Effect of type of inoculum on microbial fuel cell performance that used RuxMoySez as cathodic catalyst

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y 4 0 ( 2 0 1 5 ) 1 7 4 0 2 e1 7 4 1 2

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Effect of type of inoculum on microbial fuel cell performance that used RuxMoySez as cathodic catalyst
zquez-Larios a, H
ector Mario Poggi-Varaldo a,*, Ana Line Va Omar Solorza-Feria b, Noemı´ Rinderknecht-Seijas c a

Environmental Biotechnology and Renewable Energies Group, Dept. Biotechnology and Bioengineering, CINVESTAV del IPN, P.O. Box 14-740, Mexico City (D.F.), 07000, Mexico b Dept. of Chemistry, CINVESTAV del IPN, P.O.Box 14-740, Mexico City (D.F.), 07000, Mexico c Division of Basic Sciences, ESIQIE-IPN, Bldg. 6, Campus Zacatenco, Mexico City, Mexico

article info

abstract

Article history:

This research aimed at evaluating the effect of inoculum type and the application of Rux-

Received 9 February 2015

MoySez as a cathode catalyst on the treatment and bioelectricity production of a microbial

Received in revised form

fuel cell (MFC) fed with a municipal leachate. The inocula assayed were a plain sulphate-

27 September 2015

reducing inoculum (In-SR), an enrichment in Mn(IV)-reducing bacteria (In-EMn(IV)), and

Accepted 30 September 2015

two enrichments in Fe(III)-reducing bacteria, namely, In-EFe(III)-S and In-EFe(III)-SR.

Available online 24 October 2015

In the batch experiments where the cells were operated with the faces connected in parallel and loaded with an external resistance of 100 U, enriched inocula had a significant,

Keywords:

positive effect of cell performance. The average volumetric powers PV-ave observed ranged

Cathodic catalyst

from 2146 (In-SR) to 13 304 mW/m3 (In-EFe(III)-S). The highest value of PV-ave achieved in our

Enriched inocula

work was about 30% of that of commercial anaerobic digestion of wastes. Application of

Leachate

inocula enriched in Fe(III) and Mn (IV)-reducing bacteria significantly improved the per-

Microbial fuel cell

formance of cells that used RuxMoySez as a cathodic catalyst for the oxygen reduction

RuxMoySez

reaction. Copyright © 2015, Hydrogen Energy Publications, LLC. Published by Elsevier Ltd. All rights reserved.

Introduction A microbial fuel cell (MFC) is an electro-biochemical reactor capable of directly converting organic matter into electricity [1e3]. Platinum has been commonly used as a catalyst of the oxygen reduction reaction (ORR) in MFCs. Yet, the high cost of

a MFC is mainly due to the high price of this noble metal. This, in turn, could deter the commercial MFC applications. So, the development of materials with high catalytic properties to perform oxygen reduction is presently a task of great importance [4e7]. One of the challenges in MFC research consists of the application of electrochemically active catalytic materials (such as RuxMoySez [8]) as alternative electrocatalysts to


n y de Estudios Avanzados del IPN, Depto. Biotecnologı´a y Bioingenierı´a Environmental * Corresponding author. Centro de Investigacio
xico City, D.F., Mexico. Tel.: þ5255 5747 3800x4324; Biotechnology and Renewable Energy R&D Group, Apdo. Postal 14-740, 07000, Me fax: þ5255 5747 3313. E-mail address: [email protected] (H.M. Poggi-Varaldo). http://dx.doi.org/10.1016/j.ijhydene.2015.09.143 0360-3199/Copyright © 2015, Hydrogen Energy Publications, LLC. Published by Elsevier Ltd. All rights reserved.

i n t e r n a t i o n a l j o u r n a l o f h y d r o g e n e n e r g y 4 0 ( 2 0 1 5 ) 1 7 4 0 2 e1 7 4 1 2

