Chemical Engineering Journal 262 (2015) 958–965

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Chemical Engineering Journal

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Sustainable photosynthetic biocathode in microbial desalination cells

http://dx.doi.org/10.1016/j.cej.2014.10.0481385-8947/� 2014 Elsevier B.V. All rights reserved.

⇑ Corresponding author.E-mail addresses: gude@cee.msstate.edu, gudevg@gmail.com (V.G. Gude).

Bahareh Kokabian, Veera Gnaneswar Gude ⇑Department of Civil and Environmental Engineering, Mississippi State University, Mississippi State, MS 39762, United States

h i g h l i g h t s

� Sustainable algal biocathodes formicrobial desalination cells weredeveloped.� Effect of light/dark cycles and COD

concentrations were evaluated.� Algae perform better under natural

light/dark cycles due to better celldivision.� Maximum power densities were

1.1 W/m3 and 0.987 W/m3 for500 mg/L and 1000 mg/L COD.� Coulombic efficiency for 500 mg/L

COD (68.02%) was higher than1000 mg/L (40.36%).

g r a p h i c a l a b s t r a c t

Schematic of the photosynthetic microbial desalination cell (PMDC).

a r t i c l e i n f o

Article history:Received 2 July 2014Received in revised form 8 October 2014Accepted 15 October 2014Available online 22 October 2014

Keywords:Microbial desalination cellAlgaeLight effectBiofilmBiocathodePhotosynthesis

a b s t r a c t

Microbial desalination cells (MDCs) provide for simultaneous wastewater treatment and desalinationwhile producing clean electricity from the organic wastes. However, one major drawback with MDCstechnology is its unsustainable cathode chamber where expensive catalysts and toxic chemicals areemployed for electricity generation, similar to other bioelectrochemical systems. Introducing biologicalcathodes may enhance the system performance in an environmentally-sustainable manner. This studydescribes the use of algae as sustainable biocatalyst/biocathode in photosynthetic MDCs. Since alga isa photosynthetic microorganism, the availability of light as well as the electron-donating anodic processmay have significant effects on the biocathode performance. A series of experiments evaluating theseeffects proved that algae perform better under natural light/dark cycles and that higher COD concentra-tions do not necessarily improve the power density. A maximum power density of 1.1 W/m3 NCC(0.77 W/m3 NAC) was observed for a COD concentration of 500 mg/L while the same for 1000 mg/L ofCOD was 0.987 W/m3 NCC (0.69 W/m3 NAC). This study confirms the beneficial use of algae as a sustain-able and photosynthetic biocathode in MDCs to supply electron acceptors in an environmental-friendlymanner.

� 2014 Elsevier B.V. All rights reserved.

1. Introduction

Microbial desalination cells (MDCs) is a promising technologyto produce clean electricity from wastewater (organic wastes)along with removal of salts from saline waters in an environmen-

tal-friendly manner. As with any bio-electro-chemical system(BES), MDCs also have limitations of the need for expensive cata-lysts (platinum) and toxic chemical oxidants (Permanganate andFerricyanide) in the cathode cells. An ideal alternative to eliminatethese limitations is by incorporating biocathodes. In the anodecompartments, the "anodophilic" bacteria function as biocatalysts,degrading organic materials to produce electrons, which travelfrom the anode to the cathode via an external electric circuit. In

