Brazilian Journal

of Chemical ISSN 0104-6632 Printed in Brazil Engineering www.abeq.org.br/bjche

Vol. 34, No. 01, pp. 211 - 225, January - March, 2017 dx.doi.org/10.1590/0104-6632.20170341s20150377

MATHEMATICAL MODELING OF THE ELECTRIC CURRENT GENERATION IN A MICROBIAL FUEL CELL INOCULATED WITH MARINE SEDIMENT

J. T. Teleken1, J. de Sá Silva2, M. F. Fraga3, C. S. Ogrodowski2, F. B. Santana2 and B. A. M. Carciofi1*

1Department of Chemical and Food Engineering, Federal University of Santa Catarina, (UFSC), Campus João David Ferreira Lima, Trindade, CEP: 88040-900, Florianópolis - SC, Brazil. Phone + 55 48 37216408; Fax: + 55 48 37219687 *E-mail: [email protected] 2School of Chemistry and Food, Federal University of Rio Grande, (FURG), Campus Carreiros, Avenida Itália, km 08, PO Box 474, CEP: 96.201-900, Rio Grande - RS, Brazil. 3State Power Generation and Transmission Company, (CEEE-GT), Av. Joaquim Porto Villanova 201, CEP: 91410-400, Porto Alegre - RS, Brazil.

(Submitted: April 1, 2015 ; Revised: September 3, 2015 ; Accepted: October 5, 2015)

Abstract - Microbial fuel cells (MFC) are electrochemical devices that utilize the ability of some microorganisms to oxidize organic matter and transfer electrons resulting from their metabolism to an insoluble acceptor. The goal of the present study was to model the kinetics of electrical current generation from an MFC inoculated with marine sediment. For this purpose, a differential equation system was used, including the Nernst-Monod relationship and Ohm's Law, to describe the microbial metabolism and the mechanism of extracellular electron transfer (EET), respectively. The experimental data obtained by cyclic voltammetry analysis were properly described by the model. It was concluded that marine microorganisms preferably use a direct mechanism of EET by means of nanowires to establish the electrochemical contact with the anode. The mathematical modeling could help understand MFC operation and, consequently, contribute to improving power generation from this source. Keywords: Waste treatment; Biofilm; Nanowires; Effluent; Green energy.

INTRODUCTION energy and waste treatment (Pant et al., 2010; ElMe- kawy et al., 2015). A wide variety of microorganisms have the ability A classical MFC design includes two compart- to reduce insoluble compounds such as metal oxides ments, an anaerobic anodic chamber and an aerobic as a part of their strategy to obtain energy. This abil- cathode chamber, separated by a cation exchange ity has received considerable attention due to the membrane. In this system, electricity is generated possibility of generating electric energy from organic when microorganisms transfer electrons from the matter in microbial fuel cells (MFC) (Lovley, 2012). oxidation reaction of organic matter to an electrode A MFC can utilize complex organic substrates, in- (anode) connected to an electrical circuit. From the cluding domestic, industrial, and agricultural waste- anode, electrons are conducted through the circuit to water, as a source to produce power, drawing attention a second electrode (cathode), separated from the first as a promising technology connecting sustainable by the cation exchange membrane, where they com-

