Desalination 351 (2014) 77–81

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Desalination

j ourna l homepage: www.e lsev ie r .com/ locate /desa l

Effects of salinity anions on the anode performance inbioelectrochemical systems

Guangli Liu ⁎, Shuxian Yu, Haiping Luo ⁎, Renduo Zhang, Shiyu Fu, Xiaonan LuoSchool of Environmental Science and Engineering, Sun Yat-Sen University, Guangdong Provincial Key Laboratory of Environmental Pollution Control and Remediation Technology, Guangzhou510275, China

H I G H L I G H T S

• With HCO3− from 0 to 100 mM, the coulombic efficiencies increased from 29% to 44%.

• The power density increased from 465 to 676 mW/m2 by adding Cl− from 0 to 50 mM.• With the presence of 100 mM SO4

2−, the power density decreased to 56 mW/cm2.• At the same conductivity, the best performance was obtained with HCO3

− supplement.

⁎ Corresponding authors. Tel.: +86 20 84110052; fax:E-mail addresses: liugl@mail.sysu.edu.cn (G. Liu), luoh

http://dx.doi.org/10.1016/j.desal.2014.07.0260011-9164/© 2014 Elsevier B.V. All rights reserved.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 7 May 2014Received in revised form 12 July 2014Accepted 22 July 2014Available online xxxx

Keywords:Bioelectrochemical systemsAnion compositionElectricity generation performanceMicrobial community structure

To study the feasibility to utilize the microbial desalination cell (MDC) to desalinate complex saltwater, theobjective of this study was to investigate the effects of different salinity anions on anode performance.Experiments were conducted using three different salinity anions (Cl−, SO4

2−, and HCO3−) with different

concentrations in the anode of two-chamber microbial fuel cell (MFC). Results showed that the supplement ofanions, with concentration ranges of 25–50 mM for Cl−, 25 mM for SO4

2−, and 25–100 mM for HCO3−, into the

substrate increased the voltage output of theMFC.With the HCO3− concentrations from0 to 100mM, the coulombic

efficiencies increased from 29% to 44%, and the power densities increased from 465 to 1064 mW/m2. At the sameconductivity, the electron production in the MFC with the anions was in the order: HCO3

− N Cl− N SO42−.

The presence of HCO3− enhanced the buffer capacity of the anolyte and maintained the activity of the

anode biofilm, in which the dominant species included Geobacter uraniireducens, Desulfofaba fastidiosa,andMycobacterium fortuitum. This study suggests that theMDC can be used to desalinate complex saltwaterto improve wastewater treatment in the anode chamber.

© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Microbial desalination cell (MDC) is a newdevice that can be used totreat saltwater and brackish water using electrical power generatedfrom organic substrates by exoelectrogenic bacteria [7,14,15,24,25].With the MDC, the desalination rate of seawater can reach 60%–95%[4,11,18,19]. The stacked structure, forward osmosis, or bipolar mem-brane can be utilized in MDCs to achieve higher salt removal efficiency(95%) [5,11]. Brastad and He [3] used theMDC to soften hard water andremovedmore than 90% of hardness from several testedwater samples.The MDC can serve as a pretreatment for subsequent reverse osmosis(RO) process and significantly reduce the desalination energy costsand membrane fouling potential. Therefore, the MDC is with greatpotential in desalination systems [10,20,22].

+86 20 84110267.p5@mail.sysu.edu.cn (H. Luo).

The MDC is developed on the basis of the two-chamber microbialfuel cell (MFC) by adding a desalination chamber between the anodeand cathode chambers. Under the force of electrical field, anions andcations in saltwater filled in the desalination chamber move to theanode and cathode chambers, respectively. With movement of thesalinity ions, the conditions of both anode and cathode chambers shouldchange during operation of theMDC. The effect of the condition changecan be significant in the anode chamber because of the existence ofexoelectrogenic bacteria. Luo et al. [18,19] reported that desalinationof saltwater containing NaCl and NaHCO3 in the MDC improvedwastewater treatment in the anode chamber, by increasing the conduc-tivity by 2.5 times and stabilizing anolyte pH. Ieropoulos et al. [8] foundthat adding 150mMNa2SO4 to the anode chamber led to 100% increaseof power output and 32%–86% improvement of current output in anactivated sludge MFC. Morris and Jin [23] noted that voltage outputof the MFC was not affected when 790 mg/L of NaCl was introducedinto the anode substrate. However, Lefebvre et al. [12] reported thatcoulombic efficiency (CE) of the MFC decreased when NaCl

78 G. Liu et al. / Desalination 351 (2014) 77–81

concentrations in the anode substrate were over 500 mg/L. There-fore, both the concentration and composition of anions in the sub-strate can affect the performance of exoelectrogenic bacteriasignificantly. In the MDC, the anion concentrations in the anolyte in-crease gradually. Nonetheless, the effect of the increasing anion concen-trations on anode microorganisms is still poorly understood.

