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Bioresource Technology 261 (2018) 350–360

Contents lists available at ScienceDirect

Bioresource Technology
journal homepage: www.elsevier.com/locate/biortech

The effect of different light intensities and light/dark regimes on the T


performance of photosynthetic microalgae microbial fuel cell

Elahe Bazdara, Ramin Roshandela, , Soheila Yaghmaeib, Mohammad Mahdi Mardanpourc
a
Department of Energy Engineering, Sharif Energy Research Institute, Sharif University of Technology, Tehran, Iran
b
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

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: This study develops a photosynthetic microalgae microbial fuel cell (PMMFC) engaged Chlorella vulgaris mi-
Photosynthesis microalgae microbial fuel cell croalgae to investigate effect of light intensities and illumination regimes on simultaneous production of bioe-
Chlorella vulgaris lectricity, biomass and wastewater treatment. The performance of the system under different light intensity
Light intensity (3500, 5000, 7000 and 10,000 lx) and light/dark regimes (24/00, 12/12, 16/8 h) was investigated. The op-
Light/dark regime
timum light intensity and light/dark regimes for achieving maximum yield of PMMFC were obtained. The
Polarization
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 compartment (Dong et al., 2017; Salar-García et al., 2016; Walter et al.,
2015; Xu et al., 2015), oxygen production in cathodic compartment
Photosynthetic microalgae microbial fuel cell (PMMFC) is an at- (Colombo et al., 2017; Gajda et al., 2015; Rago et al., 2017), waste-
tractive technology in academic research (Baicha et al., 2016; He et al., water treatment (Commault et al., 2017; Yang et al., 2018), biofuels
2017; Luo et al., 2017; Saba et al., 2017; Saratale et al., 2017) that production (Khandelwal et al., 2018; Ma et al., 2017; Uggetti &
using microalgae with the aim of supplying substrates in the anodic Puigagut, 2016) and carbon dioxide capturing (Hu et al., 2015; Ma


Corresponding author.
E-mail address: roshandel@sharif.edu (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.
E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

