dark cycle and long-term performance test in a photosynthetic microbial fuel cell

Fuel 140 (2015) 209–216

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Characterization of light/dark cycle and long-term performance test in a photosynthetic microbial fuel cell Araceli Gonzalez del Campo a,⇑, Jose F. Perez a, Pablo Cañizares b, Manuel A. Rodrigo b, Francisco J. Fernandez a, Justo Lobato b a

University of Castilla-La Mancha, Chemical Engineering Department, ITQUIMA, Av. Camilo José Cela S/N, 13071 Ciudad Real, Spain University of Castilla-La Mancha, Chemical Engineering Department, Faculty of Chemical Sciences & Technologies, Building Enrique Costa Novella, Av. Camilo José Cela S/N, 13071 Ciudad Real, Spain b

h i g h l i g h t s  A photosynthetic microbial fuel cell was used to recover energy of wastewater.  Light/dark cycle in a photosynthetic microbial fuel cell was characterized.  When dissolved oxygen was low, nitrate and sulfate could be used as electron acceptor.  The system showed a great reliability and durability.

a r t i c l e

i n f o

Article history: Received 20 March 2014 Received in revised form 18 August 2014 Accepted 23 September 2014 Available online 7 October 2014 Keywords: Photosynthetic microbial fuel cell Light/dark cycle Electron acceptor Life test

a b s t r a c t In this paper, the characterization of light/dark cycle in a photosynthetic microbial fuel cell used to recover energy of wastewater was carried out. To this end, a wide range of parameters were measured throughout both periods light/darkness. During the light phase, the electricity production was higher because algae carried out photosynthesis and produced oxygen, which acted as electron acceptor. However, during the dark phase, electricity was still on production when dissolved oxygen at the cathode was nearly zero, indicating that nitrates and sulfates (added as nutrients to the cathode) were also acting as electron acceptors. COD and nutrients removal at the anodic compartment was found constant all day and about equal to 75% (COD removal), 70% (ammonium removal) and 26% (phosphate removal). The highest value of maximum power density (42.98 mW m2) and the lowest value of internal resistance (1680 O) were reached at 13:00 h. The polarization resistance of the cathodic compartment changed during the day as a function of the cycle of light/dark, between 6930 O and 13210 O. Finally, a life test was carried out for 10 months, demonstrating an adequate performance in terms of durability and reliability. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction Energy demand is steadily on the rise, as a consequence of the growing population and higher living standards. A high percentage of this energy is supplied by fossil fuels, which unfortunately contribute to the global warming. Ideally, new energy sources should preferably be renewable and carbon-neutral. On the other hand, wastewaters must be treated for both complying with the law and avoiding harms to the environment. Up to know, all the processes used in wastewater treatment are energy-consuming. It was estimated that 1.5% of the total energy produced in U.S.A. is consumed in wastewater treatments [1]. ⇑ Corresponding author. Tel.: +34 926 295300x96319; fax: +34 926 295242. E-mail address: [email protected] (A. Gonzalez del Campo). http://dx.doi.org/10.1016/j.fuel.2014.09.087 0016-2361/Ó 2014 Elsevier Ltd. All rights reserved.

Considering the aforementioned reasons, new sources of energy are under investigation. In particular, energy recovery technologies from biomass-rich wastewaters, using microorganisms, are a topic of current interest in scientific discussions [2–4]. Certain technologies, such as Microbial Fuel Cells (MFC’s), can approach successfully energy production and wastewater treatment at the same time. MFC’s are bioelectrochemical systems (BES’s) which convert chemical energy into electric using microorganisms [5]. In an MFC, a substrate (often organic matter) is oxidized in a type of biological process in which microorganisms deliver electrons to an anode surface [6]. The electrons flow through an external load (electrical current) and they are released at the cathode, where a reaction between electrons and electron acceptors take place [1,7].