B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965 959

the cathode, free electrons are delivered to terminal electronacceptors, such as oxygen, to complete the electrochemical reac-tion. Ions present in the saline water of the middle chamber (suchas Na+ and Cl�) move through the cation and anion exchange mem-branes due to the potential difference between the anode and cath-ode chambers. In abiotic cathode compartments, eitherpermanganate or ferricyanide is used as a chemical agent.Recently, researchers have replaced these chemical catalysts likeferricyanide by bacterial cathodes known as biocathodes for pro-ducing electron acceptors [1,2]. In biocathode based bio-electro-chemical systems, the cathodic electron acceptance mechanism ispromoted by microorganisms instead of a chemical catalyst; whichlowers the construction and operational costs, and offers the flex-ibility to produce useful products or remove unwanted com-pounds. However, optimum physiological conditions should bemaintained in the biocathode chamber to develop active biofilms[3]. In MFCs, the first biocathode study demonstrated denitrifica-tion in the cathode chamber where the nitrate from the anode trea-ted wastewater effluent was circulated through the biocathodechamber [4]. Wen et al. [5] studied a biocathode in an MDC con-sisting of an aerobic consortium in which, they provided the bio-cathode chamber with external aeration to maintain an activeenvironment. In this study, we evaluated the performance of aphotosynthetic (algae) biocathode in MDCs treating wastewaterand saline water simultaneously. The operational principle of pho-tosynthetic MDCs (PMDCs) is similar to a natural process thatoccurs in the surface water environments. For instance, algae con-sume carbon dioxide during sunlight hours to produce oxygen andorganic matter, which serve as organic and oxygen sources for thebenthic heterotrophs to be converted into carbon dioxide [3]. Algaeplay a similar role in PMDCs by releasing oxygen as a terminal elec-tron acceptor. Algae provide additional benefits compared to otherbiocathodes since algal biomass is considered a valuable bio-prod-uct unlike the sludge in other biological systems. In PMDCs, theyhelp mitigate the CO2 released from the wastewater treatment ina closed loop and remove the nutrients from wastewater duringphotosynthesis reaction and produce oxygen, which acts as elec-tron acceptor for electricity production. To utilize algae as biocath-ode, it is important to understand their performance which isdependent on various parameters including availability of light,availability of carbon dioxide, growth medium composition andother environmental conditions. Since algae are photosyntheticmicroorganisms requiring light for energy generation, it is impor-tant to study the effect of light on their performance in PMDCs.Continuous illumination is not a practical option for large scaleapplications, therefore natural light and dark cycles would seemfeasible. On the other hand, photosynthesis and growth rates ofmicroalgae are greatly affected by the quality and quantity of illu-mination with the maximized growth occurring under clear light[6]. Prolonged exposure of light may cause photo-inhibition whileinadequate light supply may result in photo-limitation [7]. Thus,the aim of this study was to explore the effect of light as well asthe wastewater organic concentration on the performance of pho-tosynthetic microbial desalination cell and to elucidate the role ofmicroalgae in the biocathode of microbial desalination cells. Bio-film formation and membrane fouling analyses were also discussedin detail in this paper.

2. Materials and methods

2.1. Microorganisms and Electrolyte

All MDCs were inoculated with 60 mL of acclimatized anaerobicsludge obtained from the aerobic sludge of the wastewater treat-ment plant in Starkville, Mississippi. The synthetic wastewater

solution used in the anode chamber had the following composi-tion: Glucose 468.7 mg/L, KH2PO4 (4.4 g/L), K2HPO4 (3.4 g/L), NH4Cl(1.5 g/L), MgCl2 (0.1 g/L), CaCl2 (0.1 g/L), KCl (0.1 g/L), MnCl2�4H2O(0.005 g/L), and NaMo�O4�2H2O (0.001 g/L) [8]. The microalgaeChlorella Vulgaris used in the cathode compartment was grown inthe following mineral solution: CaCl2 (25 mg/L), NaCl (25 mg/L),NaNO3 (250 mg/L), MgSO4 (75 mg/L), KH2PO4 (105 mg/L), K2HPO4

(75 mg/L), and 3 mL of trace metal solution with the following con-centration was added to 1000 mL of the above solution: FeCl3

(0.194 g/L), MnCl2 (0.082 g/L), CoCl2 (0.16 g/L), Na2MoO4�2H2O(0.008 g/L), and ZnCl2 (0.005 g/L).

2.2. Analyses and calculations

The voltage across a 1 K ohm external resistor was recordedevery 15 min by a digital multimeter (Fluke, 287/FVF). The currentwas calculated using the Ohm’s law, I = V/R. The power density wascalculated (P = V⁄I) as per the volumes of the anode/cathode cham-bers. The Coulombic efficiency (CE) and Coulombic recovery (CR)were calculated using the formulae as previously described [9].After observing stable voltage, polarization curves were obtainedby changing the external resistance from 40 k to 10 O (about20 min per resistor). COD tests were carried out using standardmethods. Electrical conductivity, TDS removal, and salinity removalwere recorded using a conductivity meter (Extech EC400 ExStikWaterproof Conductivity, TDS, Salinity, and Temperature Meter).The pH of the samples was measured using a pH meter (Orion720A+ advanced ISE/pH/mV/ORP). Charge transfer efficiency wascalculated using Eq. (3). Dissolved oxygen was measured usingYSI 5100 system. Illumination on the algae cathode chamber wasprovided by CFL white light at 60 W (276 mmol/m2/s).

2.2.1. Coulombic efficiencyThe coulombic efficiency (CE) is defined as the ratio of the total

transferred electrons from the anode to the total possible electronsgenerated from organic compound removal. The columbic recovery(CR) is defined as the ratio of the total transferred electrons fromthe anode to the total electrons available in the added organic com-pounds. The CE and CR are given as follows:

CE ¼P

IðAÞ � tðsÞ96485 C

mole e�� �

� CODremovedðmoleÞ � 4 mole e�mole O2

� � ð1Þ

CR ¼P

IðAÞ � tðsÞ96485 C

mole e�� �

� CODtotalðmoleÞ � 4 mole e�mole O2

� � ð2Þ

where I is electric current (A) and t is time (s). COD total representsthe total input COD in the anode chamber and COD removed is theamount of COD removed within time t.