et al., 2015). (2015) studied the MFC that oxygen required for cathode reduction
The influence of light availability on the PMMFC performance is reaction provided from atmospheric and alga breath from alga bior-
introduced as a substantial factor that may affect the microalgae growth eactor (ABR). The investigation of the effect of different DO con-
as well as the amount of the released oxygen through metabolic path- centration on potential, power density and internal resistance of MFCs
ways and photosynthesis of the microalgae (Luo et al., 2017; Saba et al., showed that the MFC with oxygen concentration of 39.2% produced
2017; Saratale et al., 2017). from ABR generated approximately 30% higher power density than
The effect of light intensity (Gouveia et al., 2014; He et al., 2014; MFC engaged with atmospheric.
Juang et al., 2012; Wu et al., 2014), wave length (Lan et al., 2013), and The review of previous studies that focus on assessment of PMMFC
illumination period (del Campo et al., 2015; Lobato et al., 2013; Wu performance, suggest that there is an optimal light intensity and light/
et al., 2013; Xiao et al., 2012) on photo microbial fuel cells (MFCs) dark regime. These depend on the configuration of PMMFC elements,
characteristics such as produced power, wastewater treatment effi- the operational parameters and biological conditions of microalgae
ciency and biomass production were investigated in previous studies species. To the best of author's knowledge, there is no complete study
(Naraghi et al., 2015). on that involves light intensities and light/dark regimes on PMMFC
Wu et al. (2014) studied photo-MFCs performance inoculated with performance, simultaneously.
Desmodesmus sp. A8 algae via produced power under different light The main objective of this study is to present a suitable and com-
intensities. They concluded that an increase in the light intensity could plete illumination pattern in terms of electricity generation, wastewater
enhance electricity production due to the rising of dissolved oxygen treatment and biomass production simultaneously. The optimum light
production. However, the effect of light intensities on the biomass intensity and light/dark regimes for achieving maximum yield of
production and wastewater treatment was not considered. PMMFC were investigated. An integrated energy system based on MFC
Gouveia et al. (2014) investigated the effect of two different light and microalgae bioreactor is designed and as well as assessment of
intensities on the bioelectricity generation and biomass production in microalgae growth to improve the system efficiency, the effect of illu-
the PMMFC simultaneously using Chlorella vulgaris as biocatalyst in mination on dissolve oxygen concentration in cathode compartment,
the cathodic compartment. They observed that an increase in light in- electricity production, wastewater treatment and biomass production in
tensity from 26 to 96 μe m−2 s−1, leads to significant enhancement the PMMFC utilizing Chlorella vulgaris microalgae were studied. In ad-
(about 6-fold) in power generation. They suggested that there is an dition, three different MFC including air–cathode MFC, abiotic–cathode
optimal light intensity which may be related to microbial and opera- MFC and PMMFC developed to investigate the electrochemical and
tional conditions. Nevertheless, they did not determine optimal amount biological characteristics of all cells under different DO concentrations.
of light intensity.
In contrast to this finding, Juang et al. (2012) reported that the 2. Materials and methods
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 2.1. PMMFC construction
higher potential, power density, coulombic efficiency compared to MFC
in presence of light with higher power of 18 and 26 W. The effect of A two-compartment MFC was designed and constructed with plexi
light intensity on biomass production for more clarification was not glass and the cylindrical anodic and cathodic compartments were fab-
investigated. ricated with dimensions of internal diameter of 7.1 cm; exterior dia-
The effect of light/dark cycle on cell performance is another sub- meter of 9 cm and height of 4 cm. The stainless steel mesh as anode
stantial point that could not be negligible in assessment of PMMFC electrode (with mesh size of 400, length of 70 cm, width of 3.5 cm, and
performance. Wu et al. (2013) developed a PMMFC and investigated apparent surface area 245 cm2) is formed in spirally pattern in the
two kinds of cathode electrodes including carbon paper coated with anode compartment and connected to the external resistor using copper
platinum and carbon felt without platinum coating. A photo tubular wire. Also the stainless steel mesh cathode electrode (with mesh size
reactor as the cathode compartment which uses Chlorella vulgaris as an 400, diameter of 7 cm, width of 3.5 cm and apparent surface area
oxygenator, illuminated continuously and under 16/8 h light/dark 38.46 cm2) is formed in circularly and located next to the membrane
cycle at defined light intensity. Although, the produced power density and connected to the external resistor with copper wire.
under continuous illumination was 12.7% more than the produced The anode and the cathode of the PMMFC were made of stainless
power density under intermittent cycle, but intermittent illumination steel mesh (SSM). The lower cost and higher mechanical strength
had positive effect on microalgae healthiness. As the dark period is compared with conventional material such as carbon cloth and graphite
necessary to maintain the health of the population of photosynthetic sheet, substantially decreased the overall construction cost and
microorganisms, a decrease in duration of the light/dark cycle reduces strengthen ease of application for fabrication of the PMMFC.
the production of electricity and biomass. Therefore, the performance Nafion 212 with a working area of 38.46 cm2 was used as the
of the PMMFC under 16/8 h light/dark cycle was reported as optimal PMMFC membrane. For membrane activation, nafion was pretreated by
condition. It should be noted that in addition to assessment of PMMFC submerging it into solutions of H2O2 3% (v/v), and washing with dis-
performance involves consideration of wastewater treatment and bio- tilled water. Then, the pretreated membrane was protonated with
mass production, the investigation of these operational parameters are H2SO4 0.5 M and distilled water for 1 h at 80 °C (Ghasemi et al., 2013).
critical that should be considered in future works. Finally, activated membrane was inserted between the anode and
Del Campo et al. (2015) studied the photosynthetic MFC perfor- cathode compartments.
mance under same time of light/dark cycle (i.e. 12/12 h) during The structure of abiotic–cathode MFC was the same as the PMMFC
10 months. In spite of the effluent characteristic such as chemical structure, but the cathodic compartment of abiotic–cathode MFC con-
oxygen demand (COD) at the anodic compartment was constant, but tained distillated water and phosphate buffer (4.58 g l−1 Na2HPO4,
during the light phase, the electricity generation was higher than dark 2.45 g l−1 NaH2PO4·H2O, 0.31 g l−1 NH4Cl, 0.13 g l−1 KCl). It should be
phase. This was attributed to photosynthesis of microalgae and oxygen noted that all parts of the air–cathode MFC was fabricated with the
production that facilitated cathodic half reaction. It should be noted same procedure of the PMMFC and the abiotic–cathode MFC but there
that the effect of the intermittent illumination on biomass production was no cathodic compartment for the air–cathode MFC.
and determination optimum light/dark regime were not considered in
their experiments. 2.2. PMMFC microbial culture
With regard to the importance of oxygen concentration in cathodic
compartment and its critical role in cell performance, Kakarla et al. The municipal wastewater as PMMFC substrate was obtained from

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

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.