The aim of this study was to investigate the performance andmicrobial community structure of the anode with addition of threedifferent salinity anions (Cl−, SO4

2− and HCO3−) into the substrates.

The effects of different concentrations of the anions on the systemperformance were also studied in terms of internal resistance, powerdensity and coulombic efficiency.

2. Materials and methods

2.1. MFC set-up and operation

Two-chamber MFC reactors were constructed using plexiglassplastic cylinder (Fig. 1). Each chamber was formed by drilling ahole (3-cm diameter) in the cylinder, and the anode and cathodechambers were separated by a cation exchange membrane (CMI-7000, ULTREX™, China). Carbon cloth, with an effective area of 7 cm2,was selected as the anode and cathode material. After inserting theelectrodes, net volumes of the anode and cathode chambers wereabout 28 mL, respectively. Titanium wires were used to connect thecircuit with an external resistance of 1000 Ω. The MFCs were operatedwith the fed-batch mode at room temperature.

A mixture of anaerobic and aerobic sludge (from Liede wastewatertreatment plant of Guangzhou, China) was used as the inoculumin the MFCs. The anodic medium contained (in 1 L deionized water):1.0 g CH3COONa, 4.0896 g Na2HPO4, 2.544 g NaH2PO4, 0.31 g NH4Cl,0.13 g KCl, and 12.5 mL trace metal solution and 12.5 mL vitamin solu-tion [17], except mentioned otherwise. Ferricyanide solution of 50 mMwith phosphate buffer (pH = 7) was used as the electron acceptor inthe cathode chamber.

Before data collection, all MFCswere operatedwith acetate mediumas the sole substrate until reaching stable voltage outputs. After allMFCswere started up, three types of anions (Cl−, SO4

2−, and HCO3−) were

added into the anode medium, respectively. For each type of anion,two MFCs were used as a parallel group, in which four concentrations(25, 50, 75 and 100mM)were applied sequentially. For each concentra-tion, the MECs operated for two cycles (about 240 h). The MFC withoutanion addition was used as the control.

Fig. 1. The schematic diagram of the microbial fuel cell reactor.

2.2. Analyses and calculations

At the end of each cycle, samples from the anode solutions in theMFCs were treated by filtration through a membrane (with a porediameter of 0.22 μm) to remove cells. Values of chemical oxygendemand (COD) of the samples were measured using the potassiumdichromate method [2]. During the operation, voltages across theexternal resistance (1000 Ω) of the MFCs were measured using adata acquisition system at a time interval of 15 min. The currentwas calculated based on the voltage and the external resistance.The maximum power density was obtained from polarization curvesusing different resistances (100 to 10,000 Ω). The area power density(PA, W/m2) was calculated as follows:

PA ¼ IUA

ð1Þ

where I is the current (A), U is the voltage (V), and A is the area of theanode (m2). The electron production (Q) was calculated by

Q ¼Xn

i¼1Iiti ð2Þ

where Ii is the current (A) at time ti. The coulombic efficiency, CE, isdefined as the ratio of total coulombs actually transferred to theanode, to the coulombs if all substrate removal produced current [13].The CE (%) was calculated by

CE ¼ 100%MXn

i¼1Uiti

RFbΔSVð3Þ

Here Ui is the output voltage of MFC at time ti, R is the externalresistance (1000 Ω), F is Faraday's constant (96,485 C/mole electron),b is the number of moles of electrons produced per mol of the COD(4 mol e−/mol COD), ΔS is the removal of COD concentration (g/L), Vis the liquid volume (L), and M is the molecular weight of oxygen(32 g/mol).

2.3. Microbial community analysis

Biofilm samples were scratched from the anode electrode of MFCwith two different concentrations (0 and 100mM). DNAs were isolatedfrom the bacteria in the biofilm samples using the soil DNA kit (OmegaBio-Tek) according to the manufacturer's instructions. The universalprimer sets 518R (5′-ATTACGCGGCTGCTGG-3′) and GC-357F (5′-CGCCCGCCGCGCGGCGGGCGGGGCGGGGGCACGGGGGGCCTACGGGAGGCAGCAG-3′) (Invitrogen Biotechnology Co., Ltd)were used to amplify theV3region of 16S ribosomal DNA (rDNA) from the extracted genomic DNA.The PCR amplification was performed using the following procedure:initial denaturation at 95 °C for 2 min; 30 standard cycles of denatur-ation at 94 °C for 30 s, annealing at 53 °C for 30 s, and extension at72 °C for 30 s; and a final extension at 72 °C for 7 min.

