Review Paper-V_Biocatalysts in Microbial Fuel Cells

8/8/2019 Review Paper-V_Biocatalysts in Microbial Fuel Cells

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Enzyme and Microbial Technology 47 (2010) 179188

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Review

Biocatalysts in microbial fuel cells

Vinay Sharma, P.P. Kundu

Department of Polymer Science & Technology, University of Calcutta, 92, A. P. C. Road, Kolkata-700009, India

a r t i c l e i n f o

Article history:Received 31 July 2009Received in revised form 30 June 2010Accepted 2 July 2010

Keywords:MFCBiocatalystShewanellaPseudomonasGeobacter Wastewater speciesBiocathode

a b s t r a c t

Theadvent behind microbial fuel cells (MFC) is to provide clean electricity from the waste organic mate-rial.The MFC produces electricitywith thehelpof microorganisms. In thepresent review, thebiocatalystsor microorganisms used in the MFCs are discussed. The most used microorganisms in the MFCs belong

to Shewanella , Proteobactor and Pseudomonas families. In waste water based MFCs, mixed cultures aremostly used. This review covers the biocatalysts used in both anode and cathode. In the recent times,one of the most valuable development in the MFCs is the use of biocathodes, which eliminated variousdrawbacks of these cells and enhanced the power generation capabilities as well as the production of some useful gases like hydrogen. Thepresent state of art of this technology still requires development incertain power output areas such as improvement of efciency and cost reduction.

2010 Elsevier Inc. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1791.1. Microbial fuel cells . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .179

2. Bacteria used in MFC . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1802.1. Shewanella species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1802.2. Pseudomonas species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1812.3. Geobacter species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1812.4. Wastewater species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1832.5. Biocathodes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1852.6. Miscellaneous species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

3. Conclusions and future prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187A c k n o w l e d g m e n t . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .187R e f e r e n c e s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .187

1. Introduction

Fuel cells need notbe bigto sitoutside buildingsor in rooms,norneed they be streamlined to t in an automobile. They can be verysmall andcan runon organic matter. There is presentlya niche mar-ket for stationary fuel cells, about the size of a one-car garage with300200kW fuel-cell power plants operating around the world.Biological waste materials may be anaerobically digested, subjected to pyrolysis, or otherwise pretreated to release hydrogen.Unfortunately, rawbiobasedmaterials cannotbe throwninto a fuelcell, because they currently require preliminary processing.

Corresponding author. Tel.: +91 33 23525106; fax: +91 33 23525106.E-mail address: [email protected] (P.P. Kundu).

1.1. Microbial fuel cells

The microbial fuel cell is a device that converts biochemicalenergyinto electrical energywith theaid of thecatalytic reaction of microorganisms [1] . Microbial fuel cells use bacteria or yeast cellsas a catalyst, direct electron transport or in some cases mediatorsas electron shuttles and oxidizing agents as electron acceptors. Thestructure of the fuel cell is essentially an anode compartment withcells, with or without mediator, and an electrode separated froma cathode compartment. Membranes can be required if the anodechamber is anaerobic and the cathode uses oxygen. The cathodecompartment comprisesan electrodeand an electron acceptor.Theanode and cathode are connected via a circuit and electrons owfrom the biological cells to the cathode electron acceptor becauseE potentials of the active components are arranged in an ascend-

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180 V. Sharma, P.P. Kundu / Enzyme and Microbial Technology 47 (2010) 179188

Fig. 1. Schematic of the basic components of a microbial fuel cell. The anode andcathode chambers are separated by a membrane. The bacteria grow on the anode,oxidizing organic matter and releasing electrons to the anode and protons to thesolution. The cathode is sparged with air to provide dissolved oxygen for the reac-tions of electrons, protons and oxygen at the cathode, with a wire (and load)completing the circuit and producing power. The system is shown with a resistorused as the load for the power being generated, with the current determined based

on measuring the voltage drop across the resistor using a multimeter hooked up toa data acquisition system.

ing order. A schematic of an MFC system is shown in Fig. 1. Almostall reported microbial fuel cells employ bacteria as the catalyst andthe trend is to use a consortium of organisms, often isolated fromthe waste stream, and then subjected to selection in the fuel-cellenvironment. Power produced is very low, but techniques exist toconvert this to useful power levels. Very dilute organic wastes thatcannot serve as substrates in other energy production systems canbe used as energy source for microbial fuel cells. The microbial fuelcell notonly recovers energy from dilutewaste, butwill also simul-taneouslybioremediate the waste, a process thatcurrentlyrequiresenergy input [2,3] .