2.2.2. Charge efficiencyCharge efficiency in terms of salt concentrations is given as:

g ¼ Q th

Q¼ F � ðCin � Cf Þ � VDP

IðAÞ � tðsÞ ð3Þ

where Qth is the theoretical charge transfer, Q is the total harvestedcoulomb, F is the Faraday constant, Cin is the initial molar concen-tration of salt solution; Cf is the final molar concentration of saltsolution; VD is desalination volume. I is electric current and t is time.

2.2.3. SEM analysisSamples from used and unused carbon felt electrodes and mem-

branes were collected for SEM analysis. Samples were fixed over-night in 2.5% glutaraldehyde in 0.1 M sodium cacodylate buffer(pH 7.2). Samples were rinsed and then post-fixed in 2% aqueous

960 B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965

OsO4 for 1 h. After rinsing, the membrane pieces were dehydratedthrough a graded ethanol series and chemically dried using HMDS(hexamethyldisilazane). Dried samples were affixed to Al stubswith double-sided carbon adhesive tape, coated with 30 nm Pt,and viewed on a Zeiss-50 SEM at 10 kV.

2.3. MDC set up

Three-chamber cylindrical MDCs with 7.2 cm diameter weremade using plexi-glass. Anion exchange membrane (AEM, AMI7001, Membranes International) separated the anode and the desa-lination chambers, while, cation exchange membrane (CEM, CMI7000, Membranes International) separated the cathode and thedesalination part. Both membranes were preconditioned byimmersing in 5% NaCl solution at 40 �C for 24 h and rinsed withDI water prior to use, to allow for membrane hydration and expan-sion as recommended by the supplier. Carbon papers cut in circularshape with 28.27 cm2 projected surface area, were used as anodeand cathode electrodes. Prior to use, both electrodes were washedfirst with 1 N HCl solution and then with 1 N NaOH and finallyrinsed with deionized water. The electrodes then soaked in DIwater over a night prior to use to remove any excess residues[10]. The working volume of anode, desalination, and cathodechambers were 200, 200, and 140 mL respectively.

3. Results and discussion

3.1. Effect of illumination

Fig. 1A shows the effect of illumination on the voltage genera-tion in a PMDC with an initial COD concentration of 342 mg/L overseven days of operation. Three stages were observed in the voltagegeneration profile under dark and light cycles; the slow increase,stable, and the sharp declining stages. In the cathode chamber,algae medium was introduced in a fed-batch mode to study thespecific effect of dissolved oxygen concentration and the algae oxy-gen contribution. In the first stage, due to the presence of fresh dis-solved oxygen in the fresh culture medium in the cathode, and

Fig. 1. Voltage generation trends in algae biocathode microbial desalination cells: (A) vothe voltage profiles for light/dark cycles; (C) voltage profiles for light/dark cycles test w

acclimatization period of microorganism in the anode the overallvoltage increased after a short lag time. The voltage generationthen stabilized for about 100 h. The stabilized voltage indicatesthat exoelectrogenic bacteria and algae cells have formed biofilmson anode and cathode respectively [11]. The voltage then declinedslightly, perhaps due to the depletion of oxygen production byalgae, which happens when the algae run out of inorganic carbonsource (algae biocathode operates under passive conditions) andhigh pH conditions in the growth medium and also due to the con-sumption of organic substrate by microorganisms in anodechamber.

The voltage generation trends followed a sinusoidal function forthe PMDC with 14/10 h light/dark cycles. A slight decrease in volt-age (Fig. 1B) occurred during dark period which could be attributedto the lack of light for photosynthetic activity. The voltage of thesystem was restored following the photosynthetic effect duringlight hours. Other phototrophic MFC studies also reported a similartrend for voltage and current production under light and dark per-iod cycles [10,12–14]. The oxygen production ceases during darkperiods due to lack of algal photosynthetic activity [10]. The volt-age drop in dark periods indicates the lack of oxygen generationduring this period which is the electron acceptor in this system.Thus, it can be confirmed that the power production in the photo-synthetic MDC relies on the photosynthetic activity. However, itcan be noted that the voltage did not drop significantly duringthe dark periods since the non-photosynthetic respiration of algalcells results in release of carbon dioxide which is another electronacceptor. The variations in the voltage profiles depend on the per-formance period of a particular bioelectrochemical system and theapplied resistance. Especially, in this system, the voltage genera-tion mainly depends on the photosynthetic activity of the passivealgal biocathode. He et al. [12] reported a significant effect of lightand dark cycles with prolonged operation of the sediment photo-trophic MFC compared to a fresh MFC, while Xiao et al. [9]observed a significant effect of light/dark cycle on voltage changeat low external resistance (500 O) compared to high resistance(5000 O). It may be hypothesized that the presence of light helpsthe anodic metabolism of microorganisms by transferring the heatthrough electrolyte, resulting in an increase of voltage compared to

ltage generation profiles for continuous light and light/dark cycles; (B) variations inith stainless steel mesh.