*To whom correspondence should be addressed

212 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi bine with protons and with the final acceptor in a is done by mediators, it can be modeled by applying reduction reaction. Thus, a positive and a negative Fick's law (Picioreanu et al., 2007, 2010) or, if trans- charge density are present at the cathode and at the port is by conduction through the solid components anode, respectively, resulting in a potential differ- of the biofilm, it can be modeled by applying Ohm's ence for electron transport in the circuit and leading law (Marcus et al., 2007). The reactions occurring to power generation (Logan and Regan, 2006, between the EET mechanism and the electrode are Oliveira et al., 2013a; Venkata Mohan et al., 2014; described by electrochemical models, such as the ElMekawy et al. 2015). Butller-Volmer relationship (Picioreanu et al., 2007, Exoelectrogenic microorganisms are naturally 2010; Zeng et al., 2010). found in anaerobic environments such as aquatic sedi- In light of the above, the objective of this study ments (Tender et al., 2002; Holmes et al., 2004), soils was to identify the main EET mechanism and math- (Niessen et al., 2006; Futamata et al., 2013), and ematically model the electric current generation ki- sludge from waste treatment plants (Kim et al., 2004). netics as a function of the electrical potential of the Preferably, they develop adhered to the surface of the anode of a dual-chamber MFC inoculated with sedi- electrodes in the form of biofilms and are able to use ment of marine origin. diverse anaerobic metabolic pathways to oxidize the carbon sources (Venkata Mohan et al., 2014). This microbial class establish as electrochemical MATERIALS AND METHODS contact with such electrodes using three distinct mechanisms of extracellular electron transfer (EET): Inoculum and Culture Medium 1) direct contact between the proteins present in the cell membrane (cytochromes) and the anode (Bond Sediment of marine origin, collected on the south- and Lovley, 2003); 2) diffusion of self-produced elec- ern coast of Brazil (Rio Grande, RS, Brazil), was used tron carriers, such as flavins or some artificial redox as inoculum for the MFC. The culture medium used -1 mediators, between cells and the anode (Rabaey et was composed of NaHCO3 (2.5 g L ), CaCl2·2H2O -1 -1 -1 al., 2004; Marsili et al., 2008a); and 3) conduction of (0.1 g L ), KCl (0.1 g L ), NH4Cl (1.5 g L ) NaH2PO4 -1 -1 electrons through solid components such as the ex- H2O (0.6 g L ) Na2HPO4·12H2O (1.87 g L ), NaCl -1 -1 tracellular materials (nanowires) and the multiple (0.1 g L ), MgCl2·6H2O (0.1 g L ), MgSO4 7H2O -1 -1 bacterial layers that comprise the biofilm (Reguera et (0.1 g L ), MnCl2·4H2O (0.005 g L ) NaMoO4 2H2O al., 2006; Gorby et al., 2006). Biofilms with mixed (0.001 g L-1), and yeast extract (0.05 g L-1). Acetate - culture can present more than one of these EET, ion (CH3COO ) was used as carbon source (electron whereas a pure biofilm tends to be limited (Venkata donor) at concentrations of 5 g L-1 and 10 g L-1 of Mohan et al., 2014; Sharma et al., 2014). COD. Initially, the MFC was inoculated with the sus- Therefore, to model the kinetics of electrical cur- pension obtained by mixing marine sediment (at 5 g L-1 rent generation in a MFC, one should consider the of COD) with the culture medium at a 2:1 (w/w) ratio. intracellular overpotential, associated with the bio- logical reaction, and the extracellular overpotentials, Microbial Fuel Cell associated with the EET mechanism and the transport of substrate and metabolites within the The experiments were performed in a dual-cham- biofilm. Microbial kinetics in biological reactors are ber acrylic MFC with a total volume of 2.5 L, 60% often modeled by the Monod relationship (Rittmann destined for the anodic chamber (1.5 L) and 40% and McCarty, 2001); however, this model cannot be dedicated to the cathodic chamber (1 L). A cation used in its original form to describe the current gen- exchange membrane (Membranes International Inc., eration kinetics in an MFC. Thus, according to the CMI-7000S, USA) was used to separate both cham- EET mechanism employed by the biofilm, different bers. Graphite plates with a surface area of 115 cm² behaviors are expected. Systematically, the models each were used as electrodes. In the anodic chamber, available in the literature state that the biological the two graphite plates were placed at 5 and 10 cm reaction can be described by a dual limitation rela- from the membrane, while, in the cathodic chamber, tionship, which involves the substrate concentration the plate was placed at 5 cm from the membrane. and the contraction or the electric potential of the Figure 1 illustrates the MFC configuration. An exter- EET mechanism (Picioreanu et al., 2007, Marcus et nal resistor (Rext) of 1 kΩ connected both anodic elec- al., 2007, Pinto et al., 2010; Oliveira et al., 2013b). trodes to the cathodic electrode. The anodic chamber The EET is modeled according to the mechanism was kept under constant agitation by an impeller at used by the exoelectrogenic bacteria: If the transport 300 rpm. In the cathodic chamber, a 50 mM potassium

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Modeling a Microbial Fuel Cell with Marine Sediment 213

-1 -1 ferricyanide (K3Fe(CN)6) solution was used as the 2.50 L d (CON2), day 149 and 1.77 L d (CON3), final electron acceptor. The MFC was stored in a ther- day 170 and 2.77 L d-1 (CON4), day 191 and 2.50 L d-1 mostat-controlled chamber (Eletrolab, model EL101/2, (CON5), day 212 and 4.60 L d-1 (CON6), day 246 Brazil) to keep the operation temperature constant at and 9.66 L d-1 (CON7), and day 268 and 17.43 L d-1 35 °C over the 280 days of the experiment. (CON8). The cathodic chamber was operated in batch mode. The solution of potassium ferricyanide was periodically replaced every 12 days on average, to- taling 23 renewals of the solution.

Electrochemical Monitoring

The voltage developed between the anode and the cathode (Vcel), was measured with a digital multime- ter (Icel, MD6680, Brazil) and a software (Icel, UT803 version 1.00, Brazil) was used for data acquisition Figure 1: Schematics of the MFC and the electrode and recording on a computer terminal every 60 s. geometry. A1 and A2 are the anodes, C the cathode The current density j (A m-2) was determined from and M the cation exchange membrane. Equation (1), by measuring the Vcel of the electrical