the initial sedimentation pond of the southern wastewater treatment (equivalent to 1.9 g l−1 dry weight biomass). Then at the beginning of
plant in Tehran, with following characteristics: COD of 500 mg l−1, pH experiments same concentration of Chlorella vulgaris (OD680nm = 0.8)
of 7.4 and conductivity of 15.3 ms cm−1. The PMMFC was operated was inoculated to cathode compartment of PMMFC to supply oxygen. It
under batch mode PMMFC and inoculated with facultative anaerobic should be noted that the assessment of microalgae performance at out
sludge that acquired from the last sedimentation tank of the wastewater of PMMFC was done using a bioreactor as a parallel setup which was
treatment unit. The adaptation of the electrogenesis bacteria was car- inoculated and operated in the same control conditions.
ried out using a 2:3 mixture of activated sludge as inoculums to was-
tewater as medium. 2.3. Operational condition of PMMFC
Chlorella vulgaris species was purchased from local microalgae of the
Persian Gulf and cultivated in a modified BG11 medium with compo- The cathodic compartment of PMMFC played the role of photo-
sition of 750 mg l−1 NaNO3 18 mg l−1 CaCl2·2H2O, 37.5 mg l−1 bioreactor (PBR) for growth of Chlorella vulgaris microalgae. For each
MgSO4·7H2O, 2 mg l−1 FeCl3·6H2O, 2.8 mg l−1 Na2·EDTA, 1.43 mg l−1 experiment, the anode compartment was fed with 100 ml of fresh
H3BO3, 0.11 mg l−1 ZnSO4·7H2O, 0.905 mg l−1 MnCl2·H2O, wastewater and inoculated with 50 ml of activated sludge while the
0.196 mg l−1 (NH 4)6 Mo7 O24 . 4H2 O,0.04 mg l−1 CuSO4·5H2O, cathode compartment was filled by 140 ml of Chlorella vulgaris with
0.0252 mg l−1 Co(NO3)2·6H2O, and 0.02 mg l−1 K2HPO4. Before in- BG11 culture medium at initial OD680nm of 0.8. It is need to period of
oculation, the Chlorella vulgaris was pre-cultured in a bubble column 12 days for growth of Chlorella vulgaris and approaching stationary
glass reactor (with volume of 3 lit) under continuous illumination phase in the cathode compartment as well as in the bioreactor. All of
fluorescent lamps of 18 W and at temperature of 26 °C. By applying a experiments are carried out at the same operational conditions and
light intensity of 7000 lx and agitated by aeration using a compressed, ambient temperature of 25 ± 2 °C. The pH of the microalgae culture
the optical density (OD680nm) of the microalgae culture reached 2 medium was also measured daily and it was controlled to 7–8. Aeration

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

of the cathode compartment and bioreactor to supply inorganic carbon l−1) and the number of microalgae cells (N/cells ml−1) during growth
source for microalgae growth was done using aeration pump. period based on OD680 nm was estimated as follow:
Illumination was supplied by a 15 W bubble fluorescent lamp (Philips) W = 0.9604OD + 0.0243 (2)
with a white light and a timer is used to adjust light/dark periods. The
total biomass concentration, dissolve oxygen of cathode compartment N = 1.7878OD−0.0894 (3)
and COD removal of influent/effluent were measured. It should be The specific microalgae growth rate (day−1) is calculated by Eq. (4):
noted that the amount of COD was measured at maximum power
densities using the closed refluxing method (He et al., 2014).
μ=
ln ( )
W2
W2