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The usual MFC’s set-up consists of two chambers (anodic and cathodic) separated by a proton exchange membrane (PEM). Until recently, just half of the system, the anode, was biological. But lately, full-biological set-ups have been studied using microorganisms at the cathode, so-called biocathode [8]. These systems present major advantages over abiotic or chemical cathodes. Among them, lower investment and operating costs (added catalysts may not be necessary since microorganisms are the actual ones) as well as the possibility of taking advantage of other metabolic pathways to remove pollutants or produce any other product of interest at the cathode [9]. A possible classification for biocathodes is according to the terminal electron acceptor used in the cathodic reaction: oxygen (i.e. aerobic) or non-oxygen (i.e. anaerobic). In absence of oxygen (anaerobic), other molecules can function as terminal electron acceptor: nitrate, sulfate, selenate, arsenate, carbon dioxide or oxidized metal ions like iron and manganese [10]. Among all the electron acceptors, oxygen (aerobic) is the most popular for the cathodic reaction in MFC’s. Basically, due to its high redox potential and abundance in the atmosphere resulting in relatively low cost of supply. However, aeration costs mean approximately 50% of the whole operating costs [11]. Furthermore, sunlight can be used through photosynthetic microorganisms in a MFC. If so, the system is known as photosynthetic MFC. There are many possible configurations of photosynthetic MFC’s [12]. In particular, photosynthetic oxygen production is quite interesting to provide the terminal electron acceptor, oxygen, avoiding the need for pumping and its subsequent energy costs. In this experimental set-up, a biocathode containing algae Chlorella vulgaris for oxygen production was used. Since algae are photosynthetic microorganisms, oxygen is only produced when they are exposed to sunlight causing two different periods in the system: light and darkness. In this work, a two-chambered photosynthetic MFC for energy production was under study. A wide range of parameters was measured throughout both periods light/darkness so that the behavior of the system was characterized. To finish up, important characteristics such as endurance and reliability of the system was tested, making use of a long-term life-study.

2. Experimental 2.1. Experimental set-up The photosynthetic microbial fuel cell used in this study, Fig. 1, consisted of a biological reactor separated into two identical chambers (800 mL each) by a proton exchange membrane (PEM, by SterionÒ) [13–15]. In each compartment, Toray carbon cloths with 10% of Teflon were used as electrode. Noble metal was not used as catalyst in the electrodes. The active area of each electrode was 8 cm2. Under normal working conditions, the anode and the cathode were connected by means of wires and an external resistance of 120 O. The initial inoculum was an activated sludge from a conventional domestic wastewater treatment plant described elsewhere [16], after 25 days a biofilm of microorganisms was formed on the surface of the anodic electrode [15]. It was fed in continuous mode with 1.23 mL min1 of synthetic urban wastewater, which contained 322 mg L1 of organic matter (161 mg L1 of glucose and 161 mg L1 of fructose) and nutrients. The composition of the wastewater was shown in a previous paper [15]. The cathode compartment contained an initially pure culture of Chlorella vulgaris to supply oxygen. The artificial solar energy was supplied (11.5 h per day, from 9:00 h to 20:30 h) with an 11 W Fluorescent lamp (Philips) with an illumination intensity of

Fig. 1. Picture of the set-up.