circuit with external resistance Rext (Ω). Operating Conditions

1  Vcel  The anodic chamber was operated in batch mode j    (1) during the first two days of the experiment (startup ARanode ext  period). Next, operational cycles alternatingly com- posed of sequential batch and continuous regimes in which Aanode is the total area of the anodes (0.023 were initiated. From the 37th day onwards, the ace- m2). tate concentration in the feed solution increased from 5 g L-1 to 10 g L-1 of COD. Cyclic Voltammetry - Biofilm The sequential batch regime was carried out daily by renewing the anodic medium (24-hour feeding Cyclic voltammetry scans (CV), used to model cycles), according to the procedures described be- the current generation kinetics in the MFC, were low: 1) renewal of 0.3 L of the culture medium con- conducted after day 160 of reactor operation, ensur- taining 75% of solids present in the effluent removed ing the full development of the biofilm on the anode. from the anodic chamber (0.2 h); 2) Bio-electro- These were always carried out after the feed steps to chemical conversion of acetate in electric current minimize the effects of substrate limitation. After (23 h); 3) removing the effluent from the anodic cham- feeding (10 g L-1 of COD, 20% of the volume of the ber (0.2 h); 4) separation of suspended solids in the anodic chamber) the initial acetate concentration in effluent (0.6 h). The last step was performed in a the chamber was approximately 32.3 mM. When the centrifuge (Hitachi, model CR22 GIII, Japan), with acetate ion concentration is greater than 5 mM in re- the rotation set at 18,800 g. Approximately 75% of actors with Geobacter sulfurreducens biofilm forma- the solids obtained by centrifugation were suspended tion, additional acetate has no effect on the current in the feed solution and returned to the system, re- generation rate (LaBelle and Bond, 2010). On the establishing the volume of liquid in the reactor (step other hand, it was also observed that the electric 1). During the culture medium renewal procedure, current generated by a Geobacter sulfurreducens agitation in the chamber was temporarily interrupted. biofilm was affected only at acetate concentrations The continuous mode without cell recycle was below 3 mM (Marsili et al., 2008b). implemented by maintaining a constant flow rate of CV analyses were performed using a potentiostat the culture medium for 24 h. The operations were (Metrohm, PGSTAT 101, Switzerland), the reference performed with different feeding flows with the pur- electrode of Ag/AgCl 3 M KCl (Metrohm, pose of evaluating the effect of the material solu- 6.0726.100, Switzerland), the anode at 5 cm from the bilized in the anodic chamber on electric current membrane as working electrode, and the cathode as a generation. Eight operations were performed: on day counter electrode. The selected parameters to carry -1 25 and feed flow of 2.70 L d (CON1), day 129 and out the technique were: Einitial = -0.6 V (vs Ag/AgCl),

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214 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi

Efinal = 0.0 V (vs Ag/AgCl), equilibrium time of 5 s, model proposed by Marcus et al. (2007). This model scan rates of 0.2, 1, 2.5, 5, and 10 mV s-1, and 3 cy- is for exoelectrogenic biofilms that predominantly cles. The interval from -0.6 to 0.0 V vs Ag/AgCl (in use a direct mechanism of extracellular electron relation to the standard hydrogen electrode: -0.378 to transfer. The biofilm model assumes a matrix con- 0.222 V vs EPH) was selected in order to avoid inju- ductor, in which the rate of substrate consumption is ries to cells derived from the high-potential reduction limited by the local concentration of the electron or oxidation and at the same time ensure the evalua- donor (ED) and the local electrical potential within tion of the oxidation process of interest. This work- the biofilm. The expression that describes the rate of ing range is similar to that used in studies with some substrate consumption written as the flow of sub- of the microorganisms of Geobacter and Shewanella strate into the biofilm is known as the Nernst-Monod species (-0.558 to 0.242 V vs EPH) (Marsili et al., model, and is represented by Equation (2). 2008a, 2008b, 2010). The low scan rates were se- lected with the aim of reducing the effects of capaci-  SzED ()  tive current in the analysis response and reveal the JzqED() max f fL a f    SzKED() ED  biofilm’s catalytic behavior (Harnisch and Freguia, (2) 2012). In total, eight sets of CV analysis (different 1 rates) were performed on days 161, 182, 195, 206,  F 220, 226, 256, and 276 of operation. 1exp ()z  RT Cyclic Voltammetry - Anodic Effluent in which, JzED () is the mass flow of ED at a given The cyclic voltammetry analyses of the effluent spatial location within the biofilm (g m-2 s-1), q is from the anode chamber were performed to investi- max the maximum specific rate of ED consumption (g g-1 gate the importance of soluble compounds in current s-1),  is the specific biofilm mass (g m-3), f is the generation. While operating on a continuous basis, f a effluent samples of 40 ml were collected at 0, 3, 6, 9, volume fraction of active biomass, L f is the biofilm 12, 15, 18, and 21 h after the start of operation. The thickness (m),  (zEzE ) ( ) , Ez( ) is the samples were then transferred to a second electro- bio KA bio chemical cell to proceed with the CV analysis. A electric potential at a given spatial position in the glassy carbon electrode (Metrohm, OD = 6 mm, ID = biofilm (V), EKA is the biofilm’s electric potential 1.6 mm, QA017, Switzerland) was used as a working (V) for JzED() 0.5 qmax f fL a f , SzED ( ) is the electrode, and a platinum electrode (Metrohm, mass concentration of ED (g m-3) in a given spatial 6.0331.000, Switzerland) as counter electrode. The location of the biofilm, KED is the mass concentra- technique’s parameters were the same used in CV -3 analysis of the biofilm. tion of ED (g m ) so that JzED() 0.5 qmax f fL a f , F is the Faraday constant (C mol-1), R is the uni- Scanning Electron Microscopy versal gas constant (J mol-1K-1), and T is the system temperature (K). Scanning electron microscopy was used to quali- All CV analyses of the biofilm were performed tatively analyze the exoelectrogenic biofilm attached on the excess of the substrate, thus, the term refer- to the anode. Samples were collected from the anode Sz() ring to the limitation of ED, ED , in electrodes and analyzed in a Zeiss scanning electron SzK() microscope, model DMS-940, at the end of reactor ED ED operation (day 280). The samples were fixated with a Equation (2) is approximated to the unit, and effects solution of glutaraldehyde (6%), paraformaldehyde caused by the limited mass transport were not con- (6%), and 0.1 M cacodylate at a ratio of 1:1:1. Sub- sidered in the modeling. Ohm's law was used to sequently, samples were dehydrated and ethanol was describe the effects caused by the flow of electrons replaced with CO2. in the biofilm; it is represented by Equation (3) for a one-dimensional system. Mathematical Modeling of the Electric Current Generation Kinetics dz() jz() kbio (3) dz The mathematical model used to describe the -1 electric current generation kinetics was based on the in which, kbio is the biofilm conductivity (S m ).

