamber was

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continuously aerated at 30 mL/min to provide dissolved oxygen at the cathode. Most tests were conducted using a single-chambered MFC containing an air cathode, with liquid contained inside a cylinder 4 cm long and 3 cm diameter chamber (28 mL empty bed volume) as previously described (Liu et al., 2004). The anode and cathode electrodes were located on the opposite sides of the chamber, and the reactor lacked a proton exchange membrane (PEM). The electrodes were made of the same materials as those used in the two-chambered system except a stainless steel wire was used for connecting the electrodes (by compression) to an external circuit. In some experiments, the side of the cathode facing the air was coated with polytetrauoroethylene (designated as a PTFE cathode) in order to reduce evaporation of water through the cathode. This electrode was prepared by applying a PTFE solution (50% by weight), drying at room temperature for 10 min, and then heating for 10 min at 380 1C. 2.3. Analysis Total and soluble (ltered) COD of wastewater were measured in duplicate (except as noted) using Standard Methods (method 5220; HACH COD system, HACH Company, Loveland, CO.; American Public Health Association, American Water Works Association, Water Pollution Control Federation, 1995). All samples for soluble COD (SCOD) were ltered through a 0.45 mm pore diameter syringe lter, while total COD (TCOD) measurements were conducted without treatment. Measurements on inorganic compounds were made in duplicate using procedures based on Standard Methods (American Public Health Association, American Water Works Association, Water Pollution Control Federation, 1995) for ammonia (Salicylate method), phosphate (PhosVer 3 method), nitrate (Cadmium reduction method), and nitrite (Diazotization chromotropic acid method) (HACH). The cell voltage across a resistor was measured using a multimeter, and all data were automatically recorded by a computer and a data acquisition system (2700, Keithly). Power density, P (W/m2), was obtained according to P IV =A, where I (A) is the current, V (V) is the voltage, and A (m2) is the projected surface area of the anode. The Coulombic efciency (CE) was calculated based on current generation and the amount of substrate removal during a MFC operation (Liu et al., 2004; Oh et al., 2004; Min and Logan, 2004). The maximum power density was determined by adding fresh substrate to the MFC and establishing constant power, and then varying the external resistance over a range of 2400 KO and recording the voltage (typically 510 min per resistor). The power was then calculated for each resistance as a function of the current.

3. Results and discussion 3.1. Power generation from swine wastewater using a two-chambered MFC Preliminary experiments conducted using a twochambered MFC demonstrated that electricity could be generated using swine wastewater, and that the bacteria needed were already present in the wastewater. When non-diluted swine wastewater was added into the two-chambered MFC, a circuit voltage of 2072mV (7SD, n 90; 853 h) was immediately generated within only a few hours (Fig. 1A). This initial voltage might have been due to both chemical and biological factors based on the difference of the potential between the two chambers. Thereafter, the voltage rapidly increased due to biological activity, and stabilized at 12671 mV (n 114) over the following 47 h period (83140 h), resulting in a power density of 7.170.2 mW/ m2 (R 1000 O) for this rst inoculation of the MFC with wastewater.

150 120 Voltage, mV 90 60 30 0 0 (A) 60 Power density, mW/m 50 40 30 20 200 10 0 0 (B) 50 100 150 200 250 2 Current density, mA/m 300 0 400
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50 Time, hr

100

150

800 600 Voltage, mV

Fig. 1. Voltage generation (A) with full-strength animal wastewater in a two-chambered MFC (1000 O). Voltage and maximum power generation (B) as a function of current density obtained by varying the external circuit resistance from 4 O to 400 KO.