2.7 cd cm2. CO2 was used as an inorganic carbon source for algae, therefore, every day CO2 was bubbled at the cathodic compartment during 30 min. In this way, the cathodic compartment can act as carbon sink. Moreover, the algae were fed with a Bold’s basal medium [17]. The temperature in both compartments was 26 ± 1 °C. A Keithley 2000 Digital Multimeter was connected to the system to monitor continuously the cell voltage. The cell was placed over a multipoint magnetic stirrer in order to keep the anodic and cathodic compartment in suspension and improve the matter transfer. Oxygen concentration was continuously monitored in the cathodic compartment with an Oxi538 WTW oxymeter. 2.2. Characterization techniques In both compartments, conductivity and pH were measured with a Jenway 740 conductometer and a PCE-228 pH meter, respectively. Chemical oxygen demand (COD) was determined by photometric method with MERCK COD cell test and Pharo 100 MERCK spectrophotometer. Anions were measured by ion chromatography using Shimadzu LC-20A equipment (column, Shodex IC I-524A; mobile phase, 2.5 m Mphthalic acid at pH 4.0; flow rate, 1.0 mL min1). The same ion chromatography equipment (column, Shodex IC YK-421; mobile phase, 5.0 mM tartaric, 1.0 mM dipicolinic acid and 24.3 mM boric acid; flow rate, 1.0 mL min1) was used to measure cations [18]. Polarization curves were recorded using an Autolab PGSTAT30 potentiostat/galvanostat (Ecochemie, The Netherlands) at a scan rate of 0.5 mV s1 and a step potential of 1 mV. These curves make it possible to discern three key parameters: the open circuit voltage (OCV), maximum power density (Pmax) and internal resistance [15]. In addition, analyzing the plot, the limiting processes which control the performance of the cell can be identified [19,20]. The main source of error in the characterization techniques used in this work came from the intrinsic variability in the behavior of the microorganisms of the biofilm, due to their changing nature [21]. The same potentiostat/galvanostat (Autolab PGSTAT30, Ecochemie, The Netherlands) using the frequency response analyser (FRA) module was used to carry out electrochemical impedance spectroscopy (EIS). EIS measurements were run for the full cell at open circuit conditions, in a frequency range of 10 kHz–1 mHz and with

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In order to study and understand the behavior of the photosynthetic MFC, some operational variables were monitored throughout the day during one week (7 consecutive days). In this way, the evolution of the most important variables of the system was analyzed during different hours of day. In Table 1, the sampling time and its correspondent moment in the cycle are shown. Moreover, polarization and power curves and EIS were carried out at different times (at 13:00 h and 17:00 h along the light cycle and at 9:00 h and 20:00 h along the dark cycle) in order to determine OCV, maximum power density and internal resistance from polarization and power curves and ohmic and polarization resistance from impedance. 3.1.1. Daily profiles of cell voltage and dissolved oxygen at the cathode In Fig. 2a, cell voltage and dissolved oxygen at the cathode during one day are shown. During these experiments, the cathode was operated under a 11.5 h light/12.5 h dark regime. In this way, during the light phase, algae carried out the photosynthesis absorbing light, capturing carbon dioxide and releasing oxygen. At 9:15 h, carbon dioxide was bubbled and, as a consequence, both dissolved oxygen at the cathode and cell voltage fell sharply. It is suggested that the stripping process led to lower cell voltage [15]. The plateau was reached at 13:00 h, the cell voltage and dissolved oxygen remained steady at approximately 18 mV and 7 mg L1, respectively, until 20:30 h, when the light was switched off and the dark phase began. During the dark phase, algae carry out respiration and consume oxygen. Due to this fact, dissolved oxygen decreased to 2 mg L1 and, as a consequence, cell voltage went down to 10 mV. The plateau was reached at 00:00 h and remained until 9:00 h. Schamphelaire and Verstraete studied the production of electricity in a similar system, observing sharp fluctuations in a 24 h-cycle, with a peak during daytime and minimum levels during night [23]. Thus, it can be said that cell voltage production depends on dissolved oxygen at the cathodic compartment, since oxygen is the electron acceptor of the reaction according to Eq. (1). This behavior was also observed in other publications [14,15,24,25]. Kang et al. suggested that the critical oxygen concentration is 6.6 mg L1 using a graphite cathode [26].

O2 ðgÞ þ 2Hþ ðacÞ þ 2e ! H2 OðlÞ

ð1Þ

The decrease in dissolved oxygen was higher than that of the cell voltage. In this way, in Fig. 2b the drop of cell voltage versus drop of dissolved oxygen from 20:30 h (when light was switched

Table 1 Sampling times for 24 h. Hour

Moment of the day

8:40 9:10 10:00 16:30 20:00 20:45 21:30 23:30

Before the illumination beginning 10 min after the illumination beginning 15 min after the CO2 bubbling Steady state during the day The end of the illumination cycle 15 min after the dark beginning 1 h after the dark beginning Steady state during the night

Cell voltage (mV)

3.1. Characterization of photosynthetic MFC throughout the day

20

10

18

9

16

8

14

7

12

6

10

5

8

4

6

3

4

2

Cell voltage Dissolved oxygen

2

1

0

0 0

2

4

6

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10

12

14

16

18

20

22

24

t (h)

(b)

18 16 14

Cell Voltage (mV)

3. Results and discussion

(a)

Dissolved oxygen (mg L-1)

an AC signal of 10% of OCV. The cathode was used as the working electrode and the anode as the counter and the reference electrode [22]. EIS data were fitted to an equivalent circuit in order to obtain the ohmic (or diffusion) resistance and the polarization (or charge transfer) resistance of each electrode.

