Bioresource Technology 111 (2012) 105–110

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Bioresource Technology

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Performance and microbial diversity of microbial fuel cells coupledwith different cathode types during simultaneous azo dye decolorizationand electricity generation

Bin Hou a,b,1, Yongyou Hu a,b,⇑, Jian Sun a,b,2

a Department of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Control and Ecological Remediation for Industrial Agglomeration Area,South China University of Technology, Guangzhou 510006, Chinab State Key Lab of Pulp and Paper Engineering, South China University of Technology, Guangzhou 510640, China

a r t i c l e i n f o

Article history:Received 6 November 2011Received in revised form 2 February 2012Accepted 6 February 2012Available online 16 February 2012

Keywords:Microbial fuel cellCathode typeCongo red decolorizationElectricity generationMicrobial diversity

0960-8524/$ - see front matter � 2012 Elsevier Ltd. Adoi:10.1016/j.biortech.2012.02.017

⇑ Corresponding author at: Department of Environming, South China University of Technology, Guangzho39380506; fax: +86 20 39380508.

E-mail addresses: houbin566@163.com, hou.binppyyhu@scut.edu.cn (Y. Hu), sunjian472@163.com (J.

1 Tel.: +86 159 14305840.2 Tel.: +86 20 39383780.

a b s t r a c t

To study the effect of cathode type on performance and microbial diversity of the MFC, aerobic biocath-ode and air-cathode were incorporated into microbial fuel cells (MFCs) which were explored for simul-taneous azo dye decolorization and electricity generation. The electrochemical impedancespectroscopy (EIS) results demonstrated that the catalytic activity of the microorganisms on the biocath-ode surface was comparable with that of the platinum coated on the air-cathode. The power densityachieved by using biocathode was lower than air-cathode, but the biocathode could greatly improvethe Congo red decolorization rate. By using the biocathode, 96.4% decolorization of Congo red wasobtained within 29 h, whereas, about 107 h was required to achieve the same decolorization efficiencywith the air-cathode. 16S rRNA sequencing analysis demonstrated a phylogenetic diversity in the com-munities of the anode biofilm and showed clear differences between the anode-attached populationsin the MFCs with a different cathode type.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Recently, microbial fuel cells (MFCs) have attracted growingattention for their capability to enhance the degradation of somerecalcitrant pollutants (Luo et al., 2010; Zhang et al., 2009). A con-ventional MFC utilize a biological anode and an abiotic cathode,with oxygen used as an electron-acceptor due to its unlimitedavailability and high standard redox potential. Moreover, the useof oxygen could avoid the potential environmental pollution re-sulted from the use of liquid-state electron-acceptors, such ashexacynoferrate (Rabaey et al., 2005) and acidic permanganate(You et al., 2006).

In order to accelerate the oxygen reduction on the surface of thecathode, platinum is commonly used because of its excellent cata-lytic ability. However, the high cost of platinum is a major limita-tion to MFC application and economic viability. Replacement ofplatinum with alternative cheap metals, such as manganese diox-ide (Li et al., 2010), iron(II) and cobalt-based materials (Cheng

ll rights reserved.

ental Science and Engineer-u 510006, China. Tel.: +86 20

@mail.scut.edu.cn (B. Hou),Sun).

et al., 2006; Ter Heijne et al., 2007), could also improve the oxygenreduction rate with cost saving. Metal-based materials, however,are generally susceptible to the adverse environmental conditionsthat may occur in MFCs and cause inactivation (Sun et al., 2011).

A recently developed biocathode that uses microorganisms ascatalysts to assist electron-transfer is a promising way to improvecathode performance without the use of noble metal. Many com-pounds other than oxygen could be also used as terminal elec-tron-acceptors in biocathode, such as nitrate, sulfate, iron,manganese, selenate, arsenate, urinate, fumarate, carbon dioxideand hexavalent chromium (Stams et al., 2006; Wang et al., 2008).This provides a potential approach for wastewater treatment byusing biocathode due to its variety of terminal electron-acceptors.

As a novel technology, MFC may be explored to treat the azodye-containing wastewater with simultaneous electricity genera-tion. In previous studies, the authors have demonstrated the feasi-bility of azo dye decolorization in an air-cathode single-chamberMFC. The air-cathode, however, often needs noble metal platinumas the cathode catalyst to enhance the oxygen reduction on thecathode surface. Moreover, the risk of oxygen diffusion from theair-cathode to the anode could result in an unsatisfied decoloriza-tion rate. Biocathode may be employed into MFCs which were ex-plored for simultaneous azo dye decolorization and electricitygeneration to improve the cathode performance without aboveproblems. In addition, the aerobic biocathode provided a way to

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further treat the decolorization liquid of azo dye from the anodewhich is prone to be biodegraded under aerobic conditions (Sunet al., 2011).