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3.2. Power generation using a single-chambered MFC To demonstrate the potential for greater power densities using animal wastewater, all further tests were conducted with a single-chambered MFC. Acclimation required more time with the single-chambered MFC (114 h) than the two-chambered MFC (data not shown). After two cycles of replacing the wastewater over 80 h, the voltage reached a stable value of 35771 mV (1000 O), producing a maximum power density of 18271 mW/m2 with the swine wastewater (Fig. 2A). Over a period of 44 h, the SCOD decreased by 27%, or from 83207190 to 6090760 mg/L (triplicate measurements). The CE for this measured COD removal was 8%. This CE is quite low, even compared to a value of CE 20% obtained in tests with domestic wastewater for this MFC (Liu and Logan, 2004). The maximum power density for the single-chambered MFC was 261 mW/m2 (200 O, 1.4 A/m2; Fig. 2B). This maximum power density is nearly 6 times that obtained using the two-chambered system. The observation that power density is much larger using the singlechambered than a two-chambered MFC is consistent with previous studies. For example, the maximum power density achieved using acetate in this two-chambered system was 43 mW/m2 (Oh et al., 2004), while the same substrate produced a maximum power density of 506 mW/m2 in a single-chambered MFC (Liu et al., 2005a) under high substrate (saturation) conditions. This difference in the maximum power density for these two MFC systems when the same substrate is used is a result of the different internal resistances of the systems (Min et al., 2005). The maximum power density with different substrates varies for the single-chambered MFC, indicating that the type of substrate can affect power output in this type of MFC. In previous tests using the same MFC,

(B)

Fig. 2. (A) Power and voltage generation using full-strength wastewater in a single-chambereded MFC (1000 O) following a 200-h acclimation period. (B) Power density and voltage as a function of current density obtained using external resistors of 2 O to 200 KO.

maximum power densities of 494 and 506 mW/m2 were obtained using readily biodegradable substrates of glucose and acetate (Liu and Logan, 2004; Liu et al., 2005a). However, power output was lower using butyrate (305 mW/m2), and decreased further for domestic wastewater (146 mW/m2). These results demonstrate that the substrate, and perhaps the bacterial community that developed during acclimation, affected microbial kinetics and therefore the maximum power density achievable with the swine wastewater.

3.3. Power generation as a function of wastewater concentration Power generation was measured as a function of wastewater concentration to determine if the concentration of organic matter in the wastewater was limiting power generation. The TCOD concentration of the wastewater was varied by dilution from 49471 to 44707440 mg/L (SCOD range of 359732840750 mg/ L). The maximum power density obtained with a xed external resistance (1000 O) showed a saturation-type

Voltage, mV

After replacing the anode chamber solution four times, we obtained a consistent and repeatable cycle of power generation with non-diluted swine wastewater. By varying the circuit resistance, it was determined from a polarization curve that the maximum power that this system could produce was 45 mW/m2 (141 mA/m2) at 1000 O (Fig. 1B). This maximum power output is similar to that obtained using this same two-chambered system in several other studies using acetate (38 mW/m2, Min et al., 2005; 43 mW/m2, Oh et al., 2004; 40 mW/m2, Kim et al., 2005) or cysteine (39 mW/m2, Logan et al., 2005). The observation that a similar maximum power output was achieved with several different substrates is consistent with previous ndings that power generation in this two-chambered MFC used by our research group is limited by internal resistance and not by the power that can be produced by bacteria with specic substrates (Min et al., 2005).

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relationship with respect to wastewater concentrations (Fig. 3). The maximum power density at this resistance was Pmax 225 mW=m2 , with a half-saturation concentration of K s 1510 mg=L (TCOD). The nding of a saturation-type relationship for power output as a function of substrate concentration is consistent with other studies using acetate or butyrate as a substrate in this single-chambered MFC (Liu et al., 2005a). The CE of substrate removal was determined by measuring the TCOD and SCOD of the solutions after the voltage decreased to less than 100 mV ($14 mW/m2). The CEs measured at each substrate concentration decreased from 26% to 10% with an increase in wastewater concentration (Fig. 3). This inverse relationship between CE and substrate concentration is similar to that observed by Liu et al. (2005a). They found that the CE decreased from 28% to 13% (R 1000 O) using acetate in the same type of MFC, when substrate concentration increased from 80 to 800 mg/L. It is thought that part of this relationship between CE and substrate concentration is due to the effect of oxygen transfer into the system through the cathode. The higher the substrate concentration the longer the period of time needed to fully degrade the substrate. As the time period increases, more oxygen can leak into the system causing aerobic removal of the substrate, and lowering the overall CE. Substrate can also be removed using alternate electron acceptors, for example through sulfate reduction, heterotrophic denitrication, and methanogenesis. 3.4. Other factors affecting power generation Several other factors were examined with respect to power output, including wastewater pretreatment by