Table 1Influent and effluent characteristics for the light effect test measured undercontinuous light condition.

Anode chamber Desalination chamber Cathode chamber

COD (mg/L) pH NaCl (g/L) pH DO (mg/L)

Influent 1039.4 6.5 9.9 7.9 7.78Effluent 366.3 5.7 6.9 10.7 5.56

Fig. 2. (A) Voltage generation trends in algae biocathode MDC with different CODconcentrations; (B) Polarization curves for different COD concentrations based onnet anodic compartment (NAC) and net cathodic compartment (NCC) volumes.

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the dark period. Finally, the comparison of continuous light andlight–dark cycle experiments (Fig. 1A) show that PMDCs can pro-duce higher voltage under light–dark condition which can beattributed to the better division of algae cells under naturallight–dark cycles. High light intensity and prolonged illuminationcan inhibit cell division, i.e. reproduction, in some algae [12,15].Higher light intensity over saturation limit causes photo inhibitiondue to disruption of the chloroplast lamellae and inactivation ofenzymes involved in carbon dioxide fixation. For example, growthrate of Dunaliella viridis decreased to 63% with increase in lightintensity from 700 to 1500 lmol m�2 s�1 [16–19]. Babuskin et al.[20] also found higher productivity of photosynthetic culturesunder light/dark cycles rather than continuous illumination.

Further tests were conducted to evaluate the effect of a contact-ing mechanism at a higher COD concentration. Fig. 1C depicts theeffect of light–dark cycle on PMDC with a stainless steel mesh cov-ering electrodes with an initial COD concentration of 1040 mg/L.The higher voltage indicates the beneficial use of stainless steelmesh in conducting electrons and providing a better contactbetween the carbon electrodes and the nickel-alloy rod; however,the difference between the maximum and the minimum voltageswere close between the two tests (STDEV = 0.006). The maximumpower density during illumination was 0.591 W/m3 about 9.4times higher than the maximum power production during previ-ous experiment [21]. The increase in the voltage generation canpartly be attributed to the biofilm formation and the higher CODconcentrations in the anode chamber. The lowest power produc-tion during the dark period was 0.473 W/m3. The pH in the cathodechamber increased from 7.9 to 10.7. Increase in the pH of thecathodic solution is due to the consumption of protons and oxygenreduction as stated before [9,22] and results in voltage potentiallosses [23]. The pH increased significantly since the amount of buf-fer in the algae growth medium was lower. The algae growth med-ium was prepared following the supplier recommendation forgreen algae (Connecticut Valley Biological Supply Company, MA,USA). The reduction in pH of anolyte, which typically happensdue to the anaerobic metabolism of microorganisms and the trans-fer of chloride ion from middle chamber to the anode chamber,was not very significant (6.5–5.7) possibly due to high buffer con-centration in the anolyte (KH2PO4, 4.4 g/L and K2HPO4, 3.4 g/L).Therefore, the overall voltage fluctuations occurred as a responseto a reduction in the cathode potential [5]. The coulombic effi-ciency for this test was higher (CE = 17.2%, CR = 11.14%) comparedto the previous test (CE = 10.7%, CR = 5.82%), due to higher currentproduction. The relatively low values indicate that most of sub-strate removal was used for fermentation and/or methanogenesis.However, both ranges are in accordance with regular three cham-bers MDC coulombic efficiencies reported previously [24]. Zhanget al. (2012) attributed the low CE efficiencies in their study tothe lack of N2 sparging and high internal resistance that furtherresults in a fermentation process in the anode chamber [25].According to Rabaey et al. [26] fermentation process can bereduced by enrichment of microbial consortium resulting in higherCEs which also happened in our later test with longer incubationtime. High coulombic efficiencies reported in some MDC studieswere probably due to the long-time enrichment of microbial con-sortium and design of MDC units [24,27]. In this test, the algalMDC removed 30.3 ± 0.85% of the salt in the middle chamber witha desalination rate of 0.214 g/L-d (0.042 g/d), which is about 25%faster than our previous test [21] due to the higher electricity pro-duction. The relatively low salinity removal of this study comparedto other studies is due to the equal volumes of the anode anddesalination chamber, as for higher salinity removal, largervolume ratio of wastewater to salt water is required [24]. The influ-ent and effluent parameters for the light effect test are shown inTable 1.

