dark regimes on the performance of photosynthetic microalgae microbial fuel cell

Bioresource Technology 261 (2018) 350–360

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The effect of different light intensities and light/dark regimes on the performance of photosynthetic microalgae microbial fuel cell

T

⁎

Elahe Bazdara, Ramin Roshandela, , Soheila Yaghmaeib, Mohammad Mahdi Mardanpourc a

Department of Energy Engineering, Sharif Energy Research Institute, Sharif University of Technology, Tehran, Iran Department of Chemical and Petroleum Engineering, Sharif Chemical and Petroleum Research Institute, Sharif University of Technology, Tehran, Iran c Technology and Innovation Group, Faculty of Technology, Research Institute of Petroleum Industry (RIPI), Tehran, Iran b

G R A P H I C A L A B S T R A C T

A R T I C LE I N FO

A B S T R A C T

Keywords: Photosynthesis microalgae microbial fuel cell Chlorella vulgaris Light intensity Light/dark regime Polarization

This study develops a photosynthetic microalgae microbial fuel cell (PMMFC) engaged Chlorella vulgaris microalgae to investigate effect of light intensities and illumination regimes on simultaneous production of bioelectricity, biomass and wastewater treatment. The performance of the system under different light intensity (3500, 5000, 7000 and 10,000 lx) and light/dark regimes (24/00, 12/12, 16/8 h) was investigated. The optimum light intensity and light/dark regimes for achieving maximum yield of PMMFC were obtained. The maximum power density of 126 mW m−3, the coulombic efficiency of 78% and COD removal of 5.47% were achieved. The maximum biomass concentration of 4 g l−1 (or biomass yield of 0.44 g l−1 day−1) was obtained in continuous light intensity of 10,000 lx. The comparison of the PMMFC performance with air–cathode and abiotic-cathode MFCs shows that the maximum power density of air-cathode MFC was only 13% higher than PMMFC.

1. Introduction Photosynthetic microalgae microbial fuel cell (PMMFC) is an attractive technology in academic research (Baicha et al., 2016; He et al., 2017; Luo et al., 2017; Saba et al., 2017; Saratale et al., 2017) that using microalgae with the aim of supplying substrates in the anodic ⁎

Corresponding author. E-mail address: [email protected] (R. Roshandel).

https://doi.org/10.1016/j.biortech.2018.04.026 Received 1 February 2018; Received in revised form 5 April 2018; Accepted 6 April 2018 Available online 10 April 2018 0960-8524/ © 2018 Elsevier Ltd. All rights reserved.

compartment (Dong et al., 2017; Salar-García et al., 2016; Walter et al., 2015; Xu et al., 2015), oxygen production in cathodic compartment (Colombo et al., 2017; Gajda et al., 2015; Rago et al., 2017), wastewater treatment (Commault et al., 2017; Yang et al., 2018), biofuels production (Khandelwal et al., 2018; Ma et al., 2017; Uggetti & Puigagut, 2016) and carbon dioxide capturing (Hu et al., 2015; Ma

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(2015) studied the MFC that oxygen required for cathode reduction reaction provided from atmospheric and alga breath from alga bioreactor (ABR). The investigation of the effect of different DO concentration on potential, power density and internal resistance of MFCs showed that the MFC with oxygen concentration of 39.2% produced from ABR generated approximately 30% higher power density than MFC engaged with atmospheric. The review of previous studies that focus on assessment of PMMFC performance, suggest that there is an optimal light intensity and light/ dark regime. These depend on the configuration of PMMFC elements, the operational parameters and biological conditions of microalgae species. To the best of author's knowledge, there is no complete study on that involves light intensities and light/dark regimes on PMMFC performance, simultaneously. The main objective of this study is to present a suitable and complete illumination pattern in terms of electricity generation, wastewater treatment and biomass production simultaneously. The optimum light intensity and light/dark regimes for achieving maximum yield of PMMFC were investigated. An integrated energy system based on MFC and microalgae bioreactor is designed and as well as assessment of microalgae growth to improve the system efficiency, the effect of illumination on dissolve oxygen concentration in cathode compartment, electricity production, wastewater treatment and biomass production in the PMMFC utilizing Chlorella vulgaris microalgae were studied. In addition, three different MFC including air–cathode MFC, abiotic–cathode MFC and PMMFC developed to investigate the electrochemical and biological characteristics of all cells under different DO concentrations.