TheDGGE analysis of the PCRproductswas carried out in a denaturinggradient gel electrophoresis system (C.B.S. SCIENTIFIC, Del Mar, CA, USA)as previously described [21]. 16S rDNA gene fragments cut out from theDGGE gel were used for PCR amplification, and the PCR procedure wasthe same as that mentioned above, but using the universal primer setsof 357F (5′-CCTACGGGAGGCAGCAG-3′) and 518R (5′-ATTACGCGGCTGCTGG-3′). The PCR products were used for sequencing, and then thesequences were compared to the known sequences deposited inthe GenBank database.

3. Results

3.1. Effects of salinity anions on performance of the MFCs

Representative voltage curves of the MFC affected by differentanions are shown in Fig. 2. With the Cl− concentrations from 0 to

Fig. 3. Electron production of the MFCs with different concentrations of Cl−, SO42−, and

HCO3−.

79G. Liu et al. / Desalination 351 (2014) 77–81

50 mM, the maximum output voltages slightly increased from 520 to568 mV. However, the maximum voltages decreased from 568 to480 mV when the Cl− concentration further increased to 75 mM. Atthe second cyclewith 100mMCl− concentration, themaximumvoltagewas only 240 mV but the electricity production cycle was significantlylonger than the other cycles. Compared to in the control (508 mV),with the addition of 25 mM SO4

2−, the maximum voltages increased to544 mV at the first cycle and then decreased. Voltages decreased to150mVat the SO4

2− concentration of 100mM. Theduration of electricityproduction cycle extended gradually with the increase of SO4

2− concen-trations. The addition of HCO3

− improved the maximum voltage outputof the MFC. With the HCO3

− concentration increase from 0 to 100 mM,the maximum voltages increased from 508 to 616 mV.

To further compare the effects of the anions on electricity perfor-mance, we calculated the electron production of each cycle as shown inFig. 3. The electron production increased from 93 C to the maximum of109 C with the Cl− concentrations from 0 to 50 mM, then decreased,and was 83 C at 100 mM. The electron production increased from 96 Cto the maximum of 102 C with the SO4

2− concentrations from 0 to25 mM, then decreased, and was 78 C at 100 mM. By adding the HCO3

−

solutions, the maximum electron production of 131 C was achieved at50 mM. The electron production decreased to 113 C at 100 mM, whichwas still higher than that of the control (100 C at 0 mM).

With the Cl− supplement, the CE values increased from 29% at 0mMto a range 33%–38% at the higher concentrations (Table 1). Insignificant

Fig. 2. Electricity output voltages of the MFCs with different concentrations of (A) Cl−,(B) SO4

2−, and (C) HCO3−. The arrows show the time of anode solution replacement.

change was observed in the CEs because the COD removal ratesdecreased after the addition of Cl−. The maximum power densitiesincreased from 465 to 676 mW/m2 with the Cl− concentration from 0to 50mM, and then decreased to 102mW/m2 at 100mM. The CE valuesincreased from 29% to 34% with the SO4

2− concentrations from 0 to100 mM, while the maximum power densities decreased from 465 to56 mW/m2. The MFC with the addition of HCO3

− resulted in the highestCE and power density. With the HCO3

− concentrations from 0 to100 mM, the CE values increased from 29% to 44%, and the powerdensities increased from 465 to 1064 mW/m2.

3.2. Effects of the salinity anions on the system

According to the polarization curve, internal resistances of theMFCswith the different anions and different concentrations were calculated(Table 1). The internal resistance of the MFC without anion addition(the control) was 281Ω. With addition of 25 and 50 mM Cl− solutions,the internal resistances became 192 and 197Ω, respectively. The internalresistance finally reached 1918 Ω with 100 mM Cl−. With the 100 mMSO4

2− solution, the internal resistance was 2185 Ω, which was nearlyeight times of that from the control. However, with the addition ofHCO3

− from 25 to 100 mM, the internal resistances decreased from 225to 150 Ω.