t2−t1 (4)
2.4. Process monitoring
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 3. Results and discussions
during continuous illumination. Afterwards, by selecting the optimal
light intensity, the light/dark regimes of 16/8 and 12/12 h were ap- 3.1. Effect of light intensity on electrochemical characteristics of PMMFC
plied and the variations of PMMFC characteristics were compared with
the continuous light regime. It should be noted that during all experi- PMMFC operation was initiated under open circuit potential (OCP)
ments, the anodic compartment was coated with an aluminum foil to conditions. The inoculation of the PMMFC was done under open circuit
prevent the growth of photosynthetic microorganism and oxygen pro- potential (i.e. infinite resistance). At the highest external resistance, the
duction that might have limited the power generation. formation of effective biofilm with uniform morphology which ex-
The intensity of light was measured by the LUX-meter (testo435 pedites electron production and transfer has been demonstrated in
manufactured by the testo Corp, Germany, with an accuracy of ± previously published results (Mardanpour et al., 2012; Zhang et al.,
0.06 lx). The concentration of Chlorella vulgaris suspension based on OD 2011).
at 680 nm was measured using a Lambda 25 UV/VS spectrophotometer Fig. 2a shows OCP evolution of PMMFC in various light intensities.
(manufactured by Perkin Elmer Company, with an accuracy of ± 0.01 The results show that after approximately 58 h, the OCPs of PMMFC in
nm). Temperature, pH and dissolved oxygen (DO) of catholyte were presence of light with intensities of 3500, 5000, 7000 and 10000 lx
measured by triple sensors of YK-2001 DO (manufactured by Taiwan increased gradually from the initial values to sustained values of 509,
Lutron Company with accuracy of ± 0.8 °C, ± 0.02 (for pH) and ± 544, 524, 465 ± 4 mV, respectively. Approaching the sustained po-
0.1 mg l−1 (for DO)). tential may be contributed to this point that the concentration of
The cell potential was recorded at 30 min intervals using a digital exoelectrogenic microorganisms has reached an acceptable level and
multi-meter (Fluke, 289/FVF made by the American Fluke Company microbial enrichment was successfully done (Naraghi et al., 2015). The
with an accuracy of ± 0.025 mV (DC Voltage)). The variable external effect of external resistance on the biofilm formation and bioelectricity
resistance (with the range of 10 Ω to 5000 kΩ) was used to polarize production during the inoculation period were assessed by Zhang et al.
PMMFC and calculated current and power at each resistance were (2011). It was stated that in a lower external resistance, more accu-
normalized with the anolyte volume. Internal resistance was calculated mulated active biofilm was formed but the biofilm established at higher
using the slop of polarization curve (Juang et al., 2012; Lefebvre et al., external resistance appeared uniform compared with the lower external
2011). It should be noted that assessment of the PMMFC performance resistance. Therefore, the PMMFC operation was initiated under OCP
was done based on the galvanostatic method (Damaskin, 1967). conditions and the cell potential was monitored. According to Nernst’s
Therefore, the overall cell potential was monitored to investigate the equation, any variation in the activation of species in the redox reaction
effect of all overpotentials of the cell performance. To assess the would change the OCP. So, to assess the microbial enrichment, by
PMMFC performance based on the potentiostatic method, the mea- changing the substrate and suspended bacteria concentrations to excess
surement of anode potential under the control conditions in view point level, approaching the sustained OCP was chosen as the characteristic
of investigation of microalgae performance can be the subject of future of the appropriate concentration of exoelectrogenic microorganisms.
works. Besides, after OCP monitoring, by applying the external resistance
Fig. 1 shows a schematic of the designed experimental setup (i.e. to the circuit of the PMMFC and feeding substrate and bacteria con-
Fig. 1a) and different structures of MFC including air–cathode MFC sortium at excess concentrations, the substantial variation in the trend
(Fig. 1b), PMMFC (Fig. 1c), and abiotic–cathode MFC (Fig. 1d). of current evolution was not observed.
The coulombic efficiency (CE) was calculated using Eq. (1): Therefore, the sustained OCP could infer as a characteristic of the
microbial enrichment (Mardanpour et al., 2012; Mardanpour &
t
MS × ∫0 b Idt Yaghmaei, 2016; Naraghi et al., 2015; Zhang et al., 2011). The results
CE = clearly indicate an increase in OCP with enhancement of light intensity.
F ×bes × vAn × ΔCOD (1)
The highest and lowest values of the OCP obtained at a light intensity of
−1
where, Ms (g gmol ) = 32 is the molecular weight of oxygen; I 5000 and 10000 lx, respectively. This implied the presence of optimum
(mA) denotes the current passing through the system; F represents the value for concentration of dissolved oxygen in the cathodic compart-
Faraday’s constant (96500 C mole−1); bes = 4 is the number of electrons ment (Juang et al., 2012). An increase in dissolved oxygen concentra-
interchanged per mole of oxygen; VAn (ml) = 158 is the working vo- tion as a result of light intensity enhancement from 3500 to 5000 lx,
lume of anode compartment; and ΔCOD (mg l−1) denotes the variation leads to increase in the cathode potential that consequently increases
of organic content in a closed cycle over operating period (Juang et al., OCP. By rising the light intensity from 5000 to 10000 lx and as a result
2012). increasing the concentration of oxygen, the mass transfer of proton
For calculation of produced biomass, the suspension of Chlorella through system membrane limits and diffusion of oxygen from cathode
vulgaris (in specific OD) was centrifuged at 4000 rpm and for 20 min to anode increases that eventually increases the anode potential and
using RST24 centrifuge machine. The precipitated part was dried inside reduces the OCP (Kakarla et al., 2015).
oven at 80 °C for 2 h and finally after weighting, dry weight of produced It should be noted that the monitoring of sustained current density
biomass was reported. The cell counting was done by optical micro- evolution to show approaching the sustainability performance of the
scope under magnification of 100. The amounts of dry weight (W/g system was done after microbial cultivation and recording of OCP

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

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.