12 10 8 6 4 2 0 0

1

2

3

4

5

6

-1

Dissolved Oxygen (mg L ) Fig. 2. (a) Cell voltage and dissolved oxygen at the cathode during one day. (b) Cell voltage versus dissolved oxygen from 20:30 h (when light is switched off) to 00:00 h.

off) to 00:00 h (when the plateau was reached) is shown. These experimental data were adjusted to lineal equation with a correlation coefficient of 0.919, demonstrating a reasonable goodness of fit. However, it is important to highlight that the y-intercept was no zero but 6.682 mV. It may indicate that if the dissolved oxygen at the cathode were zero, electricity would still be on production. It indicates that any other molecules, rather than oxygen, were acting as electron acceptors. Some molecules added as nutrients in the cathode (such as nitrates and sulfates) have been reported to act as electron acceptors [9,27]. 3.1.2. Evolution of other parameters for one day Conductivity and pH at both chambers were measured at indicated hours. The conductivity is not shown because this parameter remained constant at the cathodic compartment (around 2.4 mS cm1), and at the anodic compartment the conductivity ranged between 500 and 600 lS cm1 all the experimental time. In Fig. 3, pH at both compartments for 1 day can be observed. The pH of the cathodic chamber decreased when carbon dioxide was bubbled. This fact was expected, because carbon dioxide, once dissolved into water, produce carbonic acid and, after that, the equilibrium between carbonic acid, carbonate, bicarbonate is shifted to bicarbonate/carbonate and protons are generated, therefore, the pH of the cathodic chamber decreased down to 4.5. After that, the pH increased up to 6 due to buffer effect of carbonic acid/bicarbonates/carbonates and also to consumption of H+ in the oxygen reduction reaction [24,28,29]. On the other hand, the pH at the anodic compartment remained stable during the day, around 6.

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removal turned out to be 70% and 26%, respectively. A COD:N:P ratio of 100:5:1 was achieved in the anodic compartment. Taking into account the 100:20:1 COD:N:P ratio commonly required to feed the biological reactor in a conventional urban wastewater treatment plant [35], a minor quantity of nitrogen is necessary to remove COD in a MFC. In the cathodic compartment, nitrate, phosphate and sulfate were found. These compounds were added as nutrients for algae growth. It is important to highlight that nitrate and sulfate can act as electron acceptor [36], according to Reaction (2) and (3), respectively. However, any product of the reduction of these compounds was obtained. In Fig. 4b, the evolution of nitrate, phosphate and sulfate into the cathodic compartment all day is shown. As it

8

pH

7

6

5 Anode Cathode 4 8

10

12

14

16

18

20

22

24

t (h)

40

20

Fig. 3. Evolution of the pH at both compartments of the cell for one day.

+

38

16 14

36

12 10

6 NH+4

4

32

PO-3 4

-3

34

8

4

Concentration NH 4 (mg L-1)

(a) Concentration PO (mg L-1 )

2 0 000:08

30 000:12

000:16

000:20

000:24

001:04

001:08

t (h) 400

(b) Concentration (mg L-1)

350

300

250

200 -3

PO 4

150

-

NO 3 -2

SO 4

100 000:08

000:12

000:16

000:20

000:24

001:04

001:08

t (h) 30

160

4

-3

150

25

140 20 130 15

5

-2

SO 4

90 80 000:08

-

NO3

(mg L-1)

-3

PO 4

4

10

100

-2

110

-

120

3

Concentration PO (mg L-1 )

(c)