Conductivities of the anolyte with different anions at differentconcentrations are also shown in Table 1. The conductivities increasedwith the addition of Cl−, SO4

2− and HCO3−. The conductivities increased

from 7.7 to 18 mS/cm with Cl− concentrations from 0 to 100 mM. WithSO4

2− and HCO3− concentrations from 0 to 100 mM, the conductivities

increased from 7.7 to 23 mS/cm and from 7.7 to 15 mS/cm, respectively.Effects of the anions on evolution of microbial community were

characterized by analyzing the 16S rRNA gene fragments of biofilmsamples on the anode. DGGE screening of amplified 16S rDNA genefragments showed different microbial community profiles among theanode biofilm of mature MFCs (Fig. 4). Geobacter uraniireducens (band1), Desulfofaba fastidiosa (band 6), and Mycobacterium fortuitum (band9) existed in all the treatments. Table 2 lists the difference of anodemicrobial community in the MFCs with different anions (Cl−, SO4

2−,and HCO3

−) at the concentration of 100 mM. Paracoccus kocurii (band8) was observed in the control and the MFCs with Cl− and HCO3

− butnot in the MFC with SO4

2−. Flavobacterium dankookense (band 4) wasfound in the control and the MFC with HCO3

−. Geobacter psychrophilus(band 7) was found in the MFCs with SO4

2− and HCO3−. However,

Desulfobulbus rhabdoformis (band 2) and Desulfobulbus elongates (band3) were only found in the MFC with Cl−.

Fig. 4. PCR-DGGE analysis of 16S rDNA extracted from the anode of MFCs with differentanions.

Table 1Comparison of the removal ratio of COD, maximum power density, CE, and internal resistance among the MFCs with different anions (Cl−, SO4

2−, and HCO3−) and different concentrations.

Concentration(mM)

CODremoval(%)

Maximumpower density(mW/m2)

Coulombicefficiency(%)

Internalresistance(Ω)

Conductivity(mS/cm)

The control0 97 ± 1.1 465 ± 148 29 ± 3.2 281 ± 68.3 7.7 ± 0

Cl addition25 90 ± 4.4 676 ± 101 38 ± 1.1 192 ± 29.2 9.4 ± 1.250 85 ± 1.2 663 ± 100 38 ± 1.3 197 ± 30.2 12 ± 1.375 80 ± 4.3 314 ± 77.3 33 ± 2.2 592 ± 1.2 15 ± 2.1100 80 ± 3.2 102 ± 15.2 33 ± 2.4 1918 ± 280.2 18 ± 2.3

SO42− addition

25 98 ± 1.2 434 ± 178 31 ± 2.2 372 ± 163 11 ± 1.250 86 ± 11 217 ± 59.2 33 ± 3.1 770 ± 263 15 ± 2.475 88 ± 1.2 162 ± 79.2 33 ± 4.3 877 ± 767 19 ± 2.1100 81 ± 4.3 56.2 ± 8.32 34 ± 5.2 2185 ± 328 23 ± 3.3

HCO3− addition

25 97 ± 2.2 669 ± 125 33 ± 1.4 225 ± 40.2 9.2 ± 1.150 96 ± 1.3 653 ± 27.2 40 ± 4.1 232 ± 4.2 11 ± 1.375 85 ± 1.2 931 ± 67.2 41 ± 5.2 176 ± 16.1 13 ± 1.4100 86 ± 3.4 1064 ± 160 44 ± 2.3 150 ± 22.4 15 ± 1.3

80 G. Liu et al. / Desalination 351 (2014) 77–81

4. Discussion

In our study, adding 25 and 50 mM Cl− into the substrate couldenhance the power output of the MFC, attributable to the increase ofsolution conductivity. The increase of solution conductivity can reducethe internal resistance of the system [18,19]. As shown by our measure-ments, the internal resistance decreased from 281 to 197 Ω with Cl−

concentration from 0 to 50 mM. However, the output voltages declinedwith the concentrations N 50 mM. The elevated Cl− concentrations cancause the plasmolysis of microorganisms and reduce microbiologicalactivity [26,30]. Aminzadeh et al. [1] reported that the nitrate removalrate began to fall when NaCl concentration was over 3.5%. Dincer andKargi [6] suggested that in a continuous flow nitrification and denitrifica-tion biological reactor, rates of denitrification and nitrification droppedsignificantly with salt concentrations N 1%.