et al., 2015). The influence of light availability on the PMMFC performance is introduced as a substantial factor that may affect the microalgae growth as well as the amount of the released oxygen through metabolic pathways and photosynthesis of the microalgae (Luo et al., 2017; Saba et al., 2017; Saratale et al., 2017). The effect of light intensity (Gouveia et al., 2014; He et al., 2014; Juang et al., 2012; Wu et al., 2014), wave length (Lan et al., 2013), and illumination period (del Campo et al., 2015; Lobato et al., 2013; Wu et al., 2013; Xiao et al., 2012) on photo microbial fuel cells (MFCs) characteristics such as produced power, wastewater treatment efficiency and biomass production were investigated in previous studies (Naraghi et al., 2015). Wu et al. (2014) studied photo-MFCs performance inoculated with Desmodesmus sp. A8 algae via produced power under different light intensities. They concluded that an increase in the light intensity could enhance electricity production due to the rising of dissolved oxygen production. However, the effect of light intensities on the biomass production and wastewater treatment was not considered. Gouveia et al. (2014) investigated the effect of two different light intensities on the bioelectricity generation and biomass production in the PMMFC simultaneously using Chlorella vulgaris as biocatalyst in the cathodic compartment. They observed that an increase in light intensity from 26 to 96 μe m−2 s−1, leads to significant enhancement (about 6-fold) in power generation. They suggested that there is an optimal light intensity which may be related to microbial and operational conditions. Nevertheless, they did not determine optimal amount of light intensity. In contrast to this finding, Juang et al. (2012) reported that the PMMFC produced higher power density at lower light intensities. Their results indicated that a MFC in presence of light of 6 and 12 W showed higher potential, power density, coulombic efficiency compared to MFC in presence of light with higher power of 18 and 26 W. The effect of light intensity on biomass production for more clarification was not investigated. The effect of light/dark cycle on cell performance is another substantial point that could not be negligible in assessment of PMMFC performance. Wu et al. (2013) developed a PMMFC and investigated two kinds of cathode electrodes including carbon paper coated with platinum and carbon felt without platinum coating. A photo tubular reactor as the cathode compartment which uses Chlorella vulgaris as an oxygenator, illuminated continuously and under 16/8 h light/dark cycle at defined light intensity. Although, the produced power density under continuous illumination was 12.7% more than the produced power density under intermittent cycle, but intermittent illumination had positive effect on microalgae healthiness. As the dark period is necessary to maintain the health of the population of photosynthetic microorganisms, a decrease in duration of the light/dark cycle reduces the production of electricity and biomass. Therefore, the performance of the PMMFC under 16/8 h light/dark cycle was reported as optimal condition. It should be noted that in addition to assessment of PMMFC performance involves consideration of wastewater treatment and biomass production, the investigation of these operational parameters are critical that should be considered in future works. Del Campo et al. (2015) studied the photosynthetic MFC performance under same time of light/dark cycle (i.e. 12/12 h) during 10 months. In spite of the effluent characteristic such as chemical oxygen demand (COD) at the anodic compartment was constant, but during the light phase, the electricity generation was higher than dark phase. This was attributed to photosynthesis of microalgae and oxygen production that facilitated cathodic half reaction. It should be noted that the effect of the intermittent illumination on biomass production and determination optimum light/dark regime were not considered in their experiments. With regard to the importance of oxygen concentration in cathodic compartment and its critical role in cell performance, Kakarla et al.

2. Materials and methods 2.1. PMMFC construction A two-compartment MFC was designed and constructed with plexi glass and the cylindrical anodic and cathodic compartments were fabricated with dimensions of internal diameter of 7.1 cm; exterior diameter of 9 cm and height of 4 cm. The stainless steel mesh as anode electrode (with mesh size of 400, length of 70 cm, width of 3.5 cm, and apparent surface area 245 cm2) is formed in spirally pattern in the anode compartment and connected to the external resistor using copper wire. Also the stainless steel mesh cathode electrode (with mesh size 400, diameter of 7 cm, width of 3.5 cm and apparent surface area 38.46 cm2) is formed in circularly and located next to the membrane and connected to the external resistor with copper wire. The anode and the cathode of the PMMFC were made of stainless steel mesh (SSM). The lower cost and higher mechanical strength compared with conventional material such as carbon cloth and graphite sheet, substantially decreased the overall construction cost and strengthen ease of application for fabrication of the PMMFC. Nafion 212 with a working area of 38.46 cm2 was used as the PMMFC membrane. For membrane activation, nafion was pretreated by submerging it into solutions of H2O2 3% (v/v), and washing with distilled water. Then, the pretreated membrane was protonated with H2SO4 0.5 M and distilled water for 1 h at 80 °C (Ghasemi et al., 2013). Finally, activated membrane was inserted between the anode and cathode compartments. The structure of abiotic–cathode MFC was the same as the PMMFC structure, but the cathodic compartment of abiotic–cathode MFC contained distillated water and phosphate buffer (4.58 g l−1 Na2HPO4, 2.45 g l−1 NaH2PO4·H2O, 0.31 g l−1 NH4Cl, 0.13 g l−1 KCl). It should be noted that all parts of the air–cathode MFC was fabricated with the same procedure of the PMMFC and the abiotic–cathode MFC but there was no cathodic compartment for the air–cathode MFC. 2.2. PMMFC microbial culture The municipal wastewater as PMMFC substrate was obtained from 351

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Fig. 1. (a) Schematic of the designed experimental setup and different structures of MFCs including (b) air–cathode MFC, (c) PMMFC, and (d) abiotic–cathode MFC.