To date, most studies focused on the comparison of the MFCperformance in terms of electricity generation. But the comparisonon the capability of recalcitrant pollutants degradation and themicrobial diversity among the MFCs has not been made. Therefore,it is significance to make a comparison between the air-cathodeMFC and the biocathode MFC for electricity generation and azodye decolorization. In present study, an ultrafiltration membranewith molecular cutoff weights of 1K (UFM-1K) which was provedto be the most suitable membrane for simultaneous electricitygeneration and azo dye decolorization was selected as the separatemembrane (Hou et al., 2011a) and a representative azo dye of Con-go red was selected as model azo dye due to its wide use, persis-tence in natural environment and strong toxic effect to aquaticspecies and human. The effect of the cathode type on the perfor-mance and microbial diversity of the MFCs during simultaneouselectricity generation and Congo red decolorization was investi-gated in detail.

Fig. 1. PCR–DGGE analysis of 16S rDNA extracted from the original inoculums (A),the anode biofilm in the MFC with biocathode (B), and air-cathode (C) (operated formore than 6 months). Glucose (500 mg COD/L) and Congo red (300 mg/L) were usedas co-substrates.

2. Methods

2.1. Dye

Congo red (C32H22N6O6S2Na2, analytical grade) was manuallyprepared to the chosen concentrations with deionized water,which was purchased from Damao chemical reagent plant of Tian-jin, China, and used as received without further purification.

2.2. MFC construction

Two MFCs coupled with different types of cathodes were con-structed: aerobic biocathode two-chamber MFC and air-cathodesingle-chamber MFC. Aerobic biocathode two-chamber MFC wereconstructed from two plastic (Plexiglas) cubic chambers (liquidvolume of each chamber was 400 mL). The chambers were sepa-rated by a UFM-1K with a surface area of 16 cm2. Plain porous car-bon papers (without water proofing) with a projected surface areaof 3 � 3 cm2 on each side were used as electrodes. No catalyst wasapplied on the surface of the cathode. Air-cathode single-chamberMFC was constructed using Plexiglas with a total volume of 512 mL(8 � 8 � 8 cm in height with an operating volume of approximately400 mL plus a 112 mL headspace). Anodes were made of non-wet-proofed porous carbon papers with a projected surface area of3 cm � 3 cm on one side, while cathodes were similar to the an-odes in dimension and prepared by coating 0.5 mg/cm2 of Pt onwet-proofed porous carbon papers. A UFM-1K was directly appliedonto the water-facing side of the air-cathode.

2.3. MFC inoculation and operation

The anode chambers of the two MFCs were inoculated using amixture of aerobic and anaerobic sludge (1:1, v:v), collected fromthe Liede municipal wastewater treatment plant, Guangzhou, Chi-na. The sludge was added into MFCs with a final concentration of2 g of volatile suspended solids per liter. Congo red (300 mg/L)and glucose (500 mg COD/L) as the mixed fuels were used in theexperiments. The medium used for the MFCs anodes contained(per liter of deionized water): 5.544 g NaH2PO4�2H2O, 23.084 gNa2HPO4�12H2O, 0.62 g NH4Cl, 0.26 g KCl, 12.5 mL trace metalssolution and 5 mL vitamin solution as reported by Lovley and Phil-lips (1988).

The cathode chamber of aerobic biocathode two-chamber MFCwas filled with the same nutrient medium as added into the anode

without the mixed fuels (Congo red and glucose). In addition, aer-obic sludge with a final concentration of 2 g of volatile suspendedsolids per liter was used as the original inoculum.

All MFCs were operated in a batch-fed mode at a fixed load of1000 X and mixed by a magnetic stirrer to enhance mass transfer.They were fed with the mixture of Congo red (300 mg/L) and glu-cose (500 mg COD/L) from the beginning of the enrichment. Thereproducible maximum voltages indicated the end of the enrich-ment. Experiments were conducted in a constant-temperatureroom (30 ± 1 �C) and the average value was reported for all data.

2.4. Analytics and calculations

Dissolved oxygen (DO) was measured using an YSI Model 148550A meter (Yellow Springs Instruments, 149 Yellow Springs,USA).

The Congo red concentrations were measured in the UV–visiblescanning spectrophotometer (BECKMANDV640) at kmax = 496 nm.The voltage, polarization curve and power density were measuredand calculated as previously described (Hou et al., 2011a).