The MFC that utilizes mediator as electron shuttle is calledmediator-based-MFC. The electron transfer from certain microbialcells to the electrode is facilitated by the help of mediators such asthionine, methylene blue, humic acid and so on [4] . Electrons arecaptured by the oxidized mediator and transferred to the anode.At the anode the mediator is oxidized, a process that releases elec-trons to the anode and returns the mediator to its reduced state.The ideal mediator has the following properties: (i) It should dis-play reversible redox reaction to function as an electron shuttle;(ii) It should have appreciable solubility in an aqueous solution andstability; (iii) It should facilitate the electron transfer; and (iv) Itshould have low formal potential. The lower the formal potential,thelarger thecellvoltage since itis thedifferencebetween thecath-ode and anode potentials [5] . Up to now most study have focused

on the generation of electricity by Fe(III)-reducing bacteria [1,6] ,glucose and starch fermenting bacteria [7] , Sulfate-reducing bac-teria [8] and others such as E. coli, Enterobacter aerogens and so on[4] . The detailed list of different microorganism at anode is givenin Table 1 .

However, there are MFCs in which mediator is excluded, knownas mediatorless-MFC. In the mediatorless-MFC, electrochemicallyactive bacteria are used to ensure high rates of fuel oxidation andelectron transfer for the production of electrical energy.

2. Bacteria used in MFC

The development of processes that can use bacteria to produceelectricity represents a plausible method for bioenergy produc-

tion as the bacteria are self-replicating, and thus the catalysts for

Table 1Species studied by the researchers in anode chamber.

S. no. Species References

1. E. coli Potter [14] , Zhang et al. [15] ,Habermann and Pommer [22] ,Zou et al. [59] , Park and Zeikus[60] , Qiao et al. [61] , Xi and Sun[62]

2. Shewanella oneidensis DSP10 Ringeisen et al . [16] , Bifnger

et al. [18,19]3. Shewanella oneidensis MR-1 Manohar et al. [17] , Bifnger etal. [18]

4. Shewanella putrefaciens Kim et al. [1] , Park and Zeikus[21]

5. Pseudomonas aeruginosa Habermann and Pommer [22] ,Rabaey et al. [2324]

6. Geobacter sulfurreducens Bond et al. [26] , Reguera et al.[27,31] , Trinh et al. [33]

7. Geobacteraceae Holmes et al. [29] , Bond et al.[30]

8. Geobacter metallireducens Min et al. [32]9. Dessulfobulbus propionicus Lovley et al. [53]

10. Geothrix fermentans Lovley et al. [54]11. Paracoccus denitricans and

Paracoccus pantotrophusRabaey et al. [55]

12. Rhodopseudomonas palustrisDX-1

Xing et al. [56]

13. Klebsiella pneumoniae Lewandowski et al. [57,58]

organic matter oxidationare self-sustaining.Bacterial reactionscanbe carried out over a wide range of temperatures depending onthe tolerance of bacteria, ranging from moderate or room-leveltemperatures (1535 C) to both high temperatures (5060 C) tol-erated by thermophiles [9] and low temperatures (


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V. Sharma, P.P. Kundu / Enzyme and Microbial Technology 47 (2010) 179188 181

20mA/m 2 for RVC and GF, while short circuit current densitiesreached 32 mA/m 2 forGF anodesand 100 mA/m 2 forRVC. Theaddi-tion of electron mediators resulted in current and power increasesof30100%. These powerdensities were surprisinglyhighfor a pureS. oneidensis culture. They observed that the short diffusion lengthsand thehigh ratio of surface area to chamber volume utilized in themini-MFC, enhanced the power density when compared to outputfrom similar macroscopic MFCs.

Manohar et al. [17] determined the internal resistance ( Rint

) o f amediatorless microbial fuel cell (MFC) as a function of cell voltageusingelectrochemical impedancespectroscopy (EIS)for a MFC withand without S. oneidensis MR-1. The same tests were performedfor a MFC containing small stainless steel (SS) balls in the anodecompartment with a graphite feeder electrode in a packed bed cell.They observed that Rint decreased with decreasing cell voltage asthe increasing current ow decreased the polarization resistanceof the anode and the cathode. In the presence of MR-1, Rint waslower by a factor of about 100 than Rint of the MFC with buffer andlactate as anolyte. Rint was also signicantly lower for the anodecontaining SS balls with buffer and lactate as anolyte. For the MFCcontaining SS balls in the anode compartment, further no signi-cant decrease of Rint was obtained. When MR-1 was added to theanolyte, the polarization resistance of the anode was lower thanthat of the cathode.

Bifnger et al. [18] compared S. oneidensis MR-1 with DSP 10.MiniatureMFCs usingbare graphite feltelectrodesand nanoporouspolycarbonate membraneswith MR-1or DSP10cultures generated>8W/m 3 and 400 A between pH 67. The DSP10 strain signi-cantly outperformed MR-1 at neutral pH. Higher concentrations of DSP10 were sustained at pH 7 relative to that of MR-1. Whereasat pH 5, this trend was reversed, indicating that the cell count wasperhaps not solely responsible for the observed differences in cur-rent, but also by changes in the amount of autologous redox activemediators in the growth media at lower pH values. S. oneidensisMR-1 was determined to be more suitable than DSP10 for MFCswith elevated acidity levels. The concentration of riboavin in thebacterial cultures was reduced signicantly at pH 5 for DSP10, as

determined by high performance liquid chromatography (HPLC) of the ltered and sterilized growth media. In addition, these resultssuggest thatmediatorbiosynthesis and not solely bacterialconcen-tration plays a signicant role in current output from S. oneidensiscontaining MFCs.