The output voltages of MFC increased with addition of 25 mM SO42−,

whichwaspossibly due to the increase of anolyte conductivity. Ieropouloset al. [8] reported that the power output enhanced by 32–100% when70–150 mM Na2SO4 solutions were added into the activated sludgeMFC and leachate-treating MFC, respectively. They attributed theresults to the high diversity of bacteria in the activated sludge andleachate. In our study, however, the power generation of MFC becamelower with the SO4

2− concentration of 100 mM. It was likely that theanode microorganism was acclimating for sulfate utilization duringthe increasing concentrations of SO4

2−. In the MFC with 75 mM SO42−,

the SO42− concentration decreased by 28% at the end of operating

cycle. The bacteria in the anode could use the SO42− as electron acceptor,

which competed with anode on electron harvesting and led to theelectron loss and the decrease of voltage output.

With addition of 0–100mMHCO3− into theMFC, the output voltages

and CE values increased gradually as the result of decrease of internalresistances. To further investigate the influence of different anions onthe performance of the anode, we calculated the electron productionin the cycle using anolyte with the same conductivity but differentchemicals (Fig. 5). At the same conductivity, the coulombic productionwas the highest with HCO3

− supplement, followed with Cl−, and thelowest with SO4

2−. Therefore, except the effect of increasing solutionconductivity, HCO3

− addition improved theMFC performance effectively,while SO4

2− addition significantly inhibited electron transfer on theanode. The existence of HCO3

− could enhance the buffer capacity of theanolyte, keep a relatively high pH level, and maintain the activity ofexoelectrogens during the operation of the MFC [18]. The pH values of

anolyte increased from 7 to 8.54 as the HCO3− concentrations increased

from 0 to 100 mM. The pH of anolyte was 6–7 at the end of the cycle,which was still suitable for growth of bacteria. With the bufferingfunction, the anode biofilm from the MFC with HCO3

− containedmore species than the others as shown by the molecular analysis.The low capacity of buffering has always been the thorny problemin the operation of biochemical system, while high strength buffersolution could be an effective solution of the problem [18,19].

By using the bioelectrochemical system, the electrical energy canbe directly retrieved without any further conversion process to treatwastewater or saltwater. The system offers an advantage of energygeneration [28]. The actual development of the technology depends

Table 2The difference of anode microbial community in MFCs with different anions (Cl−, SO4

2−,and HCO3

−) at the concentration of 100 mM.

Treatment Anode microbial community

Control Flavobacterium dankookense (band 4)Paracoccus kocurii (band 8)

Cl− addition Desulfobulbus rhabdoformis (band 2)Desulfobulbus elongates (band 3)Paracoccus kocurii (band 8)

SO42− addition Geobacter psychrophilus (band 7)

HCO3− addition Flavobacterium dankookense (band 4)

Geobacter psychrophilus (band 7)Paracoccus kocurii (band 8)

81G. Liu et al. / Desalination 351 (2014) 77–81

on efficient microbial bioanodes. With the anion concentration andanolyte conductivity up to 100 mM and 26 mS/cm, respectively,G. uraniireducens, D. fastidiosa, and M. fortuitum were the dominantspecies in the anode biofilm of all the tested MFCs. Geobacter andDesulfofaba species have been reported to be the electrochemicallyactive bacteria in MFCs [9,16,27]. Sulfate reducers includingD. rhabdoformis and D. elongates were enriched with the presenceof Cl−, which could be halophilic strains and compete successfullywith others at high salinity environment [29].

5. Conclusions

The effects of three types of salinity anion (Cl−, SO42− and HCO3

−)with different concentrations on the anode performance were investi-gated using two-chamber MFC. Within the concentration ranges of25–50 mM for Cl−, 0–25 mM for SO4

2−, and 25–100 mM for HCO3−,

supplement of the anions into the substrate improved the power outputof the MFC. With the HCO3

− concentrations from 0 to 100 mM, the CEvalues increased from 29% to 44%, and the power densities increasedfrom 465 to 1064 mW/m2. At the same conductivity, the addition ofHCO3

− and SO42 resulted in the highest and lowest electron production

in the MFC, respectively. The existence of HCO3− could enhance buffer

capacity of the anolyte, alleviate the pH decrease, and maintain theactivity of anode biofilm. The information from this study should beuseful to utilize the MDC to desalinate complex saltwater.

Acknowledgments

This work was supported by grants from the National NaturalScience Foundation of China (51308557, 51039007, 51278500), andthe research fund program of Guangdong Provincial Key Laboratoryof Environmental Pollution Control and Remediation Technology(2013K0002), the research fund program of Key Laboratory of Waterand Air Pollution Control of Guangdong Province (GD2012A01).

Fig. 5. Electron production of MFCs with different anions and the same conductivity.

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