sonication or autoclaving, and stirring the wastewater. It was hypothesized that there would be relatively less electricity generation from the particulate organic matter than from the soluble organic matter due to slower degradation kinetics for particulate material (Bougrier et al., 2004) and the limited diffusion of the particulate material into the biolm to the electrode surface, where the electrochemically active bacteria are located. For example, sonication has been shown to increase biogas production in anaerobic digestors (Tiehm et al., 2001; Bougrier et al., 2004). To decrease the time needed to fully degrade the biodegradable material in the sample during an experiment, the wastewater was diluted (1:10). Sonication (20 min) increased the SCOD of diluted wastewater by 19%, or from 1300740 to 1550780 mg/ L, but did not change the total COD (1940780 mg/L). The increase in the SCOD came from the solids, as indicated by a decrease in TSS from 250750 to 74725 mg/L. When the sonicated and original diluted wastewaters were used in MFC tests, there was essentially no change in the maximum power density. The sonicated wastewater produced a maximum power density of 10575 mW/m2 (829 h), while the untreated wastewater produced 10174 mW/m2 (532 h) (Fig. 4). COD removals using the sonicated animal wastewater were 85% for the TCOD and 91% for SCOD (after 72 h operation; nal TCOD 290720 mg/L and SCOD 140720 mg/L), while those for the untreated wastewater were 89% and 90% (nal TCOD 220740 mg/L; SCOD 130710 mg/L), respectively. The CE for the sonicated wastewater was 6.8%, while that for the untreated wastewater was 7.2%. Given that these differences are in general quite small, wastewater sonication

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Power density, mW/m

Power density, mW/m

30 25 20 15 10 5 1000 2000 3000 4000 5000 Initial TCOD concentration, mg/L

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Fig. 3. Power density (K) and Coulombic efciency (CE; &) as a function of initial TCOD concentrations for animal wastewater in a single-chambereded MFC (PTFE cathode; 1000 O).

Fig. 4. Power generation from sonicated animal wastewater (AW; diluted by 1/10) in a single-chambereded MFC (PTFE cathode; 1000 O).

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alone does not appear at this time to be a useful way to increase power densities or COD removals in MFCs. Autoclaving the wastewater was also examined as a method of treatment to increase power generation in the MFC. Autoclaving the wastewater can kill anaerobic bacteria, such as methanogens, that can result in a loss of organic matter in a manner that does not generate electricity. The maximum power density with the autoclaved wastewater (82 or 84 mW/m2) in two tests was not appreciably different than that obtained with raw wastewater (77 or 79 mW/m2) (Fig. 5). The CE with the autoclaved wastewater was slightly lower (17%), but not substantially different from that with the raw wastewater (20%). Thus, autoclaving alone is insufcient to appreciably alter power generation in the MFC. The average power density of 11074 mW/m2 (330 h) for the sonicated and autoclaved diluted wastewater was signicantly higher (p valueo0.001, t-test) than that of raw wastewater (9674 mW/m2; 526 h) (Fig. 6). Thus, the combined pre-treatment of autoclaving and sonicating the wastewater increased power generation by 16%. The reasons for this increase could include changes in biodegradability of the organic matter, and changes in the molecular weight or particle size spectra of the organic matter. While power densities can be increased by these two processes, however, it is not likely that such pretreatment could be economical due to the high energy input needed for both processes. Another factor that was investigated to improve reactor performance was stirring the wastewater. It has been shown that slow proton transfer between the anode and cathode can limit power generation (Liu et al., 2005b). It was therefore speculated that stirring the water might increase power density due to enhancing proton transport

to the cathode, and substrate transport to the anode. It was found, however, that power generation decreased as a result of stirring. The maximum power density was signicantly (po0:001, t-test) larger in the system without stirring (12873 mW/m2; 827 h) than in the system with stirring (11872 mW/m2; 826 h) (Fig. 7). While the reason for this change is not known, stirring may have decreased the concentration gradient of volatile acids in the biolm produced from hydrolysis and fermentation of the organic matter. Alternatively, stirring might also have increased

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Raw AW Sonicated and autoclaved AW

120 100 80 60 40 20 0 0 30 60 90 Time, hr 120 150

Fig. 6. Power generation from sonicated and autoclaved animal wastewater (AW; diluted by 1/10) in a single-chambered MFC (PTFE cathode; 1000 O).