Inanother report, Bifnger etal. [19] useda miniature-microbialfuel cell to monitor biolm development from a pure culture of S. oneidensis DSP10 on graphite felt (GF) under minimal nutri-ent conditions. They observed the formation of biolms after 5days at 25 C. The power generated with the biolm-enhancedanode (26W/m 3 for Pt/C GFO 2 and 250W/m 3 for uncoatedGF-ferricyanide) was 60% of that generated with the planktonicculture (150 W/m 3 for Pt/C GFO 2 and 420 W/m 3 for uncoated GF-ferricyanide). The power output increased during the operation of

the fuelcellas the solution-phasebacterialconcentrationincreasedin the reservoir. The power densities per unit volume produced bythe DSP10-only biolm was comparable with MFCs using mixedcultures with either ferricyanide or oxygen reduction cathodes.

Kim et al. [1] used S. putrefaciens in a mediatorless-MFC. Theystudied direct electron transfer fromdifferent S. putrefaciens strainsto an electrode through cyclic voltammetry and a fuel-cell typeelectrochemical cell. Both methods studied the electrochemicalactivity of the bacterium without any electrochemical mediators.It was observed that the anaerobically grown cells of S. putrefaciens MR-1, IR-1, and SR-21 showed electrochemical activities,but no activities were observed in aerobically grown S. putrefaciens cells. The current generation from the metal reducingbacterium depended on the electrochemical activity of bacterium,

principally oxidation of fuel by the bacterial metabolism, and

the direct electron transfer capacity from the bacterial surface tothe electrode.

In another study, cysteine was used as substrate for the elec-tricity generation using a MFC [20] . 16S ribosomal RNA (16S rRNA)based analysis of the biolm on the anode of the MFC indicatedthat the predominant organisms were Shewanella spp. closelyrelated to Shewanella afnis . It was reported that over a period of a few weeks, electricity generation gradually increased to a maxi-mum power density of 19 mW/m 2 (1000 resistor; 385 mg/L of cysteine). Power output increased to 39 mW/m 2 , when cysteineconcentrations were increasedup to 770mg/Land external resistorchanged to493 .TheuseofamoreactivecathodewithPtorPtRu,increased the maximum power from 19 to 33 mW/m 2 , showingthat the cathode efciency had limited the power generation. Elec-tron recovery was 14% based on complete cysteine oxidation, withan additional 14% (28% total) potentially lost to oxygen diffusionthrough theproton exchange membrane.Park andZeikus [21] stud-iedthe effectof electrodecompositionon theelectricitygenerationina singlecompartment fuel cell using S. putrefaciens .Theyreportedthat the electricity production was dependent on anode compo-sition, electron donor type and cell concentration. A maximumcurrent of 2.5 mA and a current density of 10.2 mW/m 2 electrodewere obtained with a Mn 4+ graphite anode, 200mM sodium lactateanda cell concentration of 3.9g cell protein/mL. Current productionby S. putrefaciens was enhanced 10-fold when an electron mediator(i.e., Mn 4+ or neutral red) wasincorporatedinto thegraphiteanode.

2.2. Pseudomonas species

Pseudomonas aeruginosa is a member of the Gamma Proteobac-teria class of Bacteria. It is a Gram-negative, aerobic rod belongingto the bacterial family Pseudomonadaceae . Since, the revisionisttaxonomy is based on conserved macromolecules (e.g. 16S rRNA)the family includes only members of the genus Pseudomonas . P.aeruginosa is the type species of its group, which contains 12 othermembers. Habermann and Pommer [22] in 1991 studied biologi-cal fuel cells using cost effective fuel storing materials like sulde.

They pioneered a low maintenance fuel-cell system with long-term stability and high short-term output. They used a variety of microorganisms.The various bacterial strains were P. aeruginosa , E.coli , Proteus vulgaris , etc.

Rabaey et al. demonstrated that exogenous mediators didnot have to be added to a culture [23,24] . These self-producedor endogenous chemical mediators, for example pyocyanin andrelated compounds produced by P. aeruginosa , can shuttle elec-trons to an electrode and produce electricity in an MFC [24] . Theproduction of high concentrations of mediators by mixed culturesprimarily containing P. aeruginosa , coupled with a very lowinternalresistance MFC were achieved by using ferricyanide as a catholyte(instead of oxygen), produced 3.14.2W/m 2 in MFCs [24] . Whenthe substrate was exhausted, soluble mediators were removed,

making it difcult for these compounds to accumulate to high con-centrations.

2.3. Geobacter species

Geobacter [25] is a genus of proteobacteria . Geobacter are ananaerobic respiration bacterial species which have capabilitiesthat may make them useful in bioremediation. The geobacter wasfound to be the rst organism with the ability to oxidize organiccompounds and metals, including iron, radioactive metals andpetroleum compounds into environmentally benign carbon diox-ide while using iron oxide or other available metals as electronacceptor.