(equivalent to 1.9 g l−1 dry weight biomass). Then at the beginning of experiments same concentration of Chlorella vulgaris (OD680nm = 0.8) was inoculated to cathode compartment of PMMFC to supply oxygen. It should be noted that the assessment of microalgae performance at out of PMMFC was done using a bioreactor as a parallel setup which was inoculated and operated in the same control conditions.

the initial sedimentation pond of the southern wastewater treatment plant in Tehran, with following characteristics: COD of 500 mg l−1, pH of 7.4 and conductivity of 15.3 ms cm−1. The PMMFC was operated under batch mode PMMFC and inoculated with facultative anaerobic sludge that acquired from the last sedimentation tank of the wastewater treatment unit. The adaptation of the electrogenesis bacteria was carried out using a 2:3 mixture of activated sludge as inoculums to wastewater as medium. Chlorella vulgaris species was purchased from local microalgae of the Persian Gulf and cultivated in a modified BG11 medium with composition of 750 mg l−1 NaNO3 18 mg l−1 CaCl2·2H2O, 37.5 mg l−1 MgSO4·7H2O, 2 mg l−1 FeCl3·6H2O, 2.8 mg l−1 Na2·EDTA, 1.43 mg l−1 H3BO3, 0.11 mg l−1 ZnSO4·7H2O, 0.905 mg l−1 MnCl2·H2O, (NH 4)6 Mo7 O24 . 4H2 O,0.04 mg l−1 0.196 mg l−1 CuSO4·5H2O, 0.0252 mg l−1 Co(NO3)2·6H2O, and 0.02 mg l−1 K2HPO4. Before inoculation, the Chlorella vulgaris was pre-cultured in a bubble column glass reactor (with volume of 3 lit) under continuous illumination fluorescent lamps of 18 W and at temperature of 26 °C. By applying a light intensity of 7000 lx and agitated by aeration using a compressed, the optical density (OD680nm) of the microalgae culture reached 2

2.3. Operational condition of PMMFC The cathodic compartment of PMMFC played the role of photobioreactor (PBR) for growth of Chlorella vulgaris microalgae. For each experiment, the anode compartment was fed with 100 ml of fresh wastewater and inoculated with 50 ml of activated sludge while the cathode compartment was filled by 140 ml of Chlorella vulgaris with BG11 culture medium at initial OD680nm of 0.8. It is need to period of 12 days for growth of Chlorella vulgaris and approaching stationary phase in the cathode compartment as well as in the bioreactor. All of experiments are carried out at the same operational conditions and ambient temperature of 25 ± 2 °C. The pH of the microalgae culture medium was also measured daily and it was controlled to 7–8. Aeration 352

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l−1) and the number of microalgae cells (N/cells ml−1) during growth period based on OD680 nm was estimated as follow:

of the cathode compartment and bioreactor to supply inorganic carbon source for microalgae growth was done using aeration pump. Illumination was supplied by a 15 W bubble fluorescent lamp (Philips) with a white light and a timer is used to adjust light/dark periods. The total biomass concentration, dissolve oxygen of cathode compartment and COD removal of influent/effluent were measured. It should be noted that the amount of COD was measured at maximum power densities using the closed refluxing method (He et al., 2014).

W = 0.9604OD + 0.0243

(2)

N = 1.7878OD−0.0894

(3)

The specific microalgae growth rate (day−1) is calculated by Eq. (4):

ln μ=

2.4. Process monitoring

t2−t1

(4)

3. Results and discussions 3.1. Effect of light intensity on electrochemical characteristics of PMMFC PMMFC operation was initiated under open circuit potential (OCP) conditions. The inoculation of the PMMFC was done under open circuit potential (i.e. infinite resistance). At the highest external resistance, the formation of effective biofilm with uniform morphology which expedites electron production and transfer has been demonstrated in previously published results (Mardanpour et al., 2012; Zhang et al., 2011). Fig. 2a shows OCP evolution of PMMFC in various light intensities. The results show that after approximately 58 h, the OCPs of PMMFC in presence of light with intensities of 3500, 5000, 7000 and 10000 lx increased gradually from the initial values to sustained values of 509, 544, 524, 465 ± 4 mV, respectively. Approaching the sustained potential may be contributed to this point that the concentration of exoelectrogenic microorganisms has reached an acceptable level and microbial enrichment was successfully done (Naraghi et al., 2015). The effect of external resistance on the biofilm formation and bioelectricity production during the inoculation period were assessed by Zhang et al. (2011). It was stated that in a lower external resistance, more accumulated active biofilm was formed but the biofilm established at higher external resistance appeared uniform compared with the lower external resistance. Therefore, the PMMFC operation was initiated under OCP conditions and the cell potential was monitored. According to Nernst’s equation, any variation in the activation of species in the redox reaction would change the OCP. So, to assess the microbial enrichment, by changing the substrate and suspended bacteria concentrations to excess level, approaching the sustained OCP was chosen as the characteristic of the appropriate concentration of exoelectrogenic microorganisms. Besides, after OCP monitoring, by applying the external resistance to the circuit of the PMMFC and feeding substrate and bacteria consortium at excess concentrations, the substantial variation in the trend of current evolution was not observed. Therefore, the sustained OCP could infer as a characteristic of the microbial enrichment (Mardanpour et al., 2012; Mardanpour & Yaghmaei, 2016; Naraghi et al., 2015; Zhang et al., 2011). The results clearly indicate an increase in OCP with enhancement of light intensity. The highest and lowest values of the OCP obtained at a light intensity of 5000 and 10000 lx, respectively. This implied the presence of optimum value for concentration of dissolved oxygen in the cathodic compartment (Juang et al., 2012). An increase in dissolved oxygen concentration as a result of light intensity enhancement from 3500 to 5000 lx, leads to increase in the cathode potential that consequently increases OCP. By rising the light intensity from 5000 to 10000 lx and as a result increasing the concentration of oxygen, the mass transfer of proton through system membrane limits and diffusion of oxygen from cathode to anode increases that eventually increases the anode potential and reduces the OCP (Kakarla et al., 2015). It should be noted that the monitoring of sustained current density evolution to show approaching the sustainability performance of the system was done after microbial cultivation and recording of OCP