Concentration NO -SO

However, the pH at the anodic compartment was slightly declined when carbon dioxide was bubbled at the cathodic compartment. It was because some protons passed through the membrane from the cathode to the anode. The pH is a very important variable in an MFC, because microorganisms and algae can only carry out their vital functions across a limited range of pH, from 6.5 to 8.5 for microorganism and from 7.5 to 8 for Chlorella vulgaris [15,30,31]. Hence, it is important to maintain a neutral or slightly acid pH near the cathode to maximize power generation [1]. In this way, the pH of both compartments was found to be suitable for the correct operation of photosynthetic MFC. During this study, COD at the anodic compartment and nutrients (nitrate, sulfate, phosphate and ammonium) at both compartments were measured. COD at the anodic compartment was found constant all day. In this way, COD removal percentage was around 75% and COD removal rate was 30.38 ± 1.73 mg O2 h1. Thus, a relation between cell voltage and COD removal by microorganisms was not observed. It can be justified considering that the most of the organic matter was consumed by non-electrogenic microorganisms, as coulombic efficiency was smaller than 1%. Coulombic efficiency is a direct measure for competition between electrogens and methanogens in a mixed culture [32]. Exoelectrogens and methanogens share growing conditions so they compete with each other [33]. In a broad sense, the overall organic matter consumption by anodic microorganisms was not affected by light/dark cycles. Microorganisms and algae require nutrients and trace elements for optimum growth. Among them, the most important are nitrogen and phosphorous. The lack of these nutrients has an adverse effect upon the growth and the performance of microorganisms and algae [34]. In this way, the nutrients consumed by microorganisms (ammonium and phosphate at the anodic compartment) and by algae (nitrate, sulfate and phosphate at the cathodic compartment) was studied. To meet the objective, ammonium, nitrate, nitrite, sulfate, sulfite and phosphate were analyzed at the effluent of the anodic compartment and into the cathodic compartment. Firstly, it is important to note that ammonium and phosphate were the only compounds of nitrogen and phosphorous found at the effluent of the anodic compartment. It indicates that nitrification process did not take place. In Fig. 4a, the evolution of ammonium and phosphates at the effluent of MFC during both cycles light/dark (24 h period) is shown. The concentration of ammonium and phosphate at the effluent remained steady all day, around 10 mg L1 of ammonium and 37 mg L1 of phosphate. Taking into account flow rate and initial ammonium and phosphate concentration in wastewater, the percentage of ammonium and phosphate

18

0 000:12

000:16

000:20

000:24

001:04

001:08

t (h) Fig. 4. Evolution of nutrients (ammonium, nitrate, sulfate and phosphates) for one day. (a) At the effluent of the anodic compartment. (b) At the cathodic compartment. (c) In a culture of Chorella vulgaris, not connected to an MFC, during the dark phase.