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Modeling a Microbial Fuel Cell with Marine Sediment 215

The spatial charge distribution is described by the 0  1  jFfeq sfafmax fL  differential balance according to Equation (4):  F  1exp *  RT  1 (8) dj() z 0  1 Ffeq fF 0 (4)  j dz sfamax 1exp ()z max  RT F  1exp * RT

in which  s is the total number of moles of electrons in which * EEanode KA . that can be oxidized per gram of substrate (mol g-1)

0 and fe is the Coulomb efficiency that expresses the Numerical Solution fraction of the load transferred to the electrode versus the total amount available on the electron The CR model was made dimensionless by defin- donor. ing the spatial coordinate  0,1 as   zL / f . By combining Equations (3) and (4), and sub- 0 The equations are rearranged in the new coordinate stituting Fs fe qmaxfa f j max / L f, the expression and represented by Equation system (9), (10), (11), that describes the electrical potential gradient within and (12), in which C is the parameter defined as the the biofilm was obtained, i.e., Equation (5): ratio kLbio/ f .

2 1  d  dz() jmax jC   (9) kbio F 0 (5) d dz2 L 1exp ()z   0 f RT  2 d  1 in which j is the specific maximum current den- Cj max  0 (10) max d 2 F sity generated by the biofilm (A m-2). 1exp RT The only solution of Equation (5) requires two boundary conditions: the electric potential being con- stant at the anode/biofilm interface (Equation (6))  0 Vanode (11) and the absence of electronic flow in the biofilm/so- lution interface (Equation (7)): d C  0 (12) d  1 zV0,  anode (6) The solution of the equations was based on the d Finite Difference Method (Patankar, 1980), using a zLfbio, k 0 (7) mesh with fifty nodes with fixed spacing () of dz 1/49 between each, to represent the biofilm. The solution of the equation system in discrete form was in which V is defined in relation to E , anode KA obtained by Newton's method for nonlinear systems VEEanode anode KA , and Eanode is the electric (Burden and Faires, 2011). potential of the anode (V). The system formed by Equations (3), (5), (6), and Estimation of Parameters (7) was designed to model the electron transport resistance (CR model). An alternative form of a CR Data from the CV at a scan rate of 0.2 mV s-1 and model was also used in the analysis. For a biofilm in the direction of -0.6 to 0.0 V vs Ag/AgCl were with high electrical conductivity, the electric current used. The CR and SR models only deal with the generation kinetics are limited only by biological electrical current generation, i.e., the electron flow kinetics, written in terms of the density of electric direction occurring from the substrate to the current according to Equation (8), called the model electrode; thus, the portion of the cathodic current without resistance to electron transport (SR Model). was normalized to zero for fitting analyses.

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216 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi

The parameters of the SR model (Equation (8)), remained stable over the subsequent days of opera- jmax and EKA , were estimated by fitting the experi- tion. The maintenance of the electrical current gener- mental data using the function fit of the curve fitting ation in an asymptotic value characterizes the satura- tool in the software Matlab (MathWorks, 7:13, USA). tion phase of the biomass on the anode (Marsili et The CR model had the E and C parameters esti- al., 2008b). KA mated by minimizing the value of the root mean (A) 0.040,04 square error (RMSE, Equation (13)) between the electric current density data observed experimentally 0.030,03 ) -2 ( jexp ) and the data calculated by the model ( jcal ) 0.020,02 (A m (A j using an exhaustive calculation routine. The algo- 0.010,01 rithm designed to optimize process parameters was 0.000,00 implemented in the software Matlab (MathWorks, 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 Time (d) 7:13, USA). The value of the parameter jmax used in the calculation was the same determined by the SR (B) 0.040,04 (C) 0.040,04 ) 0.030,03 ) 0.030,03 -2 -2 model fitting. 0.020,02 0.020,02 (A m (A (A m (A j 0.010,01 j 0.010,01 CON7 0.000,00 0.000,00 N 0123456 244 245 246 247 248 1 2 Time (d) Time (d) RMSE jexp () n jcal () n (13) N  n1 Figure 2: MFC operational results: (A) Time evolu- tion of the electric current density (solid line) and in which n is the counter of the experimental data indication of operations in a continuous regime (dot- and N is the total number of experimental data ted lines); (B) Density of electric current generated points. by the MFC in the first 6 days of operation; (C) Den- The performance of the models was evaluated ac- sity of electric current during the seventh process of cording to two statistical indices: the Root Mean operation in the continuous regime (9.66 L d-1). Squared Error (RMSE, Equation (13)) and the coef- ficient of determination (R2, Equation (14)). During operations in the continuous regime, the electrical current generation is reduced slightly (in N 2 detail of Figure 2 (C)), always with reductions below  jnjnexp () cal () 10%, except for the operation with the flow of 17.77 R2 1 n1 (14) L d-1, when the reduction was approximately 16%. NN2 -1 1 This greater drop for the feed flow of 17.77 L d jnexp () jncal () may have been the effect of the detachment of cells N nn11that make up the biofilm, a result of increased shear force between fluid and biofilm. Marsili et al. (2008a) and Jain et al. (2012) observed reductions of RESULTS AND DISCUSSION 80% and 60%, respectively, and also delays in the regeneration of current, resulting from the replace- Extracellular Electron Transfer Mechanism ment of the culture medium of electrochemical cells inoculated with different Shewanella species. These Figure 2 (A) shows j vs t for 280 days of reactor microorganisms use mediators as the main mecha- operation, showing the days in which the operations nism of extracellular electron transport. were performed on a continuous regime. Figures 2 Bond and Lovley (2003) observed that the re- (B) and 2 (C) show j vs. t for the first 6 days of the placement of the medium did not affect the genera- experiment and during the seventh operation on a tion of electrical current of a MFC inoculated with G. continuous basis (9.66 L d-1), respectively. After the sulfurreducens. Upon replacement of the culture first two days of operation under batch regime, se- medium, the current was rapidly restored, indicating quential batch operation was started and an increase no influence of bacteria in the suspension or material in electricity generation was observed (Figure 2 (A)) solubilized in the medium, a behavior similar to that reaching a j value close to the maximum values ob- observed in this study. In daily renewals of the served before the fourth day of operation (between MFC’s culture medium, abrupt and substantial de- 0.30 and 0.35 A m-2). The electric current density creases were observed in current generation (Figure

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Modeling a Microbial Fuel Cell with Marine Sediment 217

2); however, this was quickly reestablished. These generation, increasing the j amplitude, for example, declines may be the result of exposure of the anode by two orders of magnitude at a scan rate of 1 mV s-1. electrodes to air during the renewal procedures of the The sigmoid-shaped CV revealed at the scan rate medium. In the presence of air, biomass can divert of 0.2 mV s-1 showed anodic current generation only the flow of electrons from the electrode to O2 seek- for values of the electric potential over the region ing to increase the rate of energy obtention in the close to -0.5 V. The positive current reflects acetate form of ATP (Heijnen, 1999). Moreover, the lack of oxidation and electron transfer to the electrode. For contact with the culture medium can deplete the lower electric potential values (> -0.5 V), the pres- available substrate within the biofilm. Sharma et al. ence of cathodic current is observed. Srikanth et al. (2014) suggest some guidelines related to the robust- (2008) and Richter et al. (2009) also observed this ness of the microbial population in the biofilm, such phenomenon and believe it to be the result of the as: it sustains a certain level of current density for an reduction reaction of some components present in extended period, the current level can be recuperated the medium, catalyzed by microorganisms which by replenishing the substrate or after a metabolic comprise the biofilm (Gregory et al., 2004). Above stress (e.g., different substrate concentration or oper- -0.5 V, the current rises continuously until reaching a ation mode of the reactor), the biofilm preserves the plateau around -0.3 V. electrochemical mechanisms, among others. The CV analyses performed with the reactor ef- fluent are presented in Figure 3 (A) and (B) and cor- roborate the hypothesis of the use of a predominantly direct EET mechanism. No peaks of anodic or ca- thodic current, characteristic of the presence of com- pounds capable of redox reaction (Bard and Faulk- ner, 2001), such as mediators (Marsili et al., 2008a), were observed at any scan rate (Figure 3 (A)), be- tween 0.2 and 10 mV s-1, or at different time inter- vals since the beginning of the continuous operation regime (Figure 3 (B)). These results are similar to those presented by Torres et al. (2008) in the study on the establishment of G. sulfurreducens biofilm on the electrode, in which the authors noted the absence of electroactive compounds suspended in the fuel cell based on the results of the CV analysis. Figure 3 (C) shows the results of the CV analyses performed on the MFC. One can observe differences in the j amplitude in the cycles obtained at different scan rates (0.2, 1, 2.5, 5, and 10 mV s-1), indicating slow process dynamics characteristic of microbial biofilms, as described by Harnisch and Freguia (2012). For scanning at 0.2 mV s-1, the conditions were within a time range sufficient to sustain micro- bial catalysis revealed by the sigmoidal profile of current generation versus the electric potential. Sig- moid-shaped voltammetry cycles were observed for all CV analyses. They are characteristic of microbial biofilms using direct EET mechanisms, such as bio- films of G. sulfurreducens or biofilms with domina- tion of G. sulfurreducens resulting from its competi- Figure 3: Cyclic voltammetry analyses for: (A) MFC tive advantage, as observed by many in the literature effluent with scan rate at 0.2, 1, 5, and 10 mV s-1; (B) (Marsili et al., 2008b, 2010; Torres et al., 2008; Sri- MFC effluent with scan rate at 1 mV s-1 for samples kanth et al., 2008, Richter et al., 2009; Sharma et al., collected at 0, 6, 12 and 18 hours after starting the 2014). From Figure 3 is evident that the biofilm at- continuous regime; (C) MFC with scan rate at 0.2, 1, tached to the electrode plays a major role in electricity 2.5, 5, and 10 mV s-1.