Electrochemistry impedance spectroscopy (EIS) measurementswere carried for the cathodes in a frequency range of 100 kHz–5 mHz with an ac signal of 10 mV amplitude using a potentiostat(Model 2273, Princeton Applied Research). The connecting modeof the electrodes was used as reported by Manohar et al. (2008a).The obtained data were fitted to an equivalent circuit using ZSimp-Win 3.10 software (Echem, US).

Community analysis was determined as reported previously(Hou et al., 2011b).

3. Results and discussion

3.1. Microbial community diversity and phylogenetic analysis

The structures of microbial communities in anode of the MFCscoupled with different cathode types were determined using theDGGE analysis following a stable operation of 6 months. Fig. 1 pre-sents the DGGE profiles of the microorganisms in the originalinoculums and anode biofilm in the two MFCs. Each band on theDGGE profile represents a specific species in the microbial commu-nity, and the staining intensity of a band represents the relativeabundance of the corresponding microbial species. As showed inFig. 1, the original inoculums had a larger number of bands thanthe anode biofilm with biocathode or air-cathode, thus appearingto have a higher overall diversity. After a 6 months operation, sev-eral major bands appeared and the profile became simpler. Thiscase was mainly due to the screening and enrichment to the anode

Fig. 2. Phylogenetic relationship based on a comparative analysis of the 16S rRNA sequences recovered from the anode biofilm in the MFC with biocathode (A), and air-cathode (B). Glucose (500 mg COD/L) and Congo red (300 mg/L) were used as co-substrates.

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bacteria induced by the anode-specific environment of MFC. TheDGGE profiles in Fig. 1B, C clearly showed that the microbial com-munity changed with different cathode types. This result suggestedthat the cathode type caused changes with respect to the dominantbacterial species on the anode and the relative abundance.

A number of bands from the gels were stabbed for sequenceanalysis (Fig. 2). In the biocathode MFC, the anode-attached popu-lation could be assigned to four groups, comprising d-Proteobacte-ria, Firmicutes, Chlorobi and Bacteroidetes. Of the sequences, 37.5%were Bacteroidetes (Table 1). The Bacteroidetes mainly included

Table 1Comparison of the microbial communities on the anode of the MFCs coupled with biocathode or air-cathode.

Enrichment procedure Proteobacteria (%) Firmicutes (%) Bacteroidetes (%) Chlorobi (%) Others (%)

a- b- d-

Biocathode 0.0 0.0 23.1 28.1 37.3 11.5 0.0Air-cathode 28.8 13.4 19.0 11.3 16.5 0.0 11.0

Table 2Fit-parameters for the cathode impedance spectra of the two MFCs.

Fit-parameter Biocathode Air-cathode

Rs (O) 3.26 13.43CPE (mF) 28.19 77.99Rct (O) 105.1 50.1

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several fermentative bacteria which were induced by the anaerobicenvironment of the anode (Grabowski et al., 2005). Firmicutes(28.1%) was the second dominant phylum on the anode, whichhas been reported to be integral members of the MFC bacterialcommunity, indicating their exocellular electron-transfer (Rabaeyet al., 2004), followed by d-Proteobacteria (23.1%) and Chlorobi(11.5%). Chlorobi was reported by Wu et al. (2010), which wascapable of denitrification. Sulfate-reducing bacteria which be-longed to the phylum d-Proteobacteria were observed in both theMFCs coupled with biocathode and air-cathode.

In the air-cathode MFC, the new phyla of a-Proteobacteria andb-Proteobacteria were detected. Azospirillum and Methylobacteriumwhich belonged to the phylum a-Proteobacteria were all nitrogen-fixing bacteria (Sy et al., 2001). The b-Proteobacteria included sev-eral groups of aerobic or facultative bacteria. Their existence in allMFCs was possibly due to oxygen diffusion from the cathode to theanode, which might support aerobic or facultative growth (Chaeet al., 2009). In addition, Geobacter sp. with a 98% similarity toGeobacter pickeringii G13 was also observed in the air-cathodeMFC, but absent in the biocathode MFC.

3.2. Cathode impedance

EIS measurements were performed to investigate the cathodeperformance of the MFCs (Fig. 3). The impedance spectra of thecathodes can be well fitted with an equivalent circuit, in which aconstant phase element (CPE) and a charge-transfer resistance(Rct) in parallel, placed in series with a solution resistance (Rs).The fit-parameters of the cathode impedance spectra of the twoMFCs were summarized in Table 2. When comparing these results,several interesting points were observed. The relative small valueof the Rs showed that the ohmic limitation played a minor rolecompared to kinetic limitation. The Rs for the air-cathode was a lit-tle higher than that of the biocathode, because the Rs for the air-cathode included the resistance of the membrane. During the EISmeasurement of the biocathode, reference electrode was insertedin the cathode chamber, whereas, the reference electrode was in-serted in the anode chamber for the EIS measurement of the air-

Fig. 3. Nyquist plots for the cathode impedance spectra of the two MFCs.

cathode. Thus, the Rs for the air-cathode included the resistanceof the membrane which was used to separate the anode chamberand the cathodic electrode (Manohar et al., 2008a).