under excess concentration of the organic substrate. As shown in amount of dissolved oxygen inside the cathodic compartment from 7.8
Fig. 2b, the highest value of produced current density at external re- to 9.5 mg l−1. As can be seen, at a light intensity of 10000 lx, the power
sistance of 850 Ω in presents of the cell overpotentials was achieved density is 59 mW m−3, which is 53.4% less than the power density at
(Mardanpour et al., 2012). 5000 lx. It might be explained that higher light intensity leads to a light
The polarization and power density curves of PMMFC under dif- saturation phenomenon, or photo-inhibition, which damages the cell
ferent light intensities were shown in Fig. 2c. As can be seen, at light growth of microalgae (Cheirsilp & Torpee, 2012; He et al., 2014). An-
intensities of 5000 lx and 10000 lx, the highest and lowest values of other problem that associated with produced current reduction is ac-
power densities were obtained, respectively. Similar to analysis of OCP cumulation of the dissolved oxygen that enhances of oxygen bubble
curves, the effect of light intensity on the photosynthesis process and pressure in cathodic compartment (Chai & Zhao, 2012; He et al., 2014).
subsequently microalgae growth and oxygen production in cathodic This may contribute to back diffusion of oxygen to anodic compartment
compartment, were significant. Since, the growth of microalgae occurs that consequently decreases power generation.
under autotrophic conditions, the light intensity plays a critical role. The variation of produced current density and concentration of
By increasing light intensity from 3500 to 5000 lx, the maximum of dissolved oxygen in a cathodic compartment under the light intensities
produced power density increases and reaches 126 mW m−3 as max- of 3500 lx up to 10000 lx were shown in Fig. 2d. Effect of light intensity
imum obtained power density of system. Further increase in light in- on the growth of the microalgae can be divided into four phases in-
tensity leads to a decrease in power density. As shown in Fig. 2d, an cluding lag, light limitation, light saturation, and light inhibition
increase in the light intensity from 3500 lx to 10000 lx, increased the phases. Therefore, the influent of light intensity on the PMMFC