Bond et al. [26] used Geobacter sulfurreducens in MFC cham-

bers, in which a graphite electrode served as the sole electron


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acceptor and acetate or hydrogen was the electron donor. Theelectron-accepting electrodeswere maintained at oxidizing poten-tials by connecting them to similar electrodes in oxygenatedmedium (fuel cells) or to potentiostats that poised electrodes at+0.2V versus an Ag/AgCl reference electrode (poised potential).When a small inoculum of G. sulfurreducens was introduced intoelectrode-containing chambers, the electrical current productionwas dependent upon the oxidation of acetate to carbon dioxideand increased exponentially, indicating for the rst time that elec-trode reduction supported the growth of this organism. When themedium was replaced with an anaerobic buffer lacking nutrientsrequired for growth, but consisting of acetate, current productionwas unaffectedand acetate-dependent cells attached to theseelec-trodes continued to generate electrical current for weeks.

This represents the rst report of microbial electricity produc-tion solely by cells attached to an electrode. Electrode-attachedcells completely oxidized acetate to levels below detection(


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of 418470mW/m 2 , obtained at an external resistor of 1000 ,wasincreased over 2-fold (from 418 to 866mW/m 2 ) as the Pt loadingon the cathode electrode was increased from 0.5 to 3.0mg Pt/cm 2 .The optimal batch mode temperature was between 30 and 32 Cwith a maximum power density of 418470mW/m 2 . It was alsonoted that the power density increase was disproportional to theplatinum concentration increase.

2.4. Wastewater species

Habermann and Pommer [22] rst reported the wastewaterbased MFCs in 1991. Logan and co-workers [34,35] have doneconsiderable work on the electricity generation from wastewatermicroorganisms. Min and Logan [34] also used a at plate micro-bial fuel cell (FPMFC) for continuous electricity generation fromdomestic wastewater and organic substrates. This microbial fuelcell wasdesignedto function as plug owreactor using a combinedelectrode/proton exchange membrane (PEM) system. The reactorconsisted of a single channel formed between two nonconductiveplates that were separated into two halves by the electrode/PEMassemblyalso knownas membraneelectrode assembly(MEA). Eachelectrodewas placedon anoppositesideof thePEM,withthe anodefacingthe chamber containing theliquid phase andthe cathode fac-ing a chamber containing only air. Electricity generation using theFPMFC was examined by continuously feeding a solution contain-ing wastewater, or a specic substrate, into the anode chamber.The system was initially acclimated for 1 month using domesticwastewater or wastewater enriched with a specic substrate suchas acetate. Average power density using only domestic wastewaterwas 72 1mW/m 2 at a liquid ow rate of 0.39mL/min [42% COD(chemical oxygen demand) removal, 1.1 h HRT (hydraulic reten-tion time)]. At a longer HRT = 4.0h, there was 79% COD removaland an average power density of 43 1mW/m 2 . Power outputwas found to be a function of wastewater strength accordingto a Monod-type relationship, with a half-saturation constant of K s = 461 or 719 mg COD/L. Power generation was sustained at highrates with several organic substrates (all at 1000mg COD/L),

including glucose (212 2 mW/m 2 ), acetate (286 3mW/m 2 ),butyrate (220 1 mW/m 2 ), dextran (150 1 mW/m 2 ), and starch(242 3mW/m 2 ). These results demonstrated the versatility of power generation in a MFC with a variety of organic substrates andshowed that power can be generated at a high rate in a continuousow reactor system.

The effect of electrode spacing and advective ow through theporous anode on the power generation by a microbial fuel cell hasbeenstudiedbyLoganand co-workers [35] . It wasobserved that themaximum power density from a MFC with glucose decreased from811 to 423 mW/m 2 , when the electrode spacing was decreasedfrom 2 to 1 cm. The MFC congurations showing different elec-trode spacing are shown in Fig. 2. When the electrode spacingwas reduced from 2 cm (anode exposed to only one side of the

uid; case A in Fig. 2) to 1 cm (anode exposed to both sides of theuid; case B),the maximum power density with glucose (500 mg/L)decreased from 811 to 684 mW/m 2 . If the anode was placed 1 cmfrom the cathode and exposed to only one side of the uid (caseC), the maximum power density further decreased to 423mW/m 2 .Power density decreased under these conditions even though Rintdecreased from 35 (2 cm) to 16 (1cm) (cases A and C). Thedecrease in Rint shouldhaveresultedin anincrease inpoweroutput,even though the difference in Rint was insignicant. The differencewas insignicant due to the reported Rint being at the wrong levelof magnitude, since with EIS it can only represent the ohmic losses.Still,it wasveryinterestingto seethatpower density also decreasedwith the improvement in the internal losses. The coulombic ef-ciency (CE) decreased from 28% (A) to 18% (C) with a decrease in

the electrode spacing. The decrease in the power density in both

cases, when the anode was moved closer to the cathode, resultedfrom decreased activity of the bacteria on the anode, as shownby a decrease in the open circuit potentials (OCPs) of the anode.The open circuit voltages (OCVs) measured for these three caseswere 0.820 V (A), 0.797 V (B), and 0.783 V (C). The OCPs of the cath-ode were essentially constant (0.268 V, A; 0.267 V, B; and 0.266V,C). Thus, the changes in the OCVs were directly a result of theincreased anode potentials, which were 0.552V (A), 0.531V (B),and 0.516 V (C).