t

MS × ∫0 b Idt F ×bes × vAn × ΔCOD

W2 W2

where μ represents the growth rate; t denotes time duration (day); and W is the dry weight of biomass (g l−1).

The effect of different light intensities of 3500, 5000, 7000 and 10000 lx on performance of the PMMFC was investigated by varying the distance between 15 W fluorescent lamp and cathodic compartment during continuous illumination. Afterwards, by selecting the optimal light intensity, the light/dark regimes of 16/8 and 12/12 h were applied and the variations of PMMFC characteristics were compared with the continuous light regime. It should be noted that during all experiments, the anodic compartment was coated with an aluminum foil to prevent the growth of photosynthetic microorganism and oxygen production that might have limited the power generation. The intensity of light was measured by the LUX-meter (testo435 manufactured by the testo Corp, Germany, with an accuracy of ± 0.06 lx). The concentration of Chlorella vulgaris suspension based on OD at 680 nm was measured using a Lambda 25 UV/VS spectrophotometer (manufactured by Perkin Elmer Company, with an accuracy of ± 0.01 nm). Temperature, pH and dissolved oxygen (DO) of catholyte were measured by triple sensors of YK-2001 DO (manufactured by Taiwan Lutron Company with accuracy of ± 0.8 °C, ± 0.02 (for pH) and ± 0.1 mg l−1 (for DO)). The cell potential was recorded at 30 min intervals using a digital multi-meter (Fluke, 289/FVF made by the American Fluke Company with an accuracy of ± 0.025 mV (DC Voltage)). The variable external resistance (with the range of 10 Ω to 5000 kΩ) was used to polarize PMMFC and calculated current and power at each resistance were normalized with the anolyte volume. Internal resistance was calculated using the slop of polarization curve (Juang et al., 2012; Lefebvre et al., 2011). It should be noted that assessment of the PMMFC performance was done based on the galvanostatic method (Damaskin, 1967). Therefore, the overall cell potential was monitored to investigate the effect of all overpotentials of the cell performance. To assess the PMMFC performance based on the potentiostatic method, the measurement of anode potential under the control conditions in view point of investigation of microalgae performance can be the subject of future works. Fig. 1 shows a schematic of the designed experimental setup (i.e. Fig. 1a) and different structures of MFC including air–cathode MFC (Fig. 1b), PMMFC (Fig. 1c), and abiotic–cathode MFC (Fig. 1d). The coulombic efficiency (CE) was calculated using Eq. (1):

CE =

( )

(1)

−1

where, Ms (g gmol ) = 32 is the molecular weight of oxygen; I (mA) denotes the current passing through the system; F represents the Faraday’s constant (96500 C mole−1); bes = 4 is the number of electrons interchanged per mole of oxygen; VAn (ml) = 158 is the working volume of anode compartment; and ΔCOD (mg l−1) denotes the variation of organic content in a closed cycle over operating period (Juang et al., 2012). For calculation of produced biomass, the suspension of Chlorella vulgaris (in specific OD) was centrifuged at 4000 rpm and for 20 min using RST24 centrifuge machine. The precipitated part was dried inside oven at 80 °C for 2 h and finally after weighting, dry weight of produced biomass was reported. The cell counting was done by optical microscope under magnification of 100. The amounts of dry weight (W/g 353

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Fig. 2. Effect of different light intensities on (a) open circuit potential (OCP), (b) current density evolution at external resistance of 850 Ω, (c) polarization & power density, and (d) the dissolved oxygen concentration in cathodic compartment at external resistance of 1000 Ω. The error bars show the variation of parameters among triplicate experiments.

