ARTICLE Energy From Algae Using Microbial Fuel Cells

Sharon B. Velasquez-Orta,1 Tom P. Curtis,1 Bruce E. Logan2 School of Civil Engineering and Geosciences, Newcastle University, Newcastle upon Tyne NE17RU, United Kingdom; telephone: 44-191-222-6415; fax: 44-191-222-6502; e-mail: s.b.velasquez-orta@ncl.ac.uk 2 Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, Pennsylvania 16802
Received 3 December 2008; revision received 19 February 2009; accepted 27 March 2009 Published online 3 April 2009 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/bit.22346
1

ABSTRACT: Bioelectricity production from a phytoplankton, Chlorella vulgaris, and a macrophyte, Ulva lactuca was examined in single chamber microbial fuel cells (MFCs). MFCs were fed with the two algae (as powders), obtaining differences in energy recovery, degradation efciency, and power densities. C. vulgaris produced more energy generation per substrate mass (2.5 kWh/kg), but U. lactuca was degraded more completely over a batch cycle (73 1% COD). Maximum power densities obtained using either single cycle or multiple cycle methods were 0.98 W/m2 (277 W/m3) using C. vulgaris, and 0.76 W/m2 (215 W/m3) using U. lactuca. Polarization curves obtained using a common method of linear sweep voltammetry (LSV) overestimated maximum power densities at a scan rate of 1 mV/s. At 0.1 mV/s, however, the LSV polarization data was in better agreement with single- and multiple-cycle polarization curves. The ngerprints of microbial communities developed in reactors had only 11% similarity to inocula and clustered according to the type of bioprocess used. These results demonstrate that algae can in principle, be used as a renewable source of electricity production in MFCs. Biotechnol. Bioeng. 2009;103: 10681076. 2009 Wiley Periodicals, Inc. KEYWORDS: microbial fuel cell; algae; bioenergy; substrate composition; polarization

Introduction
The concern about global warming effects and fossil fuel costs has encouraged the search for alternative sources of energy (Brecha, 2008). Biomass products tested for energy generation include a wide range of growth plants, crops and
Correspondence to: S.B. Velasquez-Orta Contract grant sponsor: Consejo Nacional de Ciencia y Technologia (CONACyT) Contract grant number: 196298 Contract grant sponsor: National Science Foundation Contract grant number: CBET-0730359 Contract grant sponsor: King Abdullah University of Science and Technology (KAUST) Global Research Partnership Contract grant number: KUS-I1-003013

wastes (Deublein and Steinhauser, 2008). In this context, algae are seen as an alternative to land based alternatives. The cultivation of algae has several advantages over terrestrial plants; they require less space (1/7th less surface area), have higher growth rates, and do not compete with food production (Hartman, 2008). Algae are divided into two groups: phytoplankton (microalgae), or macrophytes (macroalgae). Microalgae are unicellular green plants rich in chlorophyll that lack lignin or cellulose, and contain proteins, carbohydrates and lipids in strain-specic proportions (Schenk et al., 2008). They are abundant in oceans, suitable for cultivation in rivers, and serve as the primary source of carbohydrates and proteins for aquatic organisms. Macroalgae are more resistant to predators and environmental conditions than microalgae. They are abundant in costal zones (Riegman et al., 1993), lack lignin, and largely consist of polysaccharides (alginate, laminaran, and mannitol) and unsaturated fatty acids which are easily hydrolyzed, and low concentrations of cellulose (Vergara ndez et al., 2008). Both macrophytes and phytoFerna plankton are suitable for cultivation using river water, sea water, and some wastewaters (de-Bashan et al., 2004; Walker et al., 2005). The generation of energy products from microalgae and macroalgae has been examined by a number of workers. Microalgae have been tested as raw material for the production of bio-oil (Li et al., 2007), methane (Golueke and Oswald, 1959; Minowa and Sawayama, 1999), methanol (Hirano et al., 1998) and hydrogen (Kim et al., 2006; Turner et al., 2008). Macroalgae have primarily been used to produce methane (Hansson, 1983; Morand and Briand, 1999; Troiano et al., 1976). A disadvantage of all these technologies is that the fuel produced must be stored, transported and further processed to produce electricity. Microbial fuel cells (MFCs) offer an alternative way to obtain electricity from the hydrolysis and fermentation of algae in only one process unit. MFCs consist of an anode and cathode connected by a load (usually a resistor in laboratory studies). The anode contains mixed or pure cultures of 2009 Wiley Periodicals, Inc.