However, providing advective ow through the porous anodetoward the cathode substantially increased the power density,resulting in the highest maximum power densities yet achievedin an air-cathode system using glucose or domestic wastewateras substrates ( Fig. 2D). For glucose, with a 1-cm electrode spac-ing and ow through the anode with continuous ow operation of the MFC, the maximum power density increased to 1540 mW/m 2

(51W/m 3 ) and the CE increased to 60%. Using domestic wastew-ater (255 10mg of COD/L), the maximum power density was464mW/m 2 (15.5 W/m 3 ; CE = 27%), even though the ow throughthe anode could lead to plugging, especially for particulated sub-strates such as the domestic wastewater. Still, the system wasoperated using glucose for over 42 days without clogging. Theseresults showed that power output in the air-cathode single-chamber MFCcan be increasedby reducing theelectrode spacing, if the reactors operate in continuous ow mode with advective owthrough the anode toward the cathode.

Ieropoulos et al. [36] also referred to the inefciency of thelarge-scale reactor.They studied MFCbaseon carbon veiland inves-tigated the effect of stack conguration and scalability. In terms of power density expressed as per unit of electrode surface area andas per unit of anode volume, the small-sized MFC was superior toboth the medium- and large-scale MFCs by a factor of 1.5 and 3.5,respectively. Based on measured power outputfrom 10smallunits,a theoretical projection for 80 small units (giving the same equiv-alent anodic volume as one large 500mL unit) gave a projectedoutputof 10W/m 3 , which was approximately 50 times higher thanthe recorded output produced by the large MFC.

Ieropoulos et al. [37] investigated the behavior of MFC in waterby linking the cathodic half cell to an articial gill. The currentoutput at ambient temperature was 32 A, which was noted toincrease 100 A (200%) at 52 C. Also the increase in water owrate resulted in an increase in the output ranging from 135% to150%. Liu et al. [38] studied the effect of reactor architecture inmembrane-free single-chamber microbial fuel cells.The maximumpower density generated by the larger MFC (LMFC) containing acloth electrode was 16 W/m 3 (520mW/m 2 -cathode area) at a cur-rent density of 0.18mA/cm 2 , which was slightly higher than that(14W/m 3 ) of the smaller MFC (SMFC). They studied the effectof anode surface area, ionic strength, anode orientation, reactortype and biolm on the performance of the microbial fuel cell.They observed that the performance was improved to 20 W/m 3

(630mW/m2) at current density of 0.26mA/cm

2when the ionic

strength of the solution was increased from 100 to 300mM as aresult of the decreased internal resistance ( Rint =7.3 ).

He et al. [39] used articial wastewater in an upow micro-bial fuel cell for electricity generation. The reactor was fed withsucrose solution as the electron donor for a 5-month period andcontinuously generated electricity with a maximum power den-sity of 170 mW/m 2 . Thepowerdensityincreased with anincreasingchemical oxygendemand (COD) loading rates up to2.0 g COD/L/dayafter which, no further increase in power density were observed,indicating the presence of limiting factors. The internal resistancewas the main limiting factor for UMFC, which was 85 at themaximum power density and restricted the power output by caus-ing a signicant decrease in the operating potential. Fan et al.

[40] used bicarbonate buffer in microbial fuel cell and also out-


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Fig. 2. MFC congurations showing different electrode spacings. MFCs operated in batch mode with (A) 2-cm spacing, (B) 1-cm spacing with anode placed within chamber,and (C) 1-cm spacing. (D) Schematic and (E) prototype of the MFC with four sections used in continuous ow tests, where X , the distance between the electrodes (shownwith two sections, or X = 2 cm) is increased by adding additional 1-cm-long sections. The width of the rst two sections (inlet chamber) is xed at 2 cm.Reproduced with the permission of Environ Sci Technol 2006;40:2428 ACS Publishing, USA.

lined the proton transfer mechanism. The performances of MFCswith cloth electrode assemblies (CEA) were evaluated using bicar-bonate buffer solutions. A maximum power density of 1550W/m 3

(2770mW/m2) was obtained at a current density of 0.99mA/cm

2

using a pH 9 bicarbonate buffer solution. Such a power density was38.6% higher than that using a pH 7 phosphate buffer at the sameconcentration of 0.2M. They proposed a mechanism for the protontransfer (shown in Fig. 3) in the MFC on the basis of the quantita-tive comparison of free proton transfer rates, diffusion rates of pHbuffer species, and the generated current.