amount of dissolved oxygen inside the cathodic compartment from 7.8 to 9.5 mg l−1. As can be seen, at a light intensity of 10000 lx, the power density is 59 mW m−3, which is 53.4% less than the power density at 5000 lx. It might be explained that higher light intensity leads to a light saturation phenomenon, or photo-inhibition, which damages the cell growth of microalgae (Cheirsilp & Torpee, 2012; He et al., 2014). Another problem that associated with produced current reduction is accumulation of the dissolved oxygen that enhances of oxygen bubble pressure in cathodic compartment (Chai & Zhao, 2012; He et al., 2014). This may contribute to back diffusion of oxygen to anodic compartment that consequently decreases power generation. The variation of produced current density and concentration of dissolved oxygen in a cathodic compartment under the light intensities of 3500 lx up to 10000 lx were shown in Fig. 2d. Effect of light intensity on the growth of the microalgae can be divided into four phases including lag, light limitation, light saturation, and light inhibition phases. Therefore, the influent of light intensity on the PMMFC

under excess concentration of the organic substrate. As shown in Fig. 2b, the highest value of produced current density at external resistance of 850 Ω in presents of the cell overpotentials was achieved (Mardanpour et al., 2012). The polarization and power density curves of PMMFC under different light intensities were shown in Fig. 2c. As can be seen, at light intensities of 5000 lx and 10000 lx, the highest and lowest values of power densities were obtained, respectively. Similar to analysis of OCP curves, the effect of light intensity on the photosynthesis process and subsequently microalgae growth and oxygen production in cathodic compartment, were significant. Since, the growth of microalgae occurs under autotrophic conditions, the light intensity plays a critical role. By increasing light intensity from 3500 to 5000 lx, the maximum of produced power density increases and reaches 126 mW m−3 as maximum obtained power density of system. Further increase in light intensity leads to a decrease in power density. As shown in Fig. 2d, an increase in the light intensity from 3500 lx to 10000 lx, increased the

354

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2014). In addition, the reduction of OCP in high light intensities (544 mV at light intensity of 5000 lx and 465 mV at light intensity of 10000 lx) endorses this subject. Fig. 3b shows the growth curves of Chlorella vulgaris microalgae in a cathodic compartment of PMMFC under various light intensities. As it is known, with increasing the light intensity, amount of the microalgae cells enhanced, but its life time (due to increasing growth rate) decreased and the microalgae reach its stationary phase in shorter time. As can been observed, for light intensity of 3500, 5000 and 10000 lx, the microalgae growth approached the stationary phase on the 12th, 11th, and 9th day of growth during system operation, respectively. This indicates an increase in light intensity, decreased the growth rate of the microalgae and the ceased phase of microalgae growth (i.e. stationary phase) was achieved in the lower operating time. This may be due to damage to the microalgae cells under high light intensity, which disrupt the intracellular performance and decreases its growth rate than before. Several studies have also shown that as a result of augmented oxygen concentrations in the cathodic compartment, the potential of hydrogen peroxide formation increased. Therefore, the risk of cell damage may be increased by oxidation of the protein that the microalgae performance is limited and prohibited (Cai et al., 2013; Wang et al., 2013). Fig. 3c shows the growth rate of the Chlorella vulgaris in the cathodic compartment of the PMMFC and in the PBR without cathode electrode. As can be seen, with increasing light intensity, the microalgae growth rate increases in both systems, but inclines of growth rate curve were decreased in higher light intensities. Besides, the produced biomass in the cathodic compartment of PMMFC is lower than amount of it in the PBR. This may be attributed to the microalgae biomass loss due to stick on different parts of the cathodic compartment of the PMMFC enclosure (including the cathode electrode, proton exchange membrane, and the membrane protector) and/or environmental factors such as pH of cathodic compartment of the PMMFC and temperature variation. The maximum concentration of biomass in the cathodic compartment of PMMFC about 4.0 g l−1 was obtained in light intensity of 10000 lx (Fig. 3d). The difference between the growth rates and biomass concentration in the cathodic compartment of PMMFC and PBR compensated at high light intensities. This suggests that by increasing the light intensity, PMMFC can act as a biological reactor for growth of microalgae.