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microorganisms that are used to catalyze the decomposition of the organic matter into electrons and protons. Power is produced through the reduction of oxygen or another chemical at the cathode. A metal is usually used to catalyze oxygen reduction, although it has recently been shown that microorganisms can be used for this purpose as well (He and Angenent, 2006). In this study, we evaluated the performance of MFCs using two different types of algae as substrates. Chlorella vulgaris (a microalgae) and Ulva lactuca (a macroalgae) were selected because they have been widely tested in other technologies for energy generation. Moreover, they have very different organic matter composition, with C. vulgaris containing more than 50% protein (Becker, 2007) and U. lactuca having around 60% carbohydrates (Ventura and n, 1998). The substrate degradation and microbial o Castan composition in MFCs and in anaerobic reactors were compared. To better understand the degradation process, we monitored the production of by-products (biogas and volatile fatty acids) using U. lactuca. To estimate the maximum power obtainable, we used different methods to obtain polarization and power density curves. We found that potentiostat methods usually employed for hydrogen fuel cells can overestimate maximum power production by MFCs with algae at scan rates often used in MFC tests.

powder form (Federal Laboratory Corporation, New York, NY) with particle sizes in the same range as those for U. lactuca. It consisted of 157 46 mg/g-substrate of total carbohydrates, 428 15 mg/g-substrate of total protein and had a COD of 1587 mg/g-substrate. Both materials were certied to contain the same composition as the natural sources. Pre-treatment of the U. Lactuca consisted of drying in a hot-drum (losing 93% of total water) followed by grinding in stainless steel and tungsten carbide mills. C. Vulgaris was pre-treated using spray drying. Samples were stored in a cool (48C) dry environment. No chemical treatment processes were used. The use of algae in a powder form ensured MFC efciencies could be directly compared based on substrate composition, and not for example algae cell size. Algae powders were added to in a medium containing (g/L): NH4Cl, 0.31; KCl, 0.13; NaH2PO4H2O, 2.45 and Na2HPO47H2O, 4.57. The conductivity of the medium was 4.9 mS/cm, and it had a pH of 6.8. No additional minerals or vitamins were added to the medium.

Reactors Inoculation and Operation Reactors were inoculated using primary clarier overow from the Pennsylvania State University wastewater treatment plant in State College. All reactors were operated in fed-batch mode at a xed temperature of 308C. Voltage was monitored across the resistor every 20 min. Data were obtained when MFCs produced a repeatable cycle of current generation. The solution was replaced when the voltage was reduced to <50 mV. Maximum power densities were evaluated using three different methods, all using a high organic matter concentration (2,500 mg COD/L). The single cycle method consisted of varying the resistance (between 7,500 and 100 V) from the open circuit voltage (OCV) every 20 min in a single batch cycle, over a short time period where the substrate change did not affect power output (Heilmann and Logan, 2006). For the multiple cycle method, a single cycle was run for each resistor (Heilmann and Logan, 2006). The maximum power density value was taken at steady state conditions, when the current started to decrease the solution was replaced before using a new resistor. These two methods were compared to a commonly used method based on linear sweep voltammetry (LSV) (Aelterman et al., 2008; Chen et al., 2008; Clauwaert et al., 2008; Logan et al., 2006). For LSV, the potential was decreased using a potentiostat at a rate decrease of 1 or 0.1 mV s1 from the OCV to a cell potential of 100 mV. Substrate degradation was monitored over a batch cycle for the highest substrate concentration (2,500 mg COD/L) in terms of chemical oxygen demand (COD), protein, and carbohydrate concentrations. To assess by-products formation among the different types of reactors used, volatile fatty acids (VFAs) and headspace gas composition were monitored in reactors using U. lactuca. A plastic cap