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218 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi

As a main role in an MFC, the external resistance and the experimental values exhibit a behavior with regulates anode availability as an electron acceptor moderate divergence. Between -0.5 and -0.3 V, the and affects the biofilm diversity. In fact, exoelectro- capacity of cells to generate electrons is in excess, genic microorganisms compete for substrate with but cells are limited by the availability of an extra- other functional groups (such as fermenters, aceto- cellular electron acceptor to transport it to the elec- gens, and methanogens) and the external resistance trode. Therefore, in this potential range, the anodic has a strong effect on inhibition and competition current is limited by the electrical resistance imposed among different microorganisms. As reported in by the EET mechanism (LaBelle and Bond, 2010). previous studies, exoelectrogenic bacteria have pref- As can be seen in Figure 6, the CR model showed a erential development under lower external load sys- better description of the experimental data when tems. However, for practical purposes and in large- compared to the SR model. The CR model fitting scale applications, mixed cultures are preferred over obtained an R² coefficient higher than 0.988 and the pure cultures. Exoelectrogenic biofilms formed by RMSE was less than 0.048 for all cases. These re- mixed cultures are more tolerant to environmental sults indicate that resistance of the EET mechanics changes and more accommodating to variable organ- affects the current generation and this was appro- ic matter (González del Campo et al., 2014). priately described as the electrical conductivity of Jung and Regan (2011) studied the effect of Rext the biofilm by the CR model. on biofilm communities in an MFC inoculated with anaerobic sludge from a wastewater treatment plant. (A) (B) (C) The authors observed that, at high Rext (9.8 kΩ), the anode bacterial communities were significantly changed, while operating at 0.97 kΩ and 0.15 kΩ had no significant effects. In addition, they demon- strated that electrogenesis and methanogenesis were affected by Rext. Rismani-Yazdi et al. (2011), also while studying the effect of Rext on biofilm communi- Figure 4: Scanning electron microscopy: (A) Image ties, observed that the biofilm from an MFC with of the surface of the electrode without biofilm; (B) lower external loads, 0.020 kΩ and 0.249 kΩ, had Image of the electrode surface covered by biofilm 75% more similarity than those with higher external and (C) magnification of the electrode surface loads, 0.48 kΩ and 1 kΩ (65% similarity). In the covered by biofilm. present study, considering the high external re- sistance (1 kΩ), a mixed biofilm could be expected. Anodic current showed an asymptotic behavior at The hypothesis of a predominantly direct mecha- electrical potentials above -0.3 V (Figure 6), which nism of electron transfer was confirmed by the anal- results from limiting the intracellular microbial reac- ysis with scanning electron microscopy shown in tions involved in the acetate oxidation process. Figure 4. Figure 4 (A) shows the surface of a graphite While the extracellular electron transfer can be ac- plate similar to the one used as electrode. In Figure 4 celerated by increasing the electromotive force (in- (B), there was a dense cluster of cells on the elec- crease in electrical potential of the anode), intracellu- trode surface and, in the detail in Figure 4 (C), the lar reactions exhibit a characteristic maximum rate, presence of the cell-like pili (nanowires) extending qmax (LaBelle and Bond, 2010). between bacteria and electrode structures. The cell morphology observed in this figure is similar to that observed by other researchers for exoelectrogenic biofilms (Richter et al., 2008; Pham et al., 2008; El- Nagar et al., 2010).

Estimation of Kinetic Parameters

Figure 5 illustrates the fit of the SR model with the set of experimental data of CV analysis for day 161 of the experiment. Similar results were obtained on the remaining days of analysis. In the region Figure 5: Model without resistance to electron trans- where the increase in the value of the electric current port (Equation (8) - SR Model) ( jcal ) fitted to the occurs, bounded by the dotted lines, the calculated experimental data ( jexp ).

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Figure 6: Cyclic voltammetry of the MFC performed at a scan rate of 0.2 mV s-1. Dotted lines represent experimental data and solid lines represent the adjusted CR model. (A) CV on day 161, 10 days after CON3; (B) CV on day 182, 12 days after CON4; (C) CV on day 195, 4 days after CON5; (D) CV on day 206, 15 days after CON5; (E) CV on day 220, 12 days after CON6; (F) CV on day 226, 18 days after CON6; (G) CV performed on day 256, 10 days after CON7; (H) CV on day 275, 7 days after CON8.