performance may also be categorized as four phases: (1) lag phase in which enhancement of light intensity does not change produced current; (2) light limitation phase, when the enhancement of light intensity increases produced current; (3) light saturation phase, in which enhancement of light intensity does not change produced current; (4) finally, light inhibition phase, in which increasing light intensity decrease produced current (Wu et al., 2014). As shown in Fig. 2d, the light limitation phase, light saturation phase and light inhibition phase occurred when the light intensity raised from 3500 to 5000 lx, from 5000 to 7000 lx (due to a slope) and from 7000 lx to 10000, respectively. The light intensity between 5000 and 6500 lx can be ascribed as optimum range for Chlorella vulgaris photosynthesis and maximum power generation in the PMMFC. The similar conclusion has been reported in study of He et al. (He et al., 2014). Although, the effect of light intensity on microalgae growth depends culture conditions and genetic makeup (Wu et al., 2014), but generally, the appropriate light intensity promotes the photosynthetic activity, as well as the production of available oxygen for cathodic reaction of the PMMFC (He et al., 2014; Juang et al., 2012). Therefore, the power density does not always increase with increasing light intensity. Since the oxygen concentration in the cathode compartment has an optimal amount (as shown in Fig. 2d was about 8.4 mg l−1 at light intensity of 5000 lx), enhancement of oxygen concentration from defined dosage reduces the power generation. This is substantial subject in high-scale applications and cost engineering considerations to choose an optimal light intensity (Gouveia et al., 2014). 3.2. Effect of light intensity on COD removal, coulombic efficiency and biomass production Fig. 3a shows the COD removal and coulombic efficiency of PMMFC in different light intensities. Although the maximum variation of COD removal efficiency was about 1.3% but the variation of coulombic efficiency was about 30% that indicates the significant role of light illumination in current production. Maximum coulombic efficiencies of 78% and 48% were obtained at light intensities of 5000 and 10000 lx, respectively. As coulombic efficiency is a function of current generation and COD removal, it variation substantially affects by rate of electron production than anolyte organic content. The COD removal strongly depends on the bacterial activity and organic content of the MFC. The activity of the PMMFC biocatalysts in presence of high organic content involves longer operating time of the system. In the other hand, the activity of the MFC bacteria through the biodegradation sequence of complex organic substrates affects the COD removal (Singhvi & Chhabra, 2013). The similar results and conclusion have been reported in the study of Min & Logan (2004) for investigation the biodegradation of different substrates in the MFC. They reported only 8% COD removal and coulombic efficiency of 65% for acetate, 3% COD removal and coulombic efficiency of 28% for butyrate and 10% COD removal and coulombic efficiency of 50% for domestic wastewater with butyrate under the same conditions. The low COD removal in contrast to the relative high coulombic efficiency was attributed to the activity of exoelectrogenic bacteria. The variation of current density attributed to intensification of microalgae growth, the variation of oxygen concentration (as electron acceptor) and back diffusion of oxygen to anolyte compartment. As mentioned, an increase in light intensity leads to enhancement of oxygen-related photosynthetic efficiency, which consequently decreases cathodic resistance (Wu et al., 2014). In the other hand, augmentation of dissolved oxygen concentration inside the cathodic compartment leads to penetration of oxygen from the membrane into the anodic compartment that decreases produced current (He et al., 2014). The enhancement of internal resistance of cell which increased from 661 Ω in a light intensity of 5000 lx, to 1142 Ω at the light intensity of 10000 lx, indicating oxygen accumulation as electron transfer barriers was another reason of the decrease in power generation (He et al.,

3.3. Effect of light/dark regime on electrochemical characteristics of PMMFC The effect of light/dark cycles was done to evaluate the influential of intermittent illumination on the PMMFC performance. The different light/dark regimes of 12/12, 16/8, and 24/00 h were applied at optimal light intensity of 5000 lx. Fig. 4a shows the current density evolution at external resistance of 850 Ω under different light/dark regimes. Power density and polarization curves under different light/dark regimes are shown in Fig. 4b. With respect to Fig. 4a and b, the results showed that an increase in illumination period had a positive effect on the power generation. During the light phase, microalgae carry out the photosynthesis that consequently capture carbon dioxide and release oxygen for progression of the cathode reaction. Maximum power densities of 126, 112 and 72 mW m−3 were obtained in 24/00, 16/8, 12/ 12 h of light/dark regimes, respectively. Under continuous illumination, the maximum power density was 12.7% and 74.8% higher than produced power densities in the intermittent illumination of 16/8 and 12/12 h, respectively. These results are in agreement with study of Wu et al. (2014) investigated photo MFC performance under 12/12 h light/ dark cycle. In should be noted that in their work, the produced power densities under illumination was more than 5.6 fold in the absence of light, while the enhancement of power density of the PMMFC was about 1.68 fold. These results seem logical because the carbon dioxide gas for Chlorella vulgaris growth in cathode compartment of the PMMFC was 355

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Fig. 3. Effect of different light intensity on (a) COD removal/coulombic efficiency, (b) optical density, (c) growth Rate of microalgae, and (d) biomass concentration of microalgae under continuous light regime. The error bars show the variation of data among triplicate experiments.

consumption the concentration of dissolved oxygen for 8/16 and 12/12 hr light/dark regimes decreased to 7.5 and 7.1 mg l−1, respectively. The variation of oxygen concentration may be due to the abnormal metabolism of microalgae cells when the dark phase abruptly replaces with light phase. As the microalgae cells need to turn their metabolic pathway to adapt to the continuous illumination, so a temporary disruption in photosynthesis and respiration of microalgae occurs, which result in the variation of the oxygen concentration in the cathodic compartment (Wu et al., 2013). After adaptation, the stable trend of the concentration oxygen in a certain range was observed.