3.2. Effect of COD concentration

Fig. 2A shows the voltage profiles for PMDCs under two differ-ent initial COD concentrations of synthetic wastewater (500 mg/Land 1000 mg/L) for about 1000 h of operating time, which aftermixing with anaerobic sludge resulted in 789 mg/L and 1162 mg/L COD respectively. The cathode chamber was renewed with freshalgae following the voltage drops. It was noted that during the first150 h, 1000 mg/L COD produced higher electricity; however, thistrend changed with continued operation of the PMDC. The rapidvoltage generation with 1000 mg/L COD concentration during first150 h, indicates that more substrate was available for electricityproduction. The change in the trend of voltage profiles can beattributed to the adverse effect of high carbon dioxide concentra-tion induced by methanogenic activity of microorganisms in theanode chamber on microalgae photosynthesis [11]. Carbon dioxideconcentration higher than 10% in the air supplied to the photobior-eactors had adverse effects on the photosynthesis reaction of theChlorella sp. [28].

Although high concentration of buffer was used in the anodechamber, the final pH in the anode chamber decreased from 6.8to 3.8 for 500 mg/L synthetic wastewater, and from 6.7 to 2.9 for

Table 2pH and DO changes in COD effect tests.

COD pH DOave DOSt.Dev

Cycle 1Initial 8.1 7.5 0.172Final 500 11.3 6.6 0.030

1000 11.4 5.9 0.036

Cycle 2Initial 8.2 7.8 0.026Final 500 11.4 5.3 0.151

1000 11.6 5.7 0.415

Cycle 3Initial 8 8.3 0.115Final 500 11.7 5.5 0.515

1000 11.4 5.9 0.300

Cycle 4Initial 8.2 9.6 0.206Final 500 12 4.3 0.212

1000 11.7 4.5 0.175

0

2

4

6

8

10

12

1 18 25 30 39 45

Salin

ity(g

/l)

time (day)

1000 mg/l

500 mg/l

Fig. 3. Desalination (salinity) profiles at 500 mg/L and 1000 mg/L COD concentra-tions in PMDCs.

Table 3PMDC desalination rate constants for the first and pseudo-first-order reactions.

K (d�1) R2

First order500 COD mg/L 0.0251 0.95021000 COD mg/L 0.0248 0.9466

Pseudo first order500 COD mg/L 0.0681 0.98351000 COD mg/L 0.0699 0.9693

0

200

400

600

800

1000

1200

0 500 1000 1500 2000 2500

Ele

ctro

n H

arve

sted

( C

)

NaCl Removed expressed as Coulomb ( C)

500 mg/l COD 1000 mg/l COD

Linear (500 mg/l COD) Linear (1000 mg/l COD)

Fig. 4. NaCl removal expressed as coulombs compared to the total harvestedcoulombs.

Fig. 5. SEM images for electrodes – (A) fresh carbon paper electrode; (B) anode; (C)cathode.

962 B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965

1000 mg/L synthetic wastewater due to the accumulation of pro-tons in the anolyte. Since the anolyte solution was kept in the reac-tor for about 1000 h without any renewal, the accumulation of theprotons would result in the growth of acidophilic bacteria whichwill further decrease the performance of MDCs. Higher pH dropin the PMDC with 1000 mg/L synthetic wastewater could beanother reason for lower electricity production when comparedto the PMDC with 500 mg/L COD.

The voltage dropped when the pH of algae solution increased toa value higher than 11 and the DO decreased due to the poor pho-tosynthetic activity of algae under high pH conditions [29]. Thesystem could regain its maximum voltage, when the cathodechamber was renewed with fresh algae medium. Higher voltagesafter algae renewal demonstrate the effective role of photosyn-thetic activity of algae in long term operation of PMDC. This

Fig. 6. SEM images for membrane fouling in photosynthetic MDCs – (A) anion exchange membrane (before); (B) anion exchange membrane (after 45 days of operation); (C)cation exchange membrane (before); and (D) cation exchange membrane (after).

B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965 963

observation leads to a conclusion that cathode and photosyntheticreaction are limiting steps in the PMDC operation. Table 2 showsthe algae solution conditions before and after each cycle.