Methods
Reactors Construction Twelve reactors were used, each having a liquid volume of 25 mL. Four MFCs were operated at closed circuit (CC) using a circuit of titanium wire containing a resistor of 1,000 V (except as noted), four were operated in open circuit (OC) (no connection), and four were constructed to be completely anaerobic reactors (ARs) by sealing the reactors with an end plate. MFCs and ARs had graphite ber brush anodes 3.0 cm in outer diameter and 3.0 cm long (PANEX33 160K, ZOLTEK) (Logan et al., 2007) that were treated using a high-temperature ammonia gas process (Cheng and Logan, 2007). MFCs had air-cathodes that were prepared according to the procedures of Cheng et al. (2006), with a platinum (Pt) catalyst (0.5 mg/m2 Pt) and four diffusion layers. All materials were initially sterilized (using UV light for 2 h or autoclaved at 1218C for 15 min); although all tests were run using mixed cultures under nonsterile conditions.

Algae Characteristics and Medium Preparation U. lactuca was purchased as a powder with homogenous particles of 90200 mm (SigmaAldrich, St. Louis, MO). It consisted of 317 45 mg/g-substrate of total carbohydrates, 65 1 mg/g-substrate of total protein and had a COD of 833 mg/g-substrate. C. vulgaris was also obtained in a

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was tted on the top of selected reactors to create a headspace for gas accumulation. Gases were sampled using a gastight syringe (250 mL, Hamilton Samplelock Syringe). Bulk solution (0.5 mL) was obtained using a sterile syringe, ltered using glass ber lters (Whatman, GF/C, 4.7 cm of diameter, 1.2 mm of pore size), and stored at 208C. Once experiments were completed, samples were obtained to characterize the microbial community as described below.

Chemical Analyses Total and soluble protein, carbohydrate and chemical oxygen demand (COD) concentrations were monitored for soluble and total fractions of the bulk liquid according to Standard Methods (American Public Health Association (APHA), 1995). For the soluble fraction, samples were preltered using glass ber lters (Whatman, GF/C, 4.7 cm of diameter, 1.2 mm of pore size). Total and soluble COD analyses were carried out using method 5220 (Hach COD system, Hach Company, Loveland, Colorado). Soluble and total protein concentrations were quantied using the bicinchoninic acid protein assay kit (SigmaAldrich). A calibration curve was prepared using standard solutions ranging from 0.1 to 1.0 g/L of bovine serum albumin. Soluble and total carbohydrate concentrations were measured using a colorimetric method based on an anthrone reagent (Gerhardt et al., 1994). For this measurement, 1 mL of sample was transfer to a COD tube and 2 mL of a chilled H2SO4 solution (75%, v/v) were added. After vortexing (30 s), 4 mL of a chilled fresh anthrone solution (2 g/L, 75% (v/v) H2SO4) was added and the sample vortexed again. COD tubes were placed in a heating-block at 1008C for 15 min, cooled to room temperature, and analyzed using disposable cuvettes at 578 nm (UV-1601, Shimadzu Corporation). Every measurement included a calibration curve using glucose at concentrations of 503,000 mg/L (R2 0.99). Volatile fatty acid (VFA) concentrations (acetate, butyrate and propionate) were measured in triplicate using a gas chromatograph (Agilent 6890N) and a 30 m 0.32 mm 0.5 mm fused-silica capillary column. Before GC analysis, 50 mL 50% formic acid (v/v in water) were added to 1 mL samples. Gases (carbon dioxide, methane, and nitrogen) were analyzed using a gas chromatograph (helium carrier gas; model 310, SRI Instruments). Since nitrogen served as a dilution gas, it was removed from the calculations in order to determine the CO2 and CH4 headspace fractions.

for 30 s and bers removed. Then, tubes were centrifuged at 5,000g for 7 min. Total DNA was extracted using the Powersoil DNA isolation kit (Mobio Laboratories, Carlsbad, CA) and stored at 208C. 16S rRNA gene fragments were amplied from DNA samples using 16S rRNA gene fragments amplied using primer 3 50 -CCT ACG GGA GGC AGC AG-30 with a GC-clamp, and primer 2 50 -ATT ACC GCG GCT GCT GG-30 (Muyzer et al., 1993), and analyzed by denaturing gradient gel electrophoresis (DGGE) with a denaturing gradient ranging from 30% to 55% (100% denaturant is 7 M urea plus 40% (v/v) formamide in 1 TAE; 40 mM Tris-acetate, 1 mM EDTA, pH 8). DGGE gels were processed using the Bionumerics software package (version 3.5, Applied Maths, Austin, TX) to determine the position and intensity of all bands in all DGGE proles in relation to markers run alongside samples in the gel (Verseveld and Roling, 2008) and to analyze bands present in DGGE proles using Dice cluster analysis.