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

performance may also be categorized as four phases: (1) lag phase in 2014). In addition, the reduction of OCP in high light intensities
which enhancement of light intensity does not change produced cur- (544 mV at light intensity of 5000 lx and 465 mV at light intensity of
rent; (2) light limitation phase, when the enhancement of light intensity 10000 lx) endorses this subject.
increases produced current; (3) light saturation phase, in which en- Fig. 3b shows the growth curves of Chlorella vulgaris microalgae in a
hancement of light intensity does not change produced current; (4) fi- cathodic compartment of PMMFC under various light intensities. As it is
nally, light inhibition phase, in which increasing light intensity de- known, with increasing the light intensity, amount of the microalgae
crease produced current (Wu et al., 2014). As shown in Fig. 2d, the light cells enhanced, but its life time (due to increasing growth rate) de-
limitation phase, light saturation phase and light inhibition phase oc- creased and the microalgae reach its stationary phase in shorter time.
curred when the light intensity raised from 3500 to 5000 lx, from 5000 As can been observed, for light intensity of 3500, 5000 and 10000 lx,
to 7000 lx (due to a slope) and from 7000 lx to 10000, respectively. the microalgae growth approached the stationary phase on the 12th,
The light intensity between 5000 and 6500 lx can be ascribed as 11th, and 9th day of growth during system operation, respectively. This
optimum range for Chlorella vulgaris photosynthesis and maximum indicates an increase in light intensity, decreased the growth rate of the
power generation in the PMMFC. The similar conclusion has been re- microalgae and the ceased phase of microalgae growth (i.e. stationary
ported in study of He et al. (He et al., 2014). phase) was achieved in the lower operating time. This may be due to
Although, the effect of light intensity on microalgae growth depends damage to the microalgae cells under high light intensity, which disrupt
culture conditions and genetic makeup (Wu et al., 2014), but generally, the intracellular performance and decreases its growth rate than before.
the appropriate light intensity promotes the photosynthetic activity, as Several studies have also shown that as a result of augmented
well as the production of available oxygen for cathodic reaction of the oxygen concentrations in the cathodic compartment, the potential of
PMMFC (He et al., 2014; Juang et al., 2012). Therefore, the power hydrogen peroxide formation increased. Therefore, the risk of cell da-
density does not always increase with increasing light intensity. Since mage may be increased by oxidation of the protein that the microalgae
the oxygen concentration in the cathode compartment has an optimal performance is limited and prohibited (Cai et al., 2013; Wang et al.,
amount (as shown in Fig. 2d was about 8.4 mg l−1 at light intensity of 2013).
5000 lx), enhancement of oxygen concentration from defined dosage Fig. 3c shows the growth rate of the Chlorella vulgaris in the cathodic
reduces the power generation. This is substantial subject in high-scale compartment of the PMMFC and in the PBR without cathode electrode.
applications and cost engineering considerations to choose an optimal As can be seen, with increasing light intensity, the microalgae growth
light intensity (Gouveia et al., 2014). rate increases in both systems, but inclines of growth rate curve were
decreased in higher light intensities. Besides, the produced biomass in
3.2. Effect of light intensity on COD removal, coulombic efficiency and the cathodic compartment of PMMFC is lower than amount of it in the
biomass production PBR. This may be attributed to the microalgae biomass loss due to stick
on different parts of the cathodic compartment of the PMMFC enclosure
Fig. 3a shows the COD removal and coulombic efficiency of PMMFC (including the cathode electrode, proton exchange membrane, and the
in different light intensities. Although the maximum variation of COD membrane protector) and/or environmental factors such as pH of
removal efficiency was about 1.3% but the variation of coulombic ef- cathodic compartment of the PMMFC and temperature variation. The
ficiency was about 30% that indicates the significant role of light illu- maximum concentration of biomass in the cathodic compartment of
mination in current production. Maximum coulombic efficiencies of PMMFC about 4.0 g l−1 was obtained in light intensity of 10000 lx
78% and 48% were obtained at light intensities of 5000 and 10000 lx, (Fig. 3d). The difference between the growth rates and biomass con-
respectively. As coulombic efficiency is a function of current generation centration in the cathodic compartment of PMMFC and PBR compen-
and COD removal, it variation substantially affects by rate of electron sated at high light intensities. This suggests that by increasing the light
production than anolyte organic content. intensity, PMMFC can act as a biological reactor for growth of micro-
The COD removal strongly depends on the bacterial activity and algae.
organic content of the MFC. The activity of the PMMFC biocatalysts in
presence of high organic content involves longer operating time of the 3.3. Effect of light/dark regime on electrochemical characteristics of
system. In the other hand, the activity of the MFC bacteria through the PMMFC
biodegradation sequence of complex organic substrates affects the COD
removal (Singhvi & Chhabra, 2013). The similar results and conclusion The effect of light/dark cycles was done to evaluate the influential
have been reported in the study of Min & Logan (2004) for investigation of intermittent illumination on the PMMFC performance. The different
the biodegradation of different substrates in the MFC. They reported light/dark regimes of 12/12, 16/8, and 24/00 h were applied at op-
only 8% COD removal and coulombic efficiency of 65% for acetate, 3% timal light intensity of 5000 lx. Fig. 4a shows the current density evo-
COD removal and coulombic efficiency of 28% for butyrate and 10% lution at external resistance of 850 Ω under different light/dark re-
COD removal and coulombic efficiency of 50% for domestic wastewater gimes. Power density and polarization curves under different light/dark
with butyrate under the same conditions. The low COD removal in regimes are shown in Fig. 4b. With respect to Fig. 4a and b, the results
contrast to the relative high coulombic efficiency was attributed to the showed that an increase in illumination period had a positive effect on
activity of exoelectrogenic bacteria. the power generation. During the light phase, microalgae carry out the
The variation of current density attributed to intensification of mi- photosynthesis that consequently capture carbon dioxide and release
croalgae growth, the variation of oxygen concentration (as electron oxygen for progression of the cathode reaction. Maximum power den-
acceptor) and back diffusion of oxygen to anolyte compartment. As sities of 126, 112 and 72 mW m−3 were obtained in 24/00, 16/8, 12/
mentioned, an increase in light intensity leads to enhancement of 12 h of light/dark regimes, respectively. Under continuous illumina-
oxygen-related photosynthetic efficiency, which consequently de- tion, the maximum power density was 12.7% and 74.8% higher than
creases cathodic resistance (Wu et al., 2014). In the other hand, aug- produced power densities in the intermittent illumination of 16/8 and
mentation of dissolved oxygen concentration inside the cathodic com- 12/12 h, respectively. These results are in agreement with study of Wu
partment leads to penetration of oxygen from the membrane into the et al. (2014) investigated photo MFC performance under 12/12 h light/
anodic compartment that decreases produced current (He et al., 2014). dark cycle. In should be noted that in their work, the produced power
The enhancement of internal resistance of cell which increased from densities under illumination was more than 5.6 fold in the absence of
661 Ω in a light intensity of 5000 lx, to 1142 Ω at the light intensity of light, while the enhancement of power density of the PMMFC was about
10000 lx, indicating oxygen accumulation as electron transfer barriers 1.68 fold. These results seem logical because the carbon dioxide gas for
was another reason of the decrease in power generation (He et al., Chlorella vulgaris growth in cathode compartment of the PMMFC was

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

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.