Small Rct indicates a faster electron-transfer rate between elec-trode and electrolyte (Zhang et al., 2011). Moreover, the electron-transfer rate was a response to the catalytic activity of catalyston the electrode, thus the catalytic activity of catalyst on the elec-trode is inversely proportional to the electrode Rct. The Rct for thebiocathode (105.1 O) and the air-cathode (50.1 O) as showed in Ta-ble 2 indicated that the catalytic activity of the microorganisms onthe biocathode surface was comparable with that of the platinumcoated on the air-cathode. Additionally, the capacitance of theair-cathode calculated from the CPE was much higher than thatof the biocathode. This was due to the larger active surface areaof the platinum-plated carbon paper cathode (Manohar et al.,2008b).

3.3. Performance of MFCs coupled with different cathode types

The repeatable and stable voltages were obtained for air-cath-ode MFC after 1 month acclimation, whereas, the startup periodof biocathode MFC needed 2 months to become fully active (datanot shown). This was in accordance with previous study (Chenet al., 2008). The longer startup period of biocathode MFC was pos-sible due to the fact that the microorganisms in the biocathodeMFC were enriched not only on the anode surface but also on thecathode surface. As showed in Fig. 4, the stable voltage was higher

Fig. 4. Voltage generation for MFCs coupled with different types of cathodes usingCongo red (300 mg/L) and glucose (500 mg COD/L) as co-substrate at an externalresistance of 1000 O.

Fig. 5. Power density for MFCs coupled with different types of cathodes. Fig. 6. Decolorization of Congo red (300 mg/L) in MFCs coupled with different typesof cathodes using glucose (500 mg COD/L) as co-substrate at an external resistanceof 1000 O.

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for air-cathode MFC (0.45 V), followed by biocathode MFC (0.25 V)at the external resistance of 1000 O.

Power density curves of the two MFCs during Congo red decol-orization were drawn at their stable stage. As showed in Fig. 5, thepower densities obtained here were lower than those of previouslyreported by using acetate-fed air-cathode single-chamber MFC andglucose-fed biocathode two-chamber MFC (Cheng and Logan,2011; Chung et al., 2011). This case was due to the competition be-tween anode and azo dye for electrons from co-substrate (glucose)or the activities inhibition of electroactive bacteria caused by azodye and its broken down products (Sun et al., 2009).

Significant differences in power generation were observed forboth of the two tested MFCs. The maximum power density of theair-cathode MFC was 324 mW/m2 which was about 166% improve-ment over that of the biocathode MFC (122 mW/m2), demonstrat-ing that the air-cathode single-chamber MFC exhibited a betterperformance in electricity generation compared to the biocathodeMFC. The catalytic activity of the microorganisms on the biocath-ode surface was comparable with that of the platinum coated onthe air-cathode. However, the maximum power density of theair-cathode MFC was about 166% improvement over that of thebiocathode MFC. The difference in electricity generation betweenbiocathode and air-cathode could be a result of two factors. First,the air-cathode single-chamber MFC could minimize the electrodespace so as to decrease the internal resistance as compared withthe biocathode two-chamber MFC (You et al., 2007). Second, Geob-acter sp. has been frequently reported to be responsible for powergeneration in the MFC as they can transfer electrons directly to anelectrode (Bond and Lovley, 2003). The existence of Geobacter sp. inthe MFC can significantly improve power generation (Bond andLovley, 2003; Yi et al., 2009). Therefore, the existence of Geobactersp. in the air-cathode MFC may be the most possible reason for thehigher power density produced by the MFC with air-cathode thanthat yielded by the MFC with biocathode. The electrochemically ac-tive bacteria in MFCs have been considered to be iron-reducingbacteria such as Geobacter sp. and Shewanella sp. (Bond and Lovley,2003; Lovley, 2006). However, no Shewanella sp. was retrievedfrom the two MFCs. The successful electricity generation in the bio-cathode MFC with no detection of Geobacter sp. and Shewanella sp.indicated the possible existence of other unknown species ofelectricigens.