Calculations MFC potentials were obtained using a data acquisition system (2700, Keithly, Cleveland, OH). Potentials were converted to current using Ohms law, E IR, where E is the voltage, I is the current, and R is the resistance. Power densities ( Pd) were obtained using the equation: Pd IV/ AAn, where AAn is the cathode surface area (7.07 cm2). Columbic efciencies R t (Ec) were calculated using (Logan et al., 2006): Ec M 0f I dt=FzvAn DCOD, where: M 32, is the molecular weight of oxygen, z 4 the number of electrons transferred per mole of oxygen, F 96485.4 A mol1 Faradays constant, vAn the volume of liquid in the anode compartment, and DCOD the change in COD over the batch period of time. Statistical analysis of data was performed using Minitab1 15.1.0.0 for Windows using analysis of variance (ANOVA). The regression analysis relating maximum power densities algae concentrations was assessed using Sigmaplot1 9.0 for Windows. The rst order exponential rise-to-maximum model gave the best t (R2 0.95 0.05) according to the equation: Pd Pmax 1 ekCS , where Pmax is the maximum power density, k is the growth rate constant, and Cs is the substrate concentration.

Results
MFCs Performance Using Different Algae Concentrations

Microbial Analyses Biolms from the anodes were removed from MFCs by cutting off anode bers in a sterile laminar ow cabinet. Fibers were immediately placed in 15 mL centrifuge tubes containing sterile PBS solution (130 mM NaCl, 10 mM Na2HPO4, pH 7.2). Centrifuge tubes were vortexed

A repeatable cycle of current generation was obtained by C. vulgaris and U. lactuca (510 mg COD/L) after ve batch cycles (6 days). The maximum current for each batch cycle was obtained within 0.76.7 h depending on the substrate concentration. Batch cycles for MFCs using different concentrations of C. vulgaris required 25 days, while those

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for U. lactuca lasted 27 days (data not shown). When MFCs were fed algae at a concentration of 2,500 mg COD/L, a steady state current generation was rapidly achieved (Fig. 1). MFCs produced a steady state current between 0.52 and 0.55 mA for a period of 3 days in MFCs using U. lactuca, and 1.5 days using C. vulgaris. Following this steady output, current generation gradually decreased from 0.5 to 0.05 mA over a period of 4 days. Maximum power densities increased with substrate concentration until reaching a plateau (Fig. 2). At high organic matter concentrations the maximum power densities ( Pmax) obtained using the different algae were in the same range, with 440 mW 60 for MFCs using C. vulgaris and 450 mW 50 for MFCs using U. lactuca. MFCs fed C. vulgaris had a higher power growth rate constant (k 2:6 103 0:0012) and hence achieved Pmax at lower organic matter concentrations than MFCs using U. lactuca (k 0:9 103 0:0003). Coulombic efciencies peaked at relatively low algae concentrations (from 100 mg COD/L and 500 mg COD/L) with a maximum of 28% for C. vulgaris and 23% for U. lactuca (Fig. 3). At substrate concentrations higher than 600 mg/L, coulombic efciencies decreased and reached a plateau at 10%. COD removal increased to a maximum of 85 5% at a loading of 1,000 mg COD/L.