supplied through aeration. Such an optical function is also observed for a MFC with Cyanobacterial microalgae (Pisciotta et al., 2010; Zou et al., 2009) and eukaryotic algae (Xiao et al., 2012). However, the MFC inoculated with Spirulina platensis, produced more bioelectricity in darkness than that in the light (Fu et al., 2009). With regards to this point that microalgae do not implement photosynthesis and oxygen production in the dark and even it consumes oxygen, this is favorite phenomena for anolyte of photo MFC that placed in the dark and produced electrons are not lost. These different results about of the effect of light on the PMMFC can be attributed to the fact that microalgae can play a different role in oxidation-reduction reactions in anode and cathode of the PMMFC. The variation of dissolved oxygen at the cathode compartment of the PMMFC during the light and dark phase is shown in Fig. 4c. For light/dark cycle of 24/0, 16/8 and 12/12 h the dissolved oxygen concentration in light phase were 8.4, 8.1 and 7.9 mg l−1, respectively. As microalgae during the dark phase carried out respiration and oxygen

3.4. Effect of light/dark regimes on COD removal, coulombic efficiency and biomass production Table 1 shows the different characteristics of the bioelectrochemical performance of the PMMFC versus various light regimes. Under light/ dark cycle of 24/00, 16/8 and 12/12 light regimes, the COD removals 356

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Fig. 4. Effect of different light regime on (a) current density evolution at external resistance of 850 Ω, (b) polarization and power density curves, and (c) dissolved oxygen concentration in cathodic compartment of the PMMFC at light intensity of 5000 lx. The error bars show the variation of experimental data among repeated experiments.

of produced oxygen due to changing illumination conditions. As the microalgae growth rate in the continuous illumination is higher than two other light/dark regimes, the maximum concentration of biomass (about 3.6 g l−1) was obtained in the continuous illumination. It should be noted that the effect of light period on biomass growth in cathodic compartment of the PMMFC and the PBR was similar to the results obtained from investigation of light intensity. With increasing light period, more biomass was obtained in both systems, but in the PBR, the variation of biomass concentration versus light period is negligible compared to the cathodic compartment of the PMMFC. It should be noted that investigation of PMMFC performance under

were measured 5.47%, 4.98%, and 4.09%, respectively. As can be seen, there is no significant difference in the variation of COD removals of the anodic compartment. The internal resistance of the PMMFC slightly increased from 661 Ω, in the continuous regime, to 732 and 1066 Ω, for the light/dark cycles of 16/8 and 12/12 h, respectively. During continuous illumination, the internal resistance is greater than the internal resistance of the two light/dark regimes. Besides, the maximum coulombic efficiency for the PMMFC of 78% was obtained in the continuous regimes and it was reduced to 57% for light/dark cycle of 12/12 h. These may be contributed to sudden shocks to the system and augmented concentration Table 1 The particular characteristics of the PMMFC at different light/dark regimes. Light/Dark Cycle (h)

Open Circuit Potential (mV)

Maximum Power Density (mW m−3)

Internal Resistance (Ω)

Coulombic Efficiency (%)

COD removal (%)

Biomass production in Cathodic Compartment of the PMMFC (g l−1)

Biomass production in the PBR (g l−1)

DO in cathodic Compartment in light (mg l−1)

Continuous 16/8 12/12

544 534 498

126 112 72

661 732 1066

78 72 57

5.47 4.98 4.09

3.6 3.2 2.7

4.0 3.9 3.7

8.4 8.1 7.9

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Fig. 5. (a) Open circuit potential (OCP), (b) current density evolutions at external resistance of 850 Ω and (c) power density curves of different MFC structures. The error bars show the variation of parameters among triplicate experiments.

difference in concentration overpotentials. As can be seen in Fig. 5b, the produced current density at external resistance of 850 Ω for air – cathode MFC which was 16% and 41% higher than PMMFC and abiotic–cathode MFC, respectively. In the other hand, the maximum power density of 140 mW m−3 was obtained for air–cathode MFC which was 10% and 65% higher than PMMFC and abiotic–cathode MFC, respectively (Fig. 5c). The higher power and current densities of air–cathode MFC may attribute to lower cathodic overpotential in which may related to the effective removal of produced water from half cathodic reaction. In addition, induced forced convection of oxygen in abiotic–cathode MFC and PMMFC can leads to augmented pressure of oxygen in cathodic compartment and back diffusion in anolyte to reduce power generation. As mentioned, the oxygen penetration into the anolyte raises the potential of the anode and/or prevents the passing of the proton from membrane and ultimately increases the internal resistance. Despite the lower power generation of PMMFC, the production of biomass in catholyte of cell, as feature for biofuel generation as well as the ability of wastewater treatment in view point of nitrogen and phosphorus removal can be contributed as a

different wavelengths of light, substrate concentrations, and scale up of the systems are another area for future research.