Fig. 2B shows the polarization curve for the COD concentrationeffect tests based on the volume of net anodic compartment (NAC)and net cathodic compartment (NCC). As power production is lim-ited by cathodic potential, we can present the power density on thebasis of cathode chamber volume [30]. Our data showed thatchanging concentration of synthetic wastewater from 1162 mg/L(1000 mg/L COD) to 788 mg/L (500 mg/L COD) enhanced maxi-mum power density from 0.987 W/m3 NCC (0.69 W/m3 NAC) to1.1 W/m3 NCC (0.77 W/m3 NAC) which occurred at 400 ohm resis-tance for both MDCs. The maximum current density with 789 mg/LCOD was 9.3 A/m3 (NCC), while with 1162 mg/L was 8.5 A/m3

(NCC). This proves that the PMDCs are suitable for low to moderatestrength (COD) wastewaters. The obtained linear polarizationcurve indicates that ohmic losses are dominant in overvoltage.The linearity of this profile (R2 = 0.982 for 500 mg/l COD andR2 = 0.977 for 1000 mg/l COD), also allows us to calculate internalresistance, based on the slope of polarization curve [27]. The inter-nal resistances for 500 and 1000 mg/L COD were 430 and 441 Orespectively. These internal resistances are close to the resistanceat which maximum power density occurred (400 O) which is typ-ical for a high internal resistance MFC limited by ohmic resistance[27]. With 500 mg/L synthetic wastewater, the COD removalreached 76.06% ± 1.21 while with 1000 mg/L, the COD removalreached 82.17% ± 1.27 at the end of the experiment (after1000 h). The slight difference in power production of two MDCsdid not have a substantial effect on salinity removal (with64.21% ± 0.5 for 500 mg/L and 63.47% ± 0.1 for 1000 mg/L); how-ever due to the higher current production, the coulombic efficiencyfor 500 mg/L COD (68.02%) was higher than 1000 mg/L (40.36%).From Fig. 3, the NaCl removal for both PMDCs was higher in thefirst 20 days (about 40%), and the salinity removal increased by20% in the following 25 days, plausibly, due to the increase in inter-

nal resistance of MDCs when salt was removed from middle cham-ber [8].

Both the first and the pseudo-first-order kinetics seem to fitwell with the desalination profiles. A linear relationship of ln (St/S0) vs time for the first order and ln [(St � Sf)/(S0 � Sf)] vs. timefor the pseudo-first-order were established, where St, Sf and S0

are salt concentration at t, final and initial time. Table 3 showsthe rate constants and the corresponding R2 for these models. Asshown in Fig. 3, at initial salt concentration of 10 g/L, the salt con-centration reached final concentrations of 3.54 g/L and 3.62 g/L for500 mg/L and 1000 mg/L COD respectively. Zhang et al. (2012) alsofound a pseudo-first-order kinetic for desalination of saltwater inan ion exchange MDC [25]. In spite of the difference in the internalresistance of the two MDCs, their salt removal rates did not have anotable difference. High charge transfer efficiencies of 216% and226% (>100%) for 500 mg/L and 1000 mg/L COD respectively, indi-cate that in addition to the produced electrical field, salinity gradi-ent across the membranes, is another reason for the migration ofions from desalination chamber to the anode and cathode cham-bers [8,32]. The salt removal at different time intervals expressedas coulomb was compared to the total amount of charge transferfor the two MDCs (Fig. 4). At longer operation time, the theoreticalcharge transfer had a closer agreement with total electrons har-vested. This shows that due to the high concentration gradientbetween the middle chamber and the anode and cathode chambersat initial periods, and the low electricity production at this stage,the majority of the salt removal was due to the concentration gra-dient rather than the voltage potential differential between theanode and cathode chambers [8].

3.3. Biofilm and biofouling analyses

Fig. 5A–C show the SEM images for fresh (Fig. 5A) and used car-bon paper electrodes of anode (Fig. 5B) and cathode (Fig. 5C)respectively. The image for the fresh carbon paper electrode

964 B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965

showed a very smooth and clear surface (Fig. 5A), while the SEMimages of the used anode and cathode electrodes showed the for-mation of dense biofilm on the thread surface of carbon cloth(Fig. 5B and C). The anode biofilm had a complex dense structuredistributed on the whole surface of the carbon cloth thread. Theformation of multilayer, non-uniform biofilm on the anode surfaceof bioelectrochemical systems fed with fermentable substrates likeglucose have also been reported while acetate fed MFCs arereported to have a uniform one layer structure [31]. Distinct mor-phologies were observed between anode and cathode biofilms.Algae cells in the shape of spherical clusters covered all surfaceof carbon paper on the biocathode while the anode was submergedby a thick layer of exoelectrogenic bacteria.