Figure 2. Maximum currents with Chlorella vulgaris and Ulva lactuca as a function of COD concentration. a current density between 0.20 and 0.25 mA/ cm2, and 0.76 0.15 W/m2 (215 W/m3) for MFCs using U. lactuca at a current density of 0.20 mA/cm2 (Fig. 4). The maximum power density obtained using LSV was dependant on the scan rate selected (Fig. 5). A scan rate of 1 mV/s produced a very high maximum power density of 1.6 0.3 W/m2 (453 W/m3). At a scan rate of 0.1 mV/s, the power density was much lower (0.9 0.2 W/m2, 255 W/m3; P 0.007, ANOVA). Based on a comparison of these LSV scan results with other methods (single and multiple cycles), it appears that a scan rate of 0.1 mV/s is a better choice than 1 mV/s for obtaining polarization curves (Fig. 4). The slower scan rates of 0.1 mV/s required 34 h to complete a polarization curve. It is likely that a scan rate of 1 mV/s is too fast (30 min for a cycle) for the bacteria to respond to the changes in voltage.

Effect of Polarization Method on the Calculated Maximum Power There were no signicant differences in the maximum power produced between the single cycle and multiple cycle methods ( P 0.45, ANOVA; Fig. 4). The average maximum power density produced using these two methods was of 0.98 0.39 W/m2 (277 W/m3) for MFCs using C. vulgaris in

Figure 1. MFCs current generation with 2,500 mg COD/L of Chlorella vulgaris or Ulva lactuca. Reactors were operated using an external resistance of 1,000 V. [Color gure can be seen in the online version of this article, available at www.interscience. wiley.com.]

Figure 3. Effect of substrate concentration in CE and COD removal efciency. Filled symbols are for CE and empty symbols are for COD removal efciency

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Organic Matter Consumption Removal efciencies were compared among three types of reactors: operating MFCs or those with a closed circuit (CC); MFCs kept in an open circuit (OC); and anaerobic reactors (ARs) for one operational batch (Fig. 6). COD in C. vulgaris was better removed in MFCs at CC (1,000 V) than in other reactors ( P 0.00, ANOVA). Differences in COD removals among reactors fed U. lactuca were not signicant ( P 0.60, ANOVA). COD removals in reactors using C. vulgaris were two times higher in the operating MFCs (60 6%) than in the AR (28%), while COD removals in reactors using U. lactuca were in the same range for all reactors (approximately 73 1%). Carbohydrate removal using both types of algae was highest in operating MFCs. Protein removal from C. vulgaris was highest in the operating MFCs (51 16%) and lowest in ARs (24 3%). Protein removal from U. lactuca was highest in open circuit MFCs (62 7%) followed by the closed circuit MFCs (41 1%) and ARs (15 6%). Concentrations of the substrate on the basis of soluble and particulate matter were analyzed for the operating MFCs at the start and at the end of the experiments (Fig. 7). Initially, organic matter from both algae contained more particulate organic matter than soluble organic matter. C. vulgaris contained two times more protein than carbohydrates while U. lactuca contained ve times more carbohydrates than protein. Soluble protein was the highest fraction consumed (83%) in C. vulgaris. In contrast, particulate carbohydrate was the highest fraction consumed (90%) in U. lactuca. Total COD consumption was higher for MFCs using U. lactuca than for MFCs using C. vulgaris. All MFCs removed more than 50% of the soluble and particulate COD.

Figure 4.

MFCs power density outputs from algae using different polarization methods. Reactors were fed a concentration of 2,500 mg COD/L of C. vulgaris (a) and of U. lactuca (b). Measurements were done using different resistances in duplicate reactors. Dotted lines are cell voltages and plain lines are for power densities. [Color gure can be seen in the online version of this article, available at www.interscience.wiley.com.]

Figure 5.

Comparison of short single cycle polarizations in MFCs using 2,500 mg COD/L Chlorella vulgaris at different scan rates. [Color gure can be seen in the online version of this article, available at www.interscience.wiley.com.]

Figure 6. Comparison of organic matter removal in MFCs at closed circuit (CC), MFCs at open circuit (OCV) and anaerobic reactors (AR) on the basis of protein, carbohydrates and COD using 2,500 mg/L of algae substrate. Measurements were done in duplicates, if the difference between replicates was low errors bar do not appear.

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Figure 7. Initial and nal organic matter content in MFCs. Organic matter was measured on the basis of protein, carbohydrates and COD for one operational batch; i initial and f nal.