supplied through aeration. Such an optical function is also observed for consumption the concentration of dissolved oxygen for 8/16 and 12/12
a MFC with Cyanobacterial microalgae (Pisciotta et al., 2010; Zou et al., hr light/dark regimes decreased to 7.5 and 7.1 mg l−1, respectively.
2009) and eukaryotic algae (Xiao et al., 2012). However, the MFC in- The variation of oxygen concentration may be due to the abnormal
oculated with Spirulina platensis, produced more bioelectricity in metabolism of microalgae cells when the dark phase abruptly replaces
darkness than that in the light (Fu et al., 2009). with light phase. As the microalgae cells need to turn their metabolic
With regards to this point that microalgae do not implement pho- pathway to adapt to the continuous illumination, so a temporary dis-
tosynthesis and oxygen production in the dark and even it consumes ruption in photosynthesis and respiration of microalgae occurs, which
oxygen, this is favorite phenomena for anolyte of photo MFC that result in the variation of the oxygen concentration in the cathodic
placed in the dark and produced electrons are not lost. These different compartment (Wu et al., 2013). After adaptation, the stable trend of the
results about of the effect of light on the PMMFC can be attributed to concentration oxygen in a certain range was observed.
the fact that microalgae can play a different role in oxidation-reduction
reactions in anode and cathode of the PMMFC. 3.4. Effect of light/dark regimes on COD removal, coulombic efficiency and
The variation of dissolved oxygen at the cathode compartment of biomass production
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 con- Table 1 shows the different characteristics of the bioelectrochemical
centration in light phase were 8.4, 8.1 and 7.9 mg l−1, respectively. As performance of the PMMFC versus various light regimes. Under light/
microalgae during the dark phase carried out respiration and oxygen dark cycle of 24/00, 16/8 and 12/12 light regimes, the COD removals

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

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.

were measured 5.47%, 4.98%, and 4.09%, respectively. As can be seen, of produced oxygen due to changing illumination conditions.
there is no significant difference in the variation of COD removals of the As the microalgae growth rate in the continuous illumination is
anodic compartment. higher than two other light/dark regimes, the maximum concentration
The internal resistance of the PMMFC slightly increased from 661 Ω, of biomass (about 3.6 g l−1) was obtained in the continuous illumina-
in the continuous regime, to 732 and 1066 Ω, for the light/dark cycles tion. It should be noted that the effect of light period on biomass growth
of 16/8 and 12/12 h, respectively. During continuous illumination, the in cathodic compartment of the PMMFC and the PBR was similar to the
internal resistance is greater than the internal resistance of the two results obtained from investigation of light intensity. With increasing
light/dark regimes. Besides, the maximum coulombic efficiency for the light period, more biomass was obtained in both systems, but in the
PMMFC of 78% was obtained in the continuous regimes and it was PBR, the variation of biomass concentration versus light period is
reduced to 57% for light/dark cycle of 12/12 h. These may be con- negligible compared to the cathodic compartment of the PMMFC.
tributed to sudden shocks to the system and augmented concentration It should be noted that investigation of PMMFC performance under

Table 1
The particular characteristics of the PMMFC at different light/dark regimes.
Light/Dark Open Circuit Maximum Internal Coulombic COD Biomass production in Biomass DO in cathodic
Cycle (h) Potential Power Density Resistance Efficiency removal Cathodic Compartment of production in the Compartment in light
(mV) (mW m−3) (Ω) (%) (%) the PMMFC PBR (mg l−1)
(g l−1) (g l−1)

Continuous 544 126 661 78 5.47 3.6 4.0 8.4


16/8 534 112 732 72 4.98 3.2 3.9 8.1
12/12 498 72 1066 57 4.09 2.7 3.7 7.9

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

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.

different wavelengths of light, substrate concentrations, and scale up of difference in concentration overpotentials.
the systems are another area for future research. 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
3.5. The comparison of PMMFC characteristics with abiotic-cathode MFC other hand, the maximum power density of 140 mW m−3 was obtained
and air–cathode MFC for air–cathode MFC which was 10% and 65% higher than PMMFC and
abiotic–cathode MFC, respectively (Fig. 5c). The higher power and
Fig. 5a shows the OCP of different MFC structures. As can be seen in current densities of air–cathode MFC may attribute to lower cathodic
Fig. 5a, the maximum OCP of 453 ± 4 mV was obtained for air–- overpotential in which may related to the effective removal of produced
cathode MFC after 85 h of cell operation. As the mechanical aeration water from half cathodic reaction. In addition, induced forced con-
and photosynthesis process play critical role in effective availability of vection of oxygen in abiotic–cathode MFC and PMMFC can leads to
oxygen and facilitate mass transfer through induced forced convection augmented pressure of oxygen in cathodic compartment and back dif-
on cathode surface, the OCP of abiotic–cathode MFC and PMMFC, fusion in anolyte to reduce power generation. As mentioned, the oxygen
544 ± 4 and 535 ± 4 mV, respectively. These results are in agreement penetration into the anolyte raises the potential of the anode and/or
with Kakarla et al. conclusions (Kakarla et al., 2015). prevents the passing of the proton from membrane and ultimately in-
With regard to assessment of different structure overpotentials, the creases the internal resistance. Despite the lower power generation of
current density evolutions at external resistance of 850 Ω, and the PMMFC, the production of biomass in catholyte of cell, as feature for
power density curves of MFC in the three structures was obtained and biofuel generation as well as the ability of wastewater treatment in view
shown in Fig. 5b and c, respectively. The main features among the MFCs point of nitrogen and phosphorus removal can be contributed as a
curves are related to descending trend indicate the substantial