Venkata Mohan et al. [41,42] used wastewater based MFCfor the bioelectricity production. In another report, they [41]worked on a mediatorless-MFC in fed batch mode, usingselectively enriched hydrogen producing mixed culture underacidophilic microenvironment. Maximum voltage of 271.5 mV(5.43mA) and 304mV (6.08 mA) was recorded at operat-ing organic loading rates (OLR) of 1.165 kgCOD/m 3 day and

1.404kg COD/m3

day, respectively, when measured at 50

external. COD removal efciency of 35.4% {substrate degra-dation rate (SDR) of 0.412 kgCOD/m 3 day } and 62.9% {SDR,0.88 kg COD/m 3 day } was observed at OLRs 1.165kg COD/m 3 day

and 1.404 kg COD/m3

day, respectively. Maximum specic powerproduction of 0.163 W/kg CODR (1.165 kg COD/m 3 day; 50 ) and0.198W/kg CODR (1.404 kg COD/m 3 day; 100 ) was observedduring a stable phase of fuel-cell operation. Current den-sity of 747.96mA/m 2 (1.165 kg COD/m 3 day) and 862.85mA/m 2

(1.404 kg COD/m 3 day) was observed at 10 .The effect of anodic biolm growth on bioelectricity production

in single-chambered mediatorless-MFC using designed syntheticwastewater (DSW) and chemical wastewater (CW) was studiedby Venkata Mohan et al. [42] . Three MFCs (plain graphite elec-trodes, air-cathode, Naon membrane) were operated separatelywith variable biolm coverage [control; anode surface coverage(ASC), 0%], partially developed biolm [PDB; ASC 44%; 90 days]and fully developed biolm [FDB; ASC 96%; 180 days] under aci-

dophilic conditions(pH 6) at roomtemperature.The study depicted


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Fig. 3. Diagram of proton transfer mechanism in air-cathode MFCs with acloth/membrane layer. The monobasic phosphate/dibasic phosphate ion-pairaccounts for the major mechanism for protons transfer in air-cathode MFCs usingphosphate buffer,while bicarbonatecarbonate is themajor proton carrier for MFCsusing bicarbonate buffer.Reproduced with the permission of Environ Sci Technol 2007;41:8156 ACS Pub-lishing, USA.

the effectiveness of anodic biolm formation in enhancing theextracellular electron transfer in the absence of mediators. Cyclicvoltammetry analysis showed six-fold increment in energy out-put from control (1.812 mJ) to PDB (10.666mJ) operations andabout eight-fold increment in energy from PDB to FDB (86.856 mJ).Biolm congured MFC was shown to have the potential to selec-tively support the growth of electrogenic bacteria with robustcharacteristics, capable of generating higher power yields alongwith substrate degradation especially operated with characteris-tically complex wastewaters as substrates.

Huang et al. [43] studied the xylose degradation and gener-ated electricity using a two-chamber mediatorless-MFC. Voltageoutput followed saturation kinetics as a function of xylose concen-trationforconcentrationbelow 9.7mM, witha predictedmaximum

of 86mV (6.3mW/m2

or 116mW/m3) and half-saturation con-

stant ( K s ) of 0.29mM. Xylose concentrations from 0.5 to 1.5 mMresulted in coulombic efciencies and maximum voltage rangingfrom 41 1.6 to36 1.2%and 55 2.0 to70 3.0mV, respectively.Xylose degradation rate increased with increasing xylose concen-tration up to 9.7mM and the predicted maximum degradation ratewas 0.13mM/h and K s of 3.0 mM. Stirring by nitrogen in the anodechamber led to 99 2.3mV maximum voltage (8.4 0.4mW/m 2

or 153 7.1mW/m 3 ) and 5.9 0.3% coulombic efciency at MFCrunning time of 180h, which were respectively 17 1.2% and37 1.8%, higherthan those without stirring.A betterproton trans-port through thebuffer solution resulted in higherutilizationof theelectron donor. The COD removal under stirring was 22.1 0.3%,which was slightly lower than that of 23.7 0.4% under no stirring.

However, stirring resulted in 59% lower xylose degradation rate.Min et al. [44] also developed a submersible MFC (SMFC) byimmersingan anodeelectrodeand a cathode chamber in an anaero-bic reactor. They used domestic wastewater amended with acetateas medium. The maximum power generation was 204mW/m 2

with current density of 595mA/m 2 at a circuit resistance of 180(SCOD of wastewater = 1672 6 mg/L). The power output showeda saturation-type relationship as a function of wastewater concen-tration (SCOD), with a half-saturation coefcient of K s =244mg/Land a maximum power density of P max = 244mW/m 2 .