By-Products in MFCs and Anaerobic Reactors Using U. lactuca Differences in headspace composition and volatile fatty acids production were assessed over one batch cycle for MFCs and ARs fed 2,500 mg/L U. lactuca. The headspace composition changed over a period of 7 days (96 h; Fig. 8a). Methane concentrations were higher for ARs than for MFCs. ARs reached a maximum methane concentration of 30% between the 3rd and 5th day while methane concentrations for MFCs remained below 5%. Carbon dioxide concentrations in MFCs reactors peaked on the rst day (14%) and gradually decreased until the end of the experiment. For ARs carbon dioxide concentrations remained between 5% and 10%. Acetate concentrations rose rapidly during the rst day for all reactors, following by a gradual decrease in MFCs (Fig. 8b). ARs had sharps increases and decreases in acetate concentrations. Propionate was detected in low quantities (<75 mg/L for all reactors) but no butyrate was detected.

Figure 8. By-products produced in MFC and AR using 2,500 mg/L Ulva lactuca. a: Headspace gas composition through time; squares: MFC and triangles: anaerobic reactor. b: Acetate production through time.

Effect of Type of Reactor Used in Microbial Communities Bacterial communities were clustered (Fig. 9) according to the bioprocess (MFCs or ARs). Communities from AR had a greater similarity (59.4 11.2%) to MFCs operated under open circuit conditions than to MFCs operated for electricity production (45.8 8.3%). There was a low similarity of microbial community proles between the inoculum and MFCs (10.4 0.9% similarity with CC; 11.0 4.9% with OC) or the AR (11.5 5.2% similarity).

Discussion
MFCs using mixed microbial cultures produced signicant power from microalgae and macroalgae when compared to other substrates. Maximum power densities of

0.98 W/m2 0.39 for C. vulgaris and 0.76 W/m2 0.15 for U. lactuca were higher than those obtained using paper wastewater (0.7 W/m2) in the same reactor conguration (Huang and Logan, 2008), but lower than those obtained with acetate (2.4 W/m2) (Logan et al., 2007). The difference in power generation among substrates is perhaps due to the complexity of the substrates. Particulate substrates and macromolecules require more energy for degradation processes (hydrolysis and fermentation) than simple soluble compounds that can be directly taken into the cell. One important result observed here is that maximum power densities were over-predicted by polarization curves obtained using a potentiostat at high scan rates. A polarization scan rate of 1 mV/s using LSV gave a power density 44% higher than that obtained at a slower rate of 0.1 mV/s or using xed resistors for extended periods of time. This result has important implications in MFCs analysis since high scan rates have been used to evaluate maximum power output in several recent MFC studies

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Figure 9.

Dice cluster analysis of bands present in biolms. Indicates similarities between the DGGE bands obtained from three different reactor congurations and two different substrates (Chlorella vulgaris and Ulva lactuca). The cluster analysis was obtained using Bionumerics software.

(Aelterman et al., 2008; Chen et al., 2008; Clauwaert et al., 2008). This indicates that polarization data developed using LSV should be conrmed by data obtained using xed resistances over longer period of times. For example, in the single-cycle method an interval of 20 min is used for each resistor, allowing time for the bacteria to adjust to this new load. At high scanning rates of 1 mV/s, the LSV approach applies a potential change that is too rapid for some MFCs to reach sufciently steady conditions. Further work should be done to determine if these changes can also be observed in MFCs using simple substrates. Better energy recovery was obtained with microalgae, C. vulgaris, than with macroalgae, U. lactuca. MFCs fed with microalgae produced greater power densities at a similar COD concentration than the macroalgae. In addition, the COD per gram of C. vulgaris was higher than that of U. lactuca on a dry weight basis. This difference is presumably attributable to the nature of the carbon source in each alga; presumably C. vulgaris contained a higher quantity of organic compounds than U. lactuca per unit mass. Apart from the proteins and carbohydrates measured in C. vulgaris other molecules known to be present such as lipids and vitamins may have contributed to energy production. While Coulombic Efciencies (CEs) obtained were low (1025%), they were typical for MFCs using complex substrates, for example, wastewater (16%, Huang and Logan, 2008) and cellulose (23%, Rezaei et al., 2008). Presumably as we begin to better understand the factors that affect CE, these values can be improved. CEs achieved in MFCs fed C. vulgaris were also slightly higher that those fed