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1 N2 þ 3H2 O 2

2  SO2 þ 8OH 4 þ 4H2 O þ 8e ! S

ð2Þ ð3Þ

At the beginning of the light phase, the concentration of phosphate, nitrate and sulfate decreased from 229 to 220 mg L1, 360 to 340 mg L1 and 282 to 240 mg L1, respectively. These concentrations remained constant during the light phase. When the light was switched off, these concentrations reached a peak and soon after, they decreased to 174, 205 and 161 mg L1, respectively. Finally, the concentration increased before the light was switched on. This behavior was observed on a daily basis, seven days in a row. To our knowledge, this behavior was unusual and had not been reported before. In the absence of oxygen, other compounds, such as nitrate, sulfate, iron, manganese, selenate, arsenate, urinate, fumarate and carbon dioxide can act as terminal electron acceptors [10,37]. Regarding their redox potentials, the cathodic potential with nitrate, manganese, and iron as terminal electron acceptors is comparable to oxygen [36]. On the other hand, sulfate has a lower potential [36]. Therefore, during the dark phase, a continuous descent in the concentration of other electron acceptors (sulfate or nitrate) was expected as a result of their consumption in the reduction reaction, due to the fact that electricity was still on production when dissolved oxygen at the cathode was the lowest. In the light of the electricity produced during the dark phase (15 mV) and the stoichiometric ratios of the reduction reaction from nitrate to nitrogen (Reaction (2)), an estimation of the theoretical consumption of nitrate (the second best electron acceptor, right after oxygen) in the cathode can be obtained. Considering the aforementioned assumptions, the theoretical consumption rate 1 of nitrate (from 00:00 to 08:00) was 5.78102 mg NO , making 3 h a total of 0.463 mg NO in 8 h. This value is significantly lower than 3 the experimental consumption measured in the cathodic compartment (80 mg NO 3 ). The same results were obtained for sulfate. Therefore, the consumption of nitrate and sulfate because of the reduction reaction into the cathodic compartment was negligible and the fluctuation of nutrients concentration during the dark phase was initially put down to an indetermined process regarding the algae. With the aim of double-check this pattern, the evolution of nitrate, phosphate and sulfate concentration in a culture of Chorella vulgaris, not connected to an MFC, was studied during its dark phase. Results are shown in Fig. 4c. As a conclusion, the same pattern was found in the new culture. In view of the results, it is clear that any non-defined metabolic process of the algae is responsible for the pattern observed. On the other hand, although the initial inoculum of Chlorella vulgaris was pure, as time goes on, other photosynthetic or hereotrophic microorganisms can appear and contaminate the culture. However, if the last conjecture proves to be true, it did not pose a problem to the performance of the photosynthetic MFC. 3.1.3. Electrochemical characterization during one day In order to electrochemically characterize the photosynthetic MFC, polarization curves and electrochemical impedance spectroscopy were carried out at 9:00 h (before the light was switched on, dark phase), 13:00 h and 17:00 h (light phase) and 20:00 h (right after the light was switched off, dark phase).

0,6

(a) 0,5

0,4

V (mV)

NO3 þ 6Hþ þ 5e !

[1]: Region I, a decrease of voltage due to the polarization of the electrodes (activation losses) for low currents starting just at the OCV; Region II, a subsequent linear decrease region (ohmic losses), in which the resistance of the different components of the cell limits the process; and Region III, that corresponds to the region controlled by mass-transfer (concentration losses), in which there is a lack of electrochemically active species arriving to the electrodes surface. In this way, the types of losses in the MFC can be determined considering the shape of the graph. In Fig. 5a, polarization curves at different times are shown. In the curves of the dark phase (when oxygen concentration is low), the Region III (concentration losses) was the predominant one. In this region, the major losses are due to low concentration of reactants or mass transfer [1]. In this system, it was due to low oxygen concentration at the cathode. The slope of the Region III at 9:00 h was steeper than at 20:00 h, this was due to the oxygen concentration was higher at 20:00 h (after light was switched off, oxygen continued to be consumed) than at 9:00 h (after 12 h at dark phase, oxygen concentration was the lowest). In this way, it can be seen that the oxygen was the most important electron acceptor at the cathode. Particularly during the dark phase, the electricity production was heavily reliant on oxygen concentration. At 13:00 h, the predominant region was Region III (concentration looses) as oxygen concentration was increasing. At this time, the maximum oxygen concentration had not been reached yet. However, at 17:00 h, the maximum oxygen concentration had already been reached and the predominant region was Region I (activation looses). It indicates that when oxygen concentration was at its peak, the system was limited by the oxygen reduction

0,3

0,2

9:00 h

0,1

13:00 h 17:00 h

0

20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320

j (mA m-2) 50

(b) 40

13:00 30

17:00 h 20

20:00 h

10

9:00 h 0 0

3.1.3.1. Polarization curves. In an ideal polarization curve, there are three characteristic regions of voltage decrease in a fuel cell. Each region shows different types of losses reducing the useful current

20:00 h

0,0

P (mW m-2)

can be observed, the evolution of these compounds followed the same pattern.

20 40 60 80 100 120 140 160 180 200 220 240 260 280 300 320

j (mA m-2) Fig. 5. (a) Polarization curves at different times. (b) Power curves at different times.