2.5. Biocathodes

The conventional MFC is a two-chamber system, consisting

of anode and cathode chambers that are separated by a proton

exchange membrane (PEM). This system has been half biologi-cal, because only the anode side contains electrochemically activemicroorganisms, while the cathode is abiotic. For this reason someresearchers [4550] h ave recently started working on the conceptof biocathodes. Instead of being catalyzed by platinum, the com-bination of protons, electrons and oxidants at the cathode couldbe catalyzed by a bacterial reaction. Biocathodes are of two types:(i) aerobic biocathodes use oxygen as the oxidant and microorgan-isms to assist the oxidation of transition metal compounds, suchas Mn(II) or Fe(II), for electron delivery to oxygen; (ii) anaerobicbiocathodes use compounds such as nitrate, sulfate, iron, man-ganese, selenate, arsenate, urinate, fumarate and carbon dioxideas terminal electron acceptors.

A bafe-chamber membraneless MFC was used for electricitygeneration by Hu [45] . They studied the inuence of reactor cong-urations designed tomitigatethe impactof oxygentransport on theelectricity generation. The reactor was constructed to reduce mix-ing in the vicinity of cathode and facilitate thick (>1 mm) biolmformation on the cathode by adding anaerobic biomass/sludge(4330 410 mgCOD/L), resulting in an overall coulombic efciencyof more than 30% at glucose concentrations ranging from 96 to960mg COD/L, compared to previously reported efciencies of


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With the development of microorganisms in both compartments,the internal resistance decreased from initial 40.214.0 .

Recently, Cao et al. [50] developed a photo-biocathode forcathodic carbon dioxide reduction. The biocathode used dissolvedcarbon dioxide (bicarbonate) as the acceptor. During acclimation,the cathode was set ata potential of0.242V (vs.SHE)usinga poten-tiostat. After approximately 1 month of acclimation, a current of 1 mA was sustained. Bicarbonate was reduced in stoichiometricagreement with current generation, with 0.28 0.02mol of bicar-bonate reduced per mole of electrons. When this biocathode wasused in a two-bottle MFC, a power density of 750 mW/m 2 was pro-duced. The maximum power generated by the biocathode withacetate asthe electrondonorwas 750 mW/m 2 . Incontrast, themax-imum power generated using a plain carbon cathode, was only50mW/m 2 . The power density of the biocathode was therefore15-fold larger than that achieved with an abiotic cathode control(Fig. 4 ). Theyalsocomparedthe biocathode performance withferri-cyanide, a commonly used chemical catholyte(50 mM K 3 [Fe(CN) 6 ],100mMPBS,pH7.0)( Fig.4 ). Under theseconditions, the maximumpower generated was 1050mW/m 2 , which was 40% greater thanthat of the biocathode. Results from Fig. 4 showed that the biocath-ode performance was comparable with the chemical cathode andfar better than the abiotic cathode.

Aldrovandi et al. [51] investigated the power production ina membraneless and mediatorless synthetic wastewater micro-bial fuel cell (shown in Fig. 5). They used a biological cathodeand a compact wastewater treatment reactor, fed with syn-thetic wastewater. When operated with an external resistance of 250 , the MFC produced a long-term power of about 70 mW/m 2

for 10 months. Denaturing Gradient Gel Electrophoresis (DGGE)analysis of the cathode biomass, when the MFC was closed ona 2100 external resistance showed that the sequence bandswere afliated with Firmicutes , -Proteobacteria , -Proteobacteria ,

-Proteobacteria ,and Bacteroidetes groups. Whenthe external resis-tance was varied between 250 and 2100 , minimum sustainable

Fig. 4. Comparison of MFC performance with abiotic control cathode, biocathodeand ferricyanide cathode, respectively.Reproduced withthe permission of EnergyEnvironSci 2009;2:500 RSCPublishing,UK.

resistance decreased from 900 to 750 , while maximum sus-tainable power output decreased from 32 to 28 mW/m 2 . Theseeffects were caused by changes in the microbial ecology of anodicand cathodic biomass attached to the electrodes. The untreatedgraphite biocathode was suitable support for aerobic bacteriacapa-bleof oxygenreduction forwastewater MFCs. This is an unexploredarea and requires further work.

Simultaneous organics removal and nitrication using a novelnitrifying biocathode MFC reactor was investigated by Tran et al.[52] . The introduction of nitrifying biomass into the cathode cham-ber caused higher voltage outputs than that of MFC operated withthe abiotic cathode. They observed that the maximum power den-sity increased 18%, when the cathode was run under the bioticcondition and fed by nitrifying medium with alkalinity/NH 4 +N

Fig. 5. Reactor design: (1) rst anaerobic chamber; (2) second anaerobic chamber; (3) aerobic chamber; (4) settling tank. The anaerobic bafed reactor (ABR, chambers#1 and #2) sediments and ferments easily degradable COD, in series with an activated sludge process (chambers #3 and #4), which nitries and further reduces organiccompounds. Electrodes are connected via an external circuit on a load variable between 250 and 2100 . The volumes of the four compartments are 18, 18, 22, and 5 L,respectively.

Reproduced with the permission of Bioresour Technol 2009;100:3253 Elsevier Ltd.