The estimated values of characteristic maximum bacter sulfurreducens and Thermincola ferriacetica -2 1 -2 current, jmax , showed an average value of 0.954 A m fed acetate (order of magnitude of 10 A m ) (Torres and standard deviation equal to 0.118 A m-2 (19.7% et al., 2008; Lee et al., 2009; Parameswaran et al., of the average value). The maintenance of the values 2013). of this parameter around a mean (low standard devia- The estimated values for EKA (Figure 7 (A)) tion) value characterizes the full development of the showed a standard deviation equal to 0.003 V, which biofilm on the electrode surface (Marsili et al., 2010; corresponds to less than 1% of the average value of Torres et al., 2008). The jmax parameter values were this parameter (-0.465 V vs Ag/AgCl, or -0.243 V vs lower than those obtained for pure cultures of Geo- EPH). The value of this parameter was also lower

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220 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi than that found for pure cultures of G. sulfurreducens estimated that the biofilm conductivity value into the fed acetate, -0.372 V vs Ag/AgCl (0.15 V vs EPH) MFC under evaluation has the order of magnitude of (Marsili et al., 2008b, 2010; Torres et al., 2008; Sri- 10-3 mS cm-1. This value is close to that estimated by -4 -1 kanth et al., 2008) and T. ferriacetica fed acetate, Sedaqatvand et al. (2013) (kbio = 8.76 10 mS cm ) -0.369 vs Ag/AgCl (Parameswaran et al., 2013). The using an extend version of the Marcus et al. (2007) microorganisms that have the lowest values of EKA model for a single-chamber MFC operating in batch may be favored in MFC in competition with other mode with daily replacements of wastewater and a cultures that have similar or higher electron transfer mixed microbial community. speeds, but require a higher-potential electron accep- Malvankar et al. (2011) stated that strains of G. tor (Bond, 2010). sulfurreducens that produced the highest densities of electric current had biofilms with the highest electri- The estimated values for the C (/)kLbio f pa- cal conductivity, demonstrating a relation between this rameter are shown in Figure 7 (B). Their values density and the network of nanowires produced by remained close to the average value of 4.746 S m-2 the bacteria. In the MFC of the present study, the for all analyses (standard deviation < 9%). Accord- electrical current densities were lower than those ob- ing to Torres et al. (2010), electric conductivity is a physical characteristic inherent to the composition of tained for pure cultures of G. sulfurredeucens, which the biofilm; thus, the value of C would change if the may indicate a smaller amount of nanowires in the biofilm’s thickness or composition varied between biofilm, expressed by the low value of estimated the measurements. kbio .

Figure 8: Expected kbio and Lf values obtained by fitting the mathematical model to the experimental data of the MFC (continuous line) compared to the values of these parameters available in the literature (dotted lines). The shaded region comprises the interval of values for each parameter.

Figure 7: (A) Values of E obtained by fitting the KA Malvankar et al. (2011) stated that strains of G. CR model to the CV experimental data for each cy- sulfurreducens that produced the highest densities of cle of eight analyses. (B) Values of the C parameter electric current had biofilms with the highest electri- estimated by fitting the CR model to experimental cal conductivity, demonstrating a relation between data from CV for each cycle of the eight analyses. this density and the network of nanowires produced by the bacteria. In the MFC of the present study, the Figure 8 compares the possible values of the pa- electrical current densities were lower than those rameters Lf and kbio found in this study to those obtained for pure cultures of G. sulfurredeucens, available in the literature (Table 1). The values which may indicate a smaller amount of nanowires reported for biofilm thickness are in a narrow range in the biofilm, expressed by the low value of esti- between 10 and 79 μm. However, for the parameter mated kbio . kbio , values of higher amplitude are shown, with According to Logan and Regan (2006), MFC bio- order of magnitude between 10-3 and 100 mS cm-1. films show that there is no single emergent microor- The shaded region in the graph highlights these ganism, but rather a portion of the community can be intervals. Considering that the biofilm thickness in sustained by alternative metabolisms such as fer- this study does not transcend the values reported in mentation, methanogenesis, and using an alternative the literature (order of magnitude of 101 μm), it was acceptor that does not result in current generation.

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Table 1: Thickness and electrical conductivity of biofilms illustrated in Figure 7 (ED = electron donor; EA = electron acceptor).