3.5. The comparison of PMMFC characteristics with abiotic-cathode MFC and air–cathode MFC Fig. 5a shows the OCP of different MFC structures. As can be seen in Fig. 5a, the maximum OCP of 453 ± 4 mV was obtained for air–cathode MFC after 85 h of cell operation. As the mechanical aeration and photosynthesis process play critical role in effective availability of oxygen and facilitate mass transfer through induced forced convection on cathode surface, the OCP of abiotic–cathode MFC and PMMFC, 544 ± 4 and 535 ± 4 mV, respectively. These results are in agreement with Kakarla et al. conclusions (Kakarla et al., 2015). With regard to assessment of different structure overpotentials, the current density evolutions at external resistance of 850 Ω, and the power density curves of MFC in the three structures was obtained and shown in Fig. 5b and c, respectively. The main features among the MFCs curves are related to descending trend indicate the substantial 358

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Table 2 The particular characteristics of the air – cathode MFC, PMMFC and abiotic–cathode MFC.

OCP (mV) Power Density (mW m−3) Internal Resistance (Ω) Dissolved Oxygen (mg l−1) Coulombic Efficiency (%) COD Removal (%)

Air–cathode MFC

PMMFC

Abiotic–cathode MFC

453 ± 4 140 515 20.8%

544 ± 4 126 662 8.4

535 ± 4 84 878 8

81 5.94

78 5.47

66 4.44

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significant advantage compared with air–cathode MFC (Colombo et al., 2017; Rago et al., 2017). The bioelectrochemical characteristics of PMMFC compared with air–cathode MFC and abiotic–cathode MFC are summarized in Table 2. As shown, in spite of low COD removal, the high values of coulombic efficiencies for different structures is the noticeable characteristic that can attribute to effective performance of cells to exploit substantial bioenergy from complex wastewater even in low organic content. The air–cathode MFC has lower internal resistance (about 515 Ω) compared with other structures. This may be due to the lack of catholyte and the lack of formation of sediment on the cathode side (Kakarla et al., 2015). 4. Conclusion The effects of light intensities and illumination regimes on PMMFC performance were investigated. The light intensity between 5000 and 6500 lx can be ascribed as optimum range for Chlorella vulgaris photosynthesis and maximum power generation in the PMMFC by changing the amount of dissolved oxygen in the cathode. It demonstrated that light/dark regimes can be useful for the stable performance of the PMMFC by increasing the microalgae's lifetime. Despite the lower power generation of PMMFC compared with air–cathode MFC, the production of biomass in catholyte of cell, as feature for biofuel generation can be contributed as a significant advantage. Acknowledgements The authors would like to thank Sharif Energy Research Institute (SERI) and The Biochemical and Bioenvironmental Engineering Center (BBRC) of Sharif University of Technology, Iran for their support through this project and for permission to use their facilities. References Baicha, Z., Salar-García, M.J., Ortiz-Martínez, V.M., Hernández-Fernández, F.J., de los Ríos, A.P., Labjar, N., Lotfi, E., Elmahi, M., 2016. A critical review on microalgae as an alternative source for bioenergy production: a promising low cost substrate for microbial fuel cells. Fuel Process. Technol. 154, 104–116. Cai, P.-J., Xiao, X., He, Y.-R., Li, W.-W., Zang, G.-L., Sheng, G.-P., Hon-Wah Lam, M., Yu, L., Yu, H.-Q., 2013. Reactive oxygen species (ROS) generated by cyanobacteria act as an electron acceptor in the biocathode of a bio-electrochemical system. Biosens. Bioelectron 39 (1), 306–310. Chai, X., Zhao, X., 2012. Enhanced removal of carbon dioxide and alleviation of dissolved oxygen accumulation in photobioreactor with bubble tank. Bioresour. Technol. 116, 360–365. Cheirsilp, B., Torpee, S., 2012. Enhanced growth and lipid production of microalgae under mixotrophic culture condition: effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour. Technol. 110, 510–516. Colombo, A., Marzorati, S., Lucchini, G., Cristiani, P., Pant, D., Schievano, A., 2017. Assisting cultivation of photosynthetic microorganisms by microbial fuel cells to enhance nutrients recovery from wastewater. Bioresour. Technol. 237, 240–248. Commault, A.S., Laczka, O., Siboni, N., Tamburic, B., Crosswell, J.R., Seymour, J.R., Ralph, P.J., 2017. Electricity and biomass production in a bacteria-Chlorella based microbial fuel cell treating wastewater. J. Power Sources 356, 299–309. Damaskin, B.B., 1967. The Principles of Current Methods for the Study of Electrochemical Reactions. McGraw-Hill. del Campo, A.G., Perez, J.F., Cañizares, P., Rodrigo, M.A., Fernandez, F.J., Lobato, J., 2015. Characterization of light/dark cycle and long-term performance test in a photosynthetic microbial fuel cell. Fuel 140, 209–216.

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