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ratio of 8 (26 against 22mW/m 2 ). The voltage output was not dif-ferentiated when NH 4 +N concentration was increased from 50 to100mg/L undersuch alkalinity/NH 4 +Nratio. Themaximumpowerdensity increased by 68% in comparison with the abiotic cath-odeMFC (37against22 mW/m 2 ). Polarizationcurvesdemonstratedthat the both the activation andconcentration losses were loweredduring the period of nitrifying biocathode operation. Ammoniumwas totally nitried and mostly converted to nitrate in all casesof the biotic cathode conditions, and in addition high COD removalefciency(98%)was achieved.The application of nitrifyingbiocath-odes makes itpossibleto integratethe nitrogen andcarbon removalin MFC systems.

2.6. Miscellaneous species

Lovley et al. used Dessulfobulbus propionicus [53] and Geothrix fermentans [54] for electricity generation. The Fe(III)-reducingorganism D. propionicus and G. fermentans conserved energy tosupport growth by coupling the complete oxidation of acetate toreductionof a graphiteelectrode. Geothrix cells were able todirectlyreduce electrodes in the absence of an electron shuttle, but theaccumulation of a mediator over time further enhanced the rate of electron transfer [54] . G. fermentans transferred more than 80% of the electrons, available in their organic substrates, for the electric-ity. Rabaey et al. [55] used microbial fuel cells for sulde removal.Microbial fuel cells were coupled to an anaerobic upow ludgeblanket reactor, providing total removals of up to 98% and 46%of the sulde and acetate, respectively. The MFCs were capableof simultaneously removing sulfate via sulde. This demonstratedthat digester efuents can be polished by a MFC for both residualcarbon and sulfur compounds. The recovery of electrons from sul-des implied a recovery of energy otherwise lost in the methanedigester. They had isolated sulde oxidizing organisms Paracoccusdenitricans (with nitrate as the electron acceptor) and Paracoc-cus pantotrophus . The Paracoccus species possess a membranebound complex that allows sulde oxidation by the respiratorychain.

Xinget al. [56] investigated the Rhodopseudomonas palustris DX-1 for the electricity generation and found that it was capable of high power production of the order of 2720 60 mW/m 2 . The vol-ume size of the MFCs was 22 and 24 mL with 7cm 2 total exposedsurface area of the electrode. The internal resistance was approxi-mately 8 and the external load was xed at 1000 . Strain DX-1utilized a wide variety of substrates (volatile acids, yeast extract,andthiosulfate) forpowerproduction in differentmetabolic modes,making it highly useful for studying the power generation in MFCsand generating power from a range of simple and complex sourcesof organic matter. Lewandowski et al. [57,58] operated a microbialfuel cell in which glucose was oxidized by Klebsiella pneumoniae[57,58] in the anodic compartment,andbiomineralizedmanganeseoxides, deposited by Leptothrix discophora [58] , were electrochem-

ically reduced in the cathodic compartment.E. coli is also reported as the biocatalyst in the MFCs [5962] .

Zou et al. [59] constructed a MFC using polypyrrole coated car-bon nanotubes (CNTs) composite as an anode material and E. colias the biocatalyst. In another report, Park and Zeikus [60] inves-tigated MFC, where neutral red (NR) was utilized as an electronmediator consuming glucose to study both its efciency duringelectricity generation and its role in altering anaerobic growth andmetabolism of E. coli and Actinobacillus succinogenes . Qiaoet al. [61]investigated the electrochemistry and electrocatalytic mechanismof evolved E. coli cells in MFCs. Xi and Sun [62] reported the pre-liminary study on E. coli based MFC and on-electrode taming of thebiocatalyst. The maximum power density reached 263.94mW/m 2

with the corresponding current density 1287.50mA/m 2 and the

internal resistance of MFC was 200 .

3. Conclusions and future prospects

MFC represents a potential method for bioelectricity genera-tion and waste treatment although signicant technical barriersexist. MFC converts the chemical energy released in the oxidationof organic wastes directly to electric energy. The detailed char-acterization of the interfacial electron transfer rates, biocatalyticrate-constants and cell resistances is essential upon the construc-tion of the biofuel cells. Identication of the rate-limiting stepsallows then the development of strategies to improve and enhancethe cell output. The stepwise nano-engineering of electrode sur-faces with relay-co-factor-biocatalyst units by organic synthesisallowsustocontroltheelectrontransfercascadesintheassemblies.

The production of electrical energy from biomass substratesusing biofuels could complement energy sources from chemicalfuel cells. Recently, the use of biocathodes in microbial fuel cellssolved various problems like requirement of a catalyst or articialelectron mediators, which are very costly. These biocathodes canproduce useful products or remove unwanted compounds. There-fore, the development of new methodologies could curb the lengthof time needed for the realization of alternative sources of bioelec-tricity. In addition, these developments will lead to clean andgreenenvironment.

Acknowledgment

Authors specially acknowledge the reviewers of the manuscriptfor enabling us to rene the manuscript.

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Review Paper-V_Biocatalysts in Microbial Fuel Cells

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