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Fig. 5. Power generation using autoclaved and raw animal wastewater (AW; diluted by 1/10) in a single-chambered MFC (1000 O; non-PTFE cathode).

Fig. 7. Power generation using animal wastewater (diluted by 1/10) in a single-chambered MFC with and without stirring (PTFE cathode; 1000 O).

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the oxygen ux into the reactor by affecting the resistance to oxygen mass transfer at the cathode, resulting in an increase in the redox potential of the anode chamber, but this situation was not examined further. Consistent with this explanation, COD removal was increased when the solution was stirred (90% TCOD and 92% SCOD removal with stirring; 89% TCOD and 88% SCOD removals without stirring; Fig. 7) while the CE with stirring (5%) was also less than that (8%) without stirring. 3.5. Nitrogen and phosphate concentrations during MFC treatment Ammonia, nitrite, nitrate and phosphate concentrations were examined to determine the effect of MFC treatment on these parameters. After 100 h operation using diluted (1:10) wastewater, ammonia was removed by 8374% (from 19871 to 3470 mg NH4-N/L) when the SCOD was reduced from 1240720 to 120730 mg/L (8676% removal). The high removals observed here for a reactor operating under anaerobic conditions was surprising. Nitrite and nitrate concentrations increased from 0.470.1 to 2.970.1 mg NO2-N/L and 3.871.2 to 7.570.1 mg NO3-N/L. This increase in oxidized nitrogen suggests that nitrication was occurring, likely as a result of oxygen diffusion through the cathode. Oxygen diffusion through the cathode is known to result in a loss of carbonaceous substrates to aerobic degradation, as evidenced by low CE in MFCs (Liu and Logan, 2004). The total amount of ammonia removal (164 mg NH4-N/ L) was much larger than the corresponding increases in nitrite (2.5 mg NO2-N/L) and nitrate (3.7 mg NO2-N/L). The low CE and low concentrations of nitrate and nitrite suggest additional nitrogen removal through several possible routes including denitrication, anaerobic ammonia oxidation (anammox) (Rittmann and McCarty, 2001; Dong and Tollner, 2003), nitrite reduction by lithotrophic ammonia oxidizers (Zart and Bock, 1998), or by some previously unobserved method of ammonia oxidation coupled to electricity generation. Further work is needed to better understand the process by which nitrogen is removed in this MFC. Orthophosphate concentrations (PO4-P mg/L) did not decrease, and may have slightly increased (4171487 1 mg/L) during the reactor test cycle. The increase in orthophosphate concentration could have been a result of the low redox potential in the MFC which would stimulate the release of stored phosphates in the bacteria (Luo et al., 2002), or the conversion of organic phosphorus in the wastewater to orthophosphate.

maximum power density using a two-chambered MFC was 45 mW/m2, while 6 times more power (261 mW/m2) was generated using a single-chambered system, although the CE was low (8%). Power generation showed a saturation-type relationship with wastewater concentration, with a half-saturation concentration constant of K s 1510 mg=L (TCOD). The combined pre-treatment of sonication and autoclaving the wastewater generated 16% more power (11074 mW/m2) than that produced using a raw diluted wastewater (9674 mW/m2). Stirring the wastewater in the MFC reduced the power density. Electricity generation was accompanied by 8676% removal of COD and 8374% removal of NH4-N. However, phosphate concentrations increased by 17% during treatment. These results demonstrated the feasibility of using MFC technologies to generate electricity and simultaneously treat swine wastewaters, although additional studies are needed to scale up and optimize the process.

Acknowledgments This research was supported by the Natural Resources Conservation Service of the United States Department of Agriculture (63-3A75-3-150), the National Science Foundation (BES 0331824), and the Paul L. Busch Award from the Water Environment Research Foundation (to BEL).

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4. Conclusions Electricity was generated using swine wastewater, at a power density that depended on the type of MFC. The

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