-1 Reference Biomass ED EA Lf (μm) kbio (mS cm ) G. sulfurreducens strain DL-1 acetate gold 50 0.45 Malvankar et al. (2012a) G. sulfurreducens strain KN400 acetate gold 40 4.61 G. sulfurreducens strain BEST acetate gold 60 1.09 Malvankar et al. (2012b) anaerobic biodigester sludge acetate gold 50.3 0.25 El-Nagar et al. (2010) S. oneidensis strain MR-1 lactate - - 1.0x10-3 Morita el al. (2011) cell aggregates (25% Geobacter) - - - 7.2x10-3 cell aggregates formed by G. ethanol fumarate - 1.4x10-3 Summers et al. (2010) sulfurreducens and G. metallireducens Marsili et al. (2008b) G. sulfurreducens PCA acetate glassy carbon 15 - Torres et al. (2008) G. sulfurreducens acetate graphite 79 - Lee et al. (2009) G. sulfurreducens acetate graphite 66 - acetate graphite 27 - methanoate graphite 22 - lactate graphite 16 - Sppears et al. (2012) G. sulfurreducens strain PCA H2 graphite 10 - acetate+ methanoate graphite 27 - lactate+ acetate graphite 19 - a Bacteria grown with EA (oxygen) limitation. The conductivity value refers only to the nanowire produced by bacteria. b Cell aggregates obtained in the UASB reactor that converted brewery effluent into methane.

These presences may have led to the difference in ceptor that does not result in current generation. the behavior of current generation kinetics of the These presences may have led to the difference in MFC in this study in relation to the values obtained the behavior of current generation kinetics of the for pure cultures. In addition, as previously dis- MFC in this study in relation to the values obtained cussed, the metabolisms present in anode biofilms for pure cultures. In addition, as previously dis- are also influenced by external resistance. An MFC cussed, the metabolisms present in anode biofilms operating at 1 kΩ and with a microbial consortium are also influenced by external resistance. An MFC has a quite different portion of dominant exoelectro- operating at 1 kΩ and with a microbial consortium genic microorganism and behavior compared to a has a quite different portion of dominant exoelectro- pure culture or an MFC operated with very low re- genic microorganism and behavior compared to a sistances, as found by Rismani-Yazdi et al. (2011). In pure culture or an MFC operated with very low re- fact, the characteristic kinetic parameters ( jmax , sistances, as found by Rismani-Yazdi et al. (2011). In fact, the characteristic kinetic parameters ( j , EKA , and kbio ) are characteristics of both exoelec- max trogenic biofilm and external resistance. EKA , and kbio ) are characteristics of both exoelec- Malvankar et al. (2011) stated that strains of G. trogenic biofilm and external resistance. sulfurreducens that produced the highest densities of electric current had biofilms with the highest electri- cal conductivity, demonstrating a relation between CONCLUSION this density and the network of nanowires produced by the bacteria. In the MFC of the present study, the According to the results obtained in this study, it electrical current densities were lower than those was found that the exoelectrogenic microbiota pre- obtained for pure cultures of G. sulfurredeucens, sent in the marine sediment collected on the southern which may indicate a smaller amount of nanowires coast of Brazil predominantly uses a direct mecha- in the biofilm, expressed by the low value of esti- nism of extracellular electron transfer. Multiple evi- mated kbio . dence points toward EET through a solid conductive According to Logan and Regan (2006), MFC bio- matrix including: cyclic voltammetry results, the films show that there is no single emergent microor- presence of nanowires observed in scanning electron ganism, but rather a portion of the community can be microscopy images, and the good fit of the mathe- sustained by alternative metabolisms such as fermen- matical model to experimental data. tation, methanogenesis, and using an alternative ac- The mathematical model properly described the

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222 J. T. Teleken, J. de Sá Silva, M. F. Fraga, C. S. Ogrodowski, F. B. Santana and B. A. M. Carciofi electrical current results obtained from the cyclic n Counter of the experimental data, (-) voltammetry analysis and provided parameter values N Total number of experimental data points, with physical meaning, which allowed comparing (-) the kinetics parameters of this MFC with other stud- qmax Maximum specific rate of electron donor ies. In addition, the model’s results indicate that bio- consumption, (g g-1 s-1) film conductivity plays an important role in the elec- Rext External resistance, (Ω) tric current generation in the MFC. The identification R Universal gas constant, (J mol-1K-1) of new fonts of exoelectrogenic microorganisms, R2 Coefficient of determination, (-) such as marine sediment collected on the southern RMSE Root mean square error, (A m-2) coast of Brazil, opens new doors for research involv- S Mass concentration of electron donor at a ing biological energy generation. ED given spatial position of the biofilm,

(g m-3)

t Time, (s) ACKNOWLEDGEMENTS T Temperature, (K)

V EE , (V) The authors gratefully acknowledge financial anode anode KA support and fellowships from CEEE – Companhia Vcell Voltage between the anode and cathode, Estadual de Energia Elétrica – RS/Brazil, CNPq – (V) Conselho Nacional de Desenvolvimento Científico e z Spatial coordinate, (m) Tecnológico – Brazil, and CAPES – Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Greek Letters Brazil. -3  f Specific biofilm mass, (g m )  EEbio KA , (V) NOMENCLATURE   EE , (V) anode KA Latin Letters  s Total number of moles of electrons that can be oxidized per gram of electron donor, -1 A Anode surface area, (m2) (mol g ) Anode  C Ratio between biofilm conductivity and Dimensionless spatial coordinate ( zL/ f ), thickness, (S m-2) (-) Eanode Anode electric potential, (V)

Ebio Biofilm electric potential at a given spatial position, (V) REFERENCES

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