The scanning electron microscope (SEM) analysis of new andused ion exchange membranes showed distinctive differencesbetween membrane surfaces (Fig. 6A–D). A cracked surface wasobserved for unused ion exchange membranes (Fig. 6A and C) aspreviously reported [32], while fouling layers were observed forused membranes (Fig. 6B and D) in MDC [32,33]. AEM surface dis-played both biofouling caused mostly by rode shape bacteria, andinorganic crystal shaped scaling formed by the deposition of inor-ganic compounds in the synthetic wastewater. The CEM surfacewas covered with flaky inorganic fouling layer and spherical algalcells with a slight contamination of rod shaped bacteria. Foulingwhether due to chemical or biological will adversely affect theMDC performance both in terms of electricity production and saltremoval [33].

4. Conclusion

This study evaluated the performance of the algal biocathode ina photosynthetic microbial desalination cell. The light effect testshowed that the performance of algae biocathode depends on illu-mination and that it performs better under natural light/darkcycles. This study also confirmed the photosynthetically generatedoxygen contribution by algae as electron acceptor in the MDC. Itwas shown that increasing initial concentration of organic com-pound in PMDC did not have a considerable effect on salinityremoval but a slight reduction in maximum power density wasobserved. Regular renewal of algae medium in the cathode cham-ber maintains the PMDC performance in long term operation. SEManalysis of the used and unused electrodes and membranesshowed significant differences between these samples. Furtherstudies focusing on reuse of anode effluent as growth mediumfor algae biocathode and the nutrient removal in the algal biocath-odes could help enhance the benefits of the PMDCs. Combining thewastewater treatment with nutrient removal in the algae biocath-odes would also benefit from higher effluent quality and valuablebiomass production.

Acknowledgements

This research was supported by the Office of Research and Eco-nomic Development (ORED), the Bagley College of Engineering(BCoE), and the Department of Civil and Environmental Engineer-ing (CEE) at Mississippi State University. Authors appreciate thehelpful comments from the anonymous reviewers on a previousversion of this research article.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.cej.2014.10.048.

References

[1] Z. He, L.T. Angenent, Application of bacterial biocathodes in microbial cells,Electroanalysis 18 (2006) 2009–2015.

[2] L. Huang, X. Quan, J. Regan, Electron transfer mechanisms, new applications,and performance of biocathode microbial fuel cells, Bioresour. Technol. 102(2011) 316–323.

[3] V.G. Gude, B. Kokabian, V. Gadhamshetty, Beneficial bioelectrochemicalsystems for energy, water and biomass production, J. Microbial Biochem.Technol. S6 (2013) 005.

[4] B. Virdis, K. Rabaey, Z. Yuan, J. Keller, Microbial fuel cells for simultaneouscarbon and nitrogen removal, Water Res. 42 (2008) 3013–3024.

[5] Q. Wen, H. Zhang, Z. Chen, Y. Li, J. Nan, Y. Feng, Using bacterial catalyst in thecathode of microbial desalination cell to improve wastewater treatment anddesalination, Bioresour. Technol. 125 (2012) 108–113.

[6] M.F. Blair, B. Kokabian, V.G. Gude, Light and growth medium effect on Chlorellavulgaris biomass production, J. Environ. Chem. Eng. 2 (2014) 665–674.

[7] G.G. Markou, D.D. Georgakakis, Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review, Appl. Energy88 (2011) 3389–3401.

[8] X. Cao, X. Huang, P. Liang, K. Xiao, Y. Zhou, X. Zhang, B.E. Logan, A New methodfor water desalination using microbial desalination cells, Environ. Sci. Technol.43 (2009) 7148–7152.

[9] L. Xiao, Z. He, E. Young, J. Berges, Integrated photo-bioelectrochemical systemfor contaminants removal and bioenergy production, Environ. Sci. Technol. 46(2012) 11459–11466.

[10] S. Pandit, B. Nayak, D. Das, Microbial carbon capture cell using cyanobacteriafor simultaneous power generation, carbon dioxide sequestration andwastewater treatment, Bioresour. Technol. 107 (2012) 97–102.

[11] M. Zhou, H. He, T. Jin, H. Wang, Power generation enhancement in novelmicrobial carbon capture cells with immobilized Chlorella vulgaris, J. PowerSources 214 (2012) 216–219.

[12] Z. He, J. Kan, K. Nealson, F. Mansfeld, L. Angenent, Self-sustained phototrophicmicrobial fuel cells based on the synergistic cooperation betweenphotosynthetic microorganisms and heterotrophic bacteria, Environ. Sci.Technol. 43 (2009) 1648–1654.

[13] D.B. Strik, H.M. Hamelers, C.N. Buisman, Solar energy powered microbial fuelcell with a reversible bioelectrode, Environ. Sci. Technol. 44 (2010) 532–537.