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rate at the cathode. It was an important handicap in uncatalyzed systems. This problem may be solved using an appropriate catalyst in the electrode. It has been reported that oxygen has a high overpotential when uncatalyzed electrodes are used, even though it is the most practical electron acceptor [38]. From polarization curves (Fig. 5a) and power curves (Fig. 5b), open circuit voltage (OCV), internal resistance and maximum power density can be calculated. In this way, in Table 2 the obtained parameters at different times are shown. As it can observed in Table 2, OCV, maximum power density and internal resistance ranged during the day from 0.460 to 0.541 mV, 8.18 to 42.98 mW m2 and 8060 to 1680 O, respectively. The highest value of maximum power density and the lowest value of internal resistance were measured at 13:00 h, when the voltage was in its peak and the steady state had already been reached. The lowest value of maximum power density and the highest value of internal resistance were obtained at 9:00 h, when output voltage was the lowest due to the absence of oxygen. So, the low oxygen concentration at 9:00 h caused an increase of internal resistance and a decrease of maximum power density because the reduction reaction was oxygen-limited. On the other hand, the highest maximum power density obtained was 42.98 mW m2 at 13:00 h. This value was similar or higher than those obtained in other studies using uncatalyzed MFC’s [39–42]. 3.1.3.2. Electrochemical impedance spectroscopy. In order to determine the resistances (ohmic, or diffusion, and polarization, or charge transfer) of each part of the cell separately, electrochemical impedance spectroscopies were carried out at different times. The EIS were run on the complete cell [43]. The Nyquist plot obtained show a high polarization resistance represented by an unclosed semicircle (representation not shown). The equivalent electrical circuit (Fig. 6) was used to fit the impedance data to obtain the ohmic, anode and cathode polarization resistance. The equivalent circuit model shown in Fig. 6 consists of two electrodes (anode and cathode), each comprised of a parallel resistor and a constant phase element (CPE), and separated by a resistor (membrane + solution resistance) [36,43]. Table 3 shows the parameters from the equivalent circuit fitting EIS data. The correlation coefficient was greater than 0.99 in all cases except for 20:00 h measure. Firstly, the ohmic resistance was similar all day (in light and dark phase), between 200 and 250 O, indicating that the membrane and solution resistance was

Table 2 OCV, maximum power density and internal resistance at different times. Hour

OCV (V)

Maximum power density (mW m2)

Internal resistance (O)

9:00 13:00 17:00 20:00

0.460 0.502 0.541 0.502

8.18 42.98 30.93 22.16

8060 1680 1840 4370

Anode CPE a

Cathode CPE c Rohm

Ra

Rc Fig. 6. Equivalent circuit.

Table 3 Parameters obtained by the adjustment of EIS to an equivalent circuit ((RQ)R(RQ)). Hour

Ra (O)

Rohm (O)

Rc (O)

r2

9:00 13:00 17:00 20:00

1634 1776 2393 1834

204.9 250.1 198.2 200.1

12,650 6930 8810 13,210

0.996 0.991 0.995 0.976

not affected by the light or the lifecycle of the algae. This type of resistance was the lowest in this system. The polarization resistance of the anodic compartment (Ra) was similar along the day, as it was expected, because the photosynthetic cycle of the algae did not affect to the anodic compartment. The Ra ranged between 1600 and 2200 O. These differences can be attributable to the changes of the biofilm as times goes on. However, the polarization resistance of the cathodic compartment (Rc) changed during the day as a function of the cycle of light/dark, between 6930 and 13210 O. In this way, the highest polarization resistance of the cathodic compartment was reached at 9:00 and 20:00 h, right when the dissolved oxygen was at its lowest, limiting or controlling the reduction reaction. On the other hand, the lowest Rc was reached at 13:00 h when the steady state had already been reached. Broadly speaking, the polarization resistance of the cathodic compartment was substantially higher than that found on the anodic one, between three- and sevenfold, approximately. This is because of the absence of a precious catalyst in the cathode whereas in the anode, a biofilm formed on the surface of the electrode acted as biocatalyst [15,44]. In general, biocathodes have higher electrical resistances and, therefore, higher energy losses [10,45,46].