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E. Bazdar et al. Bioresource Technology 261 (2018) 350–360

Table 2 Dong, Y., Qu, Y., Li, C., Han, X., Ambuchi, J.J., Liu, J., Yu, Y., Feng, Y., 2017.
The particular characteristics of the air – cathode MFC, PMMFC and abio- Simultaneous algae-polluted water treatment and electricity generation using a bio-
tic–cathode MFC. cathode-coupled electrocoagulation cell (bio-ECC). J. Hazard. Mater. 340, 104–112.
Fu, C.-C., Su, C.-H., Hung, T.-C., Hsieh, C.-H., Suryani, D., Wu, W.-T., 2009. Effects of
Air–cathode MFC PMMFC Abiotic–cathode MFC biomass weight and light intensity on the performance of photosynthetic microbial
fuel cells with Spirulina platensis. Bioresour. Technol. 100 (18), 4183–4186.
OCP (mV) 453 ± 4 544 ± 4 535 ± 4 Gajda, I., Greenman, J., Melhuish, C., Ieropoulos, I., 2015. Self-sustainable electricity
Power Density (mW m−3) 140 126 84 production from algae grown in a microbial fuel cell system. Biomass Bioenergy 82,
87–93.
Internal Resistance (Ω) 515 662 878
Ghasemi, M., Daud, W.R.W., Ismail, M., Rahimnejad, M., Ismail, A.F., Leong, J.X.,
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Coulombic Efficiency (%) 81 78 66 (13), 5480–5484.
COD Removal (%) 5.94 5.47 4.44 Gouveia, L., Neves, C., Sebastião, D., Nobre, B.P., Matos, C.T., 2014. Effect of light on the
production of bioelectricity and added-value microalgae biomass in a photosynthetic
alga microbial fuel cell. Bioresour. Technol. 154, 171–177.
significant advantage compared with air–cathode MFC (Colombo et al., He, H., Zhou, M., Yang, J., Hu, Y., Zhao, Y., 2014. Simultaneous wastewater treatment,
electricity generation and biomass production by an immobilized photosynthetic
2017; Rago et al., 2017). algal microbial fuel cell. Bioprocess Biosyst. Eng. 37 (5), 873–880.
The bioelectrochemical characteristics of PMMFC compared with He, L., Du, P., Chen, Y., Lu, H., Cheng, X., Chang, B., Wang, Z., 2017. Advances in mi-
air–cathode MFC and abiotic–cathode MFC are summarized in Table 2. crobial fuel cells for wastewater treatment. Renew. Sustain. Energy Rev. 71, 388–403.
Hu, X., Liu, B., Zhou, J., Jin, R., Qiao, S., Liu, G., 2015. CO2 fixation, lipid production, and
As shown, in spite of low COD removal, the high values of coulombic power generation by a novel air-lift-type microbial carbon capture cell system.
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with other structures. This may be due to the lack of catholyte and the cathode microbial fuel cell with oxygen supply from an externally connected algal
bioreactor. Bioresour. Technol. 195, 210–216.
lack of formation of sediment on the cathode side (Kakarla et al., 2015).
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lipid extracted algae: a promising system for algal lipids and power generation.
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Lan, J.C.-W., Raman, K., Huang, C.-M., Chang, C.-M., 2013. The impact of monochromatic
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The effects of light intensities and illumination regimes on PMMFC Chlamydomonas reinhardtii transformation F5 as biocatalyst. Biochem. Eng. J. 78,
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light/dark regimes can be useful for the stable performance of the Lagooning microbial fuel cells: a first approach by coupling electricity-producing
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PMMFC by increasing the microalgae's lifetime. Despite the lower Luo, S., Berges, J.A., He, Z., Young, E.B., 2017. Algal-microbial community collaboration
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production of biomass in catholyte of cell, as feature for biofuel gen- bioelectrochemical systems. Algal Res. 24 (Part B), 527–539.
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Acknowledgements Ma, M., Cao, L., Chen, L., Ying, X., Deng, Z., 2015. A carbon-neutral photosynthetic
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The authors would like to thank Sharif Energy Research Institute Mardanpour, M.M., Esfahany, M.N., Behzad, T., Sedaqatvand, R., 2012. Single chamber
(SERI) and The Biochemical and Bioenvironmental Engineering Center microbial fuel cell with spiral anode for dairy wastewater treatment. Biosens.
Bioelectron. 38 (1), 264–269.
(BBRC) of Sharif University of Technology, Iran for their support
Mardanpour, M.M., Yaghmaei, S., 2016. Characterization of a microfluidic microbial fuel
through this project and for permission to use their facilities. cell as a power generator based on a nickel electrode. Biosens. Bioelectron 79,
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