[14] X. Cao, X. Huang, P. Liang, M. Fan, N. Boon, Electricity generation by anenriched phototrophic consortium in a microbial fuel cell, Electrochem.Commun. 10 (2008) 1392–1395.

[15] S.W. Chisholm, Temporal patterns of cell division in unicellular algae, Can.Bull. Fish. Aquat. Sci. 210 (1981) 150–181.

[16] F.J.L. Gordillo, M. Goutx, F.L. Figueroa, F.X. Niell, Effects of light intensity, CO2

and nitrogen supply on lipid class composition of Dunaliella viridis, J. Appl.Phycol. 10 (1998) 135–144.

[17] T. You, S.M. Barnett, Effect of light quality on production of extracellularpolysaccharides and growth rate of Porphyridium cruentum, Biochem. Eng. J. 19(2004) 251–258.

[18] M. Brody, A.E. Vatter, Observations on cellular structures of Porphyridiumcruentum, J. Biophys. Biochem. Cytol. 5 (1959) 289–294.

[19] M. Iqbal, S. Zafar, Effects of photon flux density, CO2, aeration rate, andinoculum density on growth and extracellular polysaccharide production byPorphyridium cruentum, Folia Microbiol. 38 (1993) 509–514.

[20] S. Babuskin, K. Radhakrishnan, P. Babu, M. Sukumar, M. Sivarajan, Effect ofphotoperiod, light intensity and carbon sources on biomass and lipidproductivities of Isochrysis galbana, Biotechnol. Lett. 36 (2014) 1653–1660.

[21] B. Kokabian, V.G. Gude, Photosynthetic microbial desalination cells (PMDCs)for clean energy, water and biomass production, Environ. Sci. ProcessesImpacts 15 (2013) 2178–2185.

[22] Y. Qu, Y. Feng, J. Liu, J. Lv, W. He, B. Logan, X. Wang, Simultaneous waterdesalination and electricity generation in a microbial desalination cell withelectrolyte recirculation for pH control, Bioresour. Technol. 106 (2012) 89–94.

[23] F. Zhang, K. Jacobson, P. Torres, Z. He, Effects of anolyte recirculation rates andcatholytes on electricity generation in a litre-scale upflow microbial fuel cell,Energy Environ. Sci. 3 (2010) 1347–1352.

[24] Y.G. Kim, B.E. Logan, Microbial desalination cells for energy production anddesalination, Desalination 308 (2013) 122–130.

[25] F.F. Zhang, M.M. Chen, Y.Y. Zhang, R.J. Zeng, Microbial desalination cells withion exchange resin packed to enhance desalination at low salt concentration, J.Membr. Sci. 417–418 (2012) 28–33.

[26] K. Rabaey, N. Boon, S.D. Siciliano, M. Verhaege, W. Verstraete, Biofuel cellsselect for microbial consortia that self-mediate electron transfer, Appl.Environ. Microbiol. 70 (2004) 5373–5382.

[27] B.E. Logan, B. Hamelers, R. Rozendal, U. Schröder, J. Keller, S. Freguia, K. Rabaey,Microbial fuel cells: methodology and technology, Environ. Sci. Technol. 40(2006) 5181–5192.

[28] S. Chiu, C. Kao, T. Kuan, S. Ong, C. Lin, C. Chen, Reduction of CO2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor, Bioresour.Technol. 99 (2008) 3389–3396.

[29] A. Middelboe, P. Hansen, Direct effects of pH and inorganic carbon onmacroalgal photosynthesis and growth, Mar. Biol. Res. 3 (2007) 134–144.

[30] P. Clauwaert, K. Rabaey, P. Aelterman, L. De Schamphelaire, T. Pham, N. Boon,P. Boeckx, Biological denitrification in microbial fuel cells, Environ. Sci.Technol. 41 (2007) 3354–3360.

B. Kokabian, V.G. Gude / Chemical Engineering Journal 262 (2015) 958–965 965

[31] K.P. Katuri, A. Enright, V. O’Flaherty, D. Leech, Microbial analysis of anodicbiofilm in a microbial fuel cell using slaughterhouse wastewater,Bioelectrochemistry 87 (2012) 164–171.

[32] Q. Ping, Z. He, B. Cohen, C. Dosoretz, Long-term investigation of fouling ofcation and anion exchange membranes in microbial desalination cells,Desalination 325 (2013) 48–55.

[33] H. Luo, Z. Ren, P. Xu, Long term performance and characterization of microbialdesalination cells in treating domestic wastewater, Bioresour. Technol. 120(2012) 187–193.