U. lactuca. CEs decreased at COD concentrations higher than 600 mg/L. This trend towards a reduction in CE with organic loading has previously been observed, and is thought to be due to increased substrate losses over a longer batch cycle time either through methanogenesis or due to aerobic degradation of organic matter sustained by oxygen leakage through the cathode (Feng et al., 2008). Since low methane compositions and VFA concentrations were measured for MFCs using U. lactuca it appears that, in this case, methanogenesis was not the main contributor to the decrease in CE. At a high organic matter load, the difference in algae composition produced different COD removals among MFCs. The best COD removals were obtained in reactors using U. lactuca. This was correlated with a higher degradation of carbohydrate in MFCs using U. lactuca than of protein in MFCs using C. vulgaris. Moreover, particulate carbohydrates in MFCs using U. lactuca or C. vulgaris were more readily consumed than particulate proteins. Analysis of microbial communities showed that bacterial selection occurred in all reactors (MFCs and ARs) as a result of the treatments. Microbial communities clustered according to the type of bioprocess (MFC at OC, MFC at CC and AR) used. This implies that the reactor conditions had an effect in the nal microbial selection suggesting that there were possible differences in the metabolisms occurring in each reactor. The utility of power generation from algae using MFCs can be evaluated in comparison to other methods of energy production exploiting this source of organic matter. The

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Table I.

Comparison of total energy production using different technologies with Chlorella vulgaris and Ulva lactuca. Chlorella vulgaris (kW-h/kg-DW) 9.3 9.8b 0.4c 13.5d 2.5e
a

Technology Incineration Anaerobic digestion Hydrogen production Oil extraction Microbial fuel cells

References Minowa and Sawayama (1999) Golueke and Oswald (1959) Kim et al. (2006) Li et al. (2007) This study

Ulva lactuca (kWh/kg DW) 13.5 6.6g n.a. n.a. 2.0h

f

References Grahame (1973) Briand and Morand (1997) n.a. n.a. This study

n.a, not available. a,b,c,e,f,g,h 2.77 kWh/MJ, assuming 30% (for a, b, d, f, g) and 70% (for c) conversion efciencies to convert energy from heat to power. b Using mixed cultures of microalgae containing Chlorella vulgaris, 1 mol CH4 981 kJ. c Converted to energy assuming 1 mol of H2 237 103 J (Turner et al., 2008). d Converted to grams of algae assuming 0.48 gbiodiesel/g-algae. e,h Calculated from the linear regression equation obtained in the plot of joules produced over a range of algae concentrations.

energy obtained per gram of algae with an MFC is currently low relative to other technologies, based on assuming a 30% efciency from heat to power with other technologies (Table I). For C. vulgaris the highest power output was derived from oil extraction and methane production from anaerobic digestion. MFCs and hydrogen production had a low energy recovery indicating the need for technology improvement. For U. lactuca the best option seems to be incineration, but the sustainability of this technology is debatable (Minowa and Sawayama, 1999). Incineration could result in the production of hazardous ash and emission of partially combusted products.

References
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Conclusions
Using microalgae and macroalgae for energy generation presents several benets over other biomass sources: they can grow using different substrates such as CO2 or wastewater, have high growth rates, and require less space for cultivation. MFCs using either microalgae or macroalgae produced relatively high power densities compared to the use of other substrates in this MFC conguration. Maximum power densities were best obtained either using xed resistances in the circuit for a sufciently long time for the system to reach steady conditions, or by LSV using a slow scan rate (0.1 mV/s). C. vulgaris gave the highest energy generation per gram of substrate while, the macroalgae U. lactuca was degraded more efciently in MFCs. The substrate composition and bioprocess had an effect on the nal COD removal obtained and the type of microbial communities present. Carbohydrates contained in U. lactuca were more completely degraded than proteins in C. vulgaris. Bioelectricity production using algae in MFCs is useful as a low temperature method of power generation, but it needs to be further improved in order to make it competitive with alternative energy technologies.

The authors greatly appreciate the help of David W. Jones during laboratory measurements.

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