Decolorization of Congo red can be achieved with simultaneouselectricity generation in MFCs. During the operation of MFCs, theazo bonds of Congo red were cleaved using protons and electrons

from glucose oxidized by anodic bacteria, resulting in the forma-tion of colorless products, such as aromatic intermediates (DosSantos et al., 2006). It can be seen from Fig. 6 that a clear effectof cathode type on Congo red decolorization was observed. Byusing the biocathode, 96.4% decolorization of Congo red was ob-tained within 29 h, whereas about 107 h was required to achievethe same decolorization efficiency with the air-cathode, indicatingthat the biocathode MFC was more favorable for Congo red decol-orization as compared with the air-cathode MFC.

As showed in Fig. 2, a large number of aerobic or facultative bac-teria were detected in the air-cathode MFC, but absent in the bio-cathode MFC, demonstrating that the oxygen diffusion from thecathode to the anode in the air-cathode MFC was more seriousthan that in the biocathode MFC. This was in accordance withthe measured values of the DO in the anode chambers. The DO ofthe anode chamber increased from 0 to 0.69 mg/L in 2 h in theair-cathode MFC. However, the DO of the anode chamber was only0.12 mg/L after 2 h in the biocathode MFC. The serious oxygen dif-fusion was not helpful for the highly efficient decolorization. As aresult, the biocathode MFC obtained a higher decolorization ratethan the air-cathode MFC. The sulfate-reducing bacteria of thephylum d-Proteobacteria, which have been demonstrated tocontribute not only to power output in the seafloor fuel cell(Ryckelynck et al., 2005) but also to the decolorization of azo dyein azo dye-containing wastewater treatment(Yoo et al., 2001),were observed in both the MFCs. In this study, the sulfate-reducingbacteria could be responsible for the azo dye decolorization in thetwo MFCs. It would be more speculative to describe the exact rolesof most of the identified bacteria based on only 16S rRNA sequenceanalysis. It is proposed that some of the bacteria except the sulfate-reducing bacteria in the MFCs may also take part in the decoloriza-tion, and there were some bacteria which might be involved in afurther biodegradation of the decolorization products under themicroaerophilic condition resulted from the oxygen diffusion fromthe cathode into the anode chamber.

Biocathode alleviate the need to use noble metal or non-noblemetal catalysts for the reduction of oxygen, which increases sub-stantially the viability and sustainability of MFCs (Clauwaertet al., 2007). However, the power density obtained from the bio-cathode MFC was low. As previous research, the feasibility ofsimultaneous Congo red decolorization and electricity generationby using the MFCs equipped with the biocathode and the air-cath-ode has been demonstrated. The biocathode MFC produced a

110 B. Hou et al. / Bioresource Technology 111 (2012) 105–110

higher Congo red decolorization rate with a lower power density ascompared with the air-cathode MFC. Therefore, further efforts arerequired to improve the power output of the biocathode MFC. Ef-forts have been made to address this problem by using ferro/man-ganese-oxidizing bacteria in the biocathode. For example, Rhoadset al. (2005) used a manganese-oxidizing bacterium, Leptothrix dis-cophora, as the catalyst to complete the cycle of Mn(IV) reductionand subsequent reoxidation of Mn(II) in the biocathode. After add-ing the cycle of manganese reduction/oxidation to an aerated cath-ode, the maximum power generation increased by more than 40times. Mao et al. (2010) investigated the performance of a biocath-ode MFC catalyzed by ferro/manganese-oxidizing bacteria. Theyfound that in a batch-fed system, the maximum cell potential dif-ference was higher than 600 mV with an external resistance of100 O. Additional, the authors have demonstrated that the decolor-ization products of azo dye can also serve as redox mediator forincreasing power generation simultaneously in the biocathode(Sun et al., 2011). With the advancement in power output andthe potential use for further treating the decolorization productsof azo dye, biocathode was more favorable for azo dye-containingwastewater treatment with simultaneous electricity generation.However, the study of biocathode is still in its infancy, more workwill be needed to further improve the overall performance and theelectron-transfer mechanisms in the biocathode should be fullyunderstood.

4. Conclusions

EIS demonstrated that the catalytic activity of the microorgan-isms in the biocathode was comparable with that of platinum.Cathode type could induce the difference in anode-attached popu-lations. As a result, the performance of the MFCs used for simulta-neous azo dye decolorization and electricity generation wasdifferent. In comparison with air-cathode MFC, the power densityobtained by biocathode MFC was lower. However, biocathodeMFC could greatly improve the Congo red decolorization rate.

Acknowledgement

The authors would like to acknowledge the financial support forthis work provided by the National Natural Science Fund of China(No. 20977032).

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