3.2. Life test durability A life test consists in monitoring a variable of a process throughout a long period of time. In order to evaluate the performance of the photosynthetic microbial fuel cell, its durability and reliability were studied. The implementation of this system for energy supply applications calls for a high degree of reliability. For this purpose, some researchers have studied the durability of different elements in a MFC for 250 days [47], six months [48] and 3–5 weeks of operation [49]. In this work, the life test was carried out for 10 months. This study monitored two of the most important operational variables: electricity production and treatment capacity. During the abovesaid period, the system was subjected to different studies, some of them reported in previous works (study of performance of photosynthetic MFC with microorganisms in biofilm and both microorganisms in biofilm and suspension; study of influence of COD concentration in wastewater and study of different inorganic carbon sources for algae) [50] and others shown in this work (characterization of photosynthetic MFC throughout the day). In this way, in Fig. 7, cell voltage (Fig. 7a), COD removal percentage (Fig. 7b) and COD removal rate (Fig. 7c) during 10 months are shown. Blank spaces correspond to periods in which sampling or measuring was not possible, because any other process was in progress (polarization curves, EIS, etc.). Taking into account that cell voltage fluctuated throughout the day, in Fig. 7a the cell voltage at 5:00 h (plateau of dark phase) and 17:00 h (plateau of light phase) are plotted. The cell voltage at 17:00 h varied between 10 and 25 mV and at 5:00 h between 7 and 15 mV. The variations of this parameter are due to different experiments carried out in the cell, which led to changing conditions in the anodic compartment. It is important to highlight that

A. Gonzalez del Campo et al. / Fuel 140 (2015) 209–216

(a)

40 17:00 5:00

35

Voltage (mV)

30 25 20 15

215

wastewater (COD reduction). Moreover, the electrodes showed no mechanical degradation with time. This is due to the presence of Teflon in its formulation, acting as a glue of the carbon paper fibers. On the other hand, although fouling of proton exchange membrane was observed, it did not affect its performance. As the main conclusion drawn from the durability test, it can be concluded that the system showed a great reliability, durability and resilience under changing operational conditions.

10 5

4. Conclusions

0 0

25

50

75

100 125 150 175 200 225 250 275 300 325 350

From this work, the following conclusions can be drawn:

t (d)

– Cell voltage production depended on dissolved oxygen. During the light phase, algae produced oxygen and electricity production was at its highest. However, during the dark phase, when dissolved oxygen was at its lowest, the electricity production indicated that nitrates or sulfates acted as electron acceptor. The cathodic compartment was the limiting compartment of the system. This was because the absence of a precious catalyst to overcome the adverse thermodynamic of the oxygen reduction reaction. – The photosynthetic MFC was stable, as far as electricity production and wastewater treatment was concerned, after 10 months in operation.

COD removal percentage (%)

(b) 100 90 80 70 60 50 40 30 20 10 0 0

25

50

75

100 125 150 175 200 225 250 275 300 325 350

(c)

60

COD removal rate (mg h-1)

t (d)

50

Acknowledgement Authors thanks the JCCM for the financial support thorough the Project POII10-0329-5194.

40

References

30 20 10 0 0

25

50

75

100 125 150 175 200 225 250 275 300 325 350

t (d) Fig. 7. (a) Cell voltage at 5:00 h and 17:00 h. (b) COD removal percentage. (c) COD removal rate for 10 months.

the range of variation was wider in the plateau of the light phase than in the plateau of the dark. It is because during the dark phase, the cathode was the limiting compartment and, therefore, the production of electricity was determined by the performance of this compartment irrespective of the conditions in the anodic one. In Fig. 7b, COD removal percentage versus operation time is shown. This parameter ranged between 40% and 90%. Finally, the COD removal rate versus time can be observed in Fig. 7c, it varied between 15 and 40 mg O2 h1. The variations of these variables were due to the change of operation conditions in different experiments. Considering the aforementioned results (cell voltage, COD percentage and removal rate), it can be stated that the photosynthetic microbial fuel cell was effectively abating COD and producing electricity during 10 months with no dead times (avoiding reinoculations or any other operational problems). Concerning electricity production, the system has demonstrated to be robust and stable, with the additional advantage of effectively treating the

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