replace the extensive use of the more expensive platinum. Vazquez-Larios et al. [8] evaluated the application of bimetallic chalcogenide RuxMoySez, as an ORR catalyst and two anodic materials on the performance of two MFCs fed with synthetic substrate. The power delivered by the cells equipped with fitted graphite triangular pieces and chalcogenide catalyst was 43% inferior to those of a similar cells with Pt although the cost of the first catalyst was significantly lower than that of Pt., i.e., 73% lower. On the other hand, municipal leachate is an aggressive effluent with relatively high concentration of organic matter [9,10]. Leachate from sanitary landfills is of concern in Mexico City, since very recently its “Bordo Poniente” mega landfill has been closed and is known to generate large amounts of both fresh and aged leachates. The metropolitan area of Mexico City (the capital city plus neighbouring counties) has a population of nearly 22 million people. In the recent past, the municipal wastes were disposed of in the “Bordo Poniente” sanitary landfill mentioned above. This landfill has been emplaced in a site that was part of the desiccated bottoms of the former Texcoco lake near Mexico City characterized by its saline-sodic soils. The landfill has been in operation for nearly 25 years, it has a surface area of 300 ha and has received an average of 12 000 metric tons per day of wastes in the last years of operation. A total of 70 million metric tons of municipal wastes were buried there. The landfill was closed in 2011. After closure, the landfill still generates significant amounts of leachates with moderate-to-high organic matter concentration (http://www.excelsior.com.mx/comunidad/ 2013/03/05/887324). The site of the former landfill can become an environmental liability because of the generation of leachates that infiltrate into the ground thus contaminating the underlying aquifer [11]. So far, the available information on treatment of actual municipal leachate in MFC loaded with enriched inocula, particularly enriched in Mn (IV)-reducing bacteria, is still scarce. Previous works have demonstrated the feasibility of using leachate as substrate in MFCs. Yet, the powers delivered were low-to-moderate. Greenman et al. [12] demonstrated that it was possible to generate electricity and simultaneously treat landfill leachate in MFC columns, they observed a density power of 1.35 mW/m2 and 43%
lvez et al. [13] biochemical oxygen demand (BOD) removal. Ga operated three MFCs hydraulically connected in series for simultaneous leachate treatment and electricity generation. The system, when was configured into a loop, could remove 79% of COD and 82% of BOD5 after 4 days of operation. Ganesh & Jambeck [14] worked with a cylindrical single aircathode without inoculation to treat landfill leachate; they observed a volumetric power (PV) of 699 mW/m3 and 74% COD removal. Tugtas et al. [15] investigated treatment of anaerobically pre-trated landfill leachate in batch and continuous-flow two-chambered MFCs. They reported a PV of 2482 mW/m3 and 90% COD removal. On the other hand, Puig et al. [16] evaluated an air-cathode MFC fed with landfill leachate, the device achieved a PV of 344 mW/m3 whereas the COD removal was 70%. It can be seen that, in general, volumetric powers obtained in MFC fed with leachate were in the low-to-mid part of the power range reported in the open literature for MFCs.

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Therefore, this research aimed at evaluating the effect of inoculum type on the treatment and bioelectricity production of a MFC that used RuxMoySez as a cathode catalyst. The cell was fed with an actual municipal leachate.

Materials and methods Microbial fuel cell architecture The MFC-G consisted of a horizontal cylinder built Plexiglass 90 mm long and 57 mm internal diameter. The opposing faces of the cylindrical shell were fitted with corresponding sets of an assemblage of (inside to outside) proton exchange membrane (Nafion 117), a Toray flexible carbon-cloth containing 1 mg/cm2 RuxMoySez (20wt%/C) and a perforated plate of stainless steel 1 mm thickness. Each assemblage was corresponded with anodes made of granular graphite and a graphite rod as collector (80 mm long and 5 mm diameter). The average separation between cathode-anode in MFC-G was 17.5 mm. The anode chamber volume was 100 mL. All the cathodes in cell were in direct contact with atmospheric air on the perforate metallic plate side. When the cathodic biocatalyst was the chalcogenide compound, the cathode contained 1 mg/cm2 RuxMoySez 20 wt% of 1.0 mg/cm2 RuxMoySez 20 wt% dispersed in Vulcan carbon XC-72 as it was mentioned above. The catalytic ink was prepared by mixing 11.1 mL/cm2 Nafion® 5 wt% and 333.3 mL/cm2 of ethanol and the resulting suspension was sprayed onto the proton exchange membrane (PEM) of a home fabricated electronic semiautomatic device. Afterwards, the PEM was set by hot pressing (4.4 kgf/cm2) at 120  C for 3 min to improve adherence of catalyst to the membrane [17,18].

Catalyst synthesis The RuxMoySez catalyst was synthesized by decarbonylation of transition-metal carbonyl compounds in organic solvent, under refluxing [19,20]. The RuxMoySez catalyst was synthesized by reacting 0.07 mM Ru3(CO)12 (Aldrich) with 0.20 mM Mo(CO)6 (Strem) and 0.20 mM of elemental selenium (Strem) in a chemical reactor containing 150 mL of 1,6-hexanediol for 3 h at 230  C. The un-reacted precursors and the organic reaction medium were eliminated by several washes using organic solvents, and dried overnight at room temperature [21].

Physical characterization of the chalcogenide catalyst The chemical formula of the catalyst was Ru6Mo1Se3. The texture of the catalyst consisted of nanocrystalline particles forming uniform agglomerates and embedded in an amorphous phase. Tafel slopes for the ORR did not significantly change with temperature at 0.116 V dec1 whereas there was an increase of the charge transfer coefficient in da/ dT ¼ 1.6  103. The latter was probably related to an entropy turnover contribution to the electrocatalytic reaction. Further characterization showed that the catalyst produced less than 2.5% H2O2 during oxygen reduction; the apparent activation energy was 45.6 ± 0.5 kJmol1 [20,21].

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Municipal leachates The cells were loaded with 20 mL of municipal leachates sampled from the Mexico City landfill “Bordo Poniente” stage 4. The characterization of the leachate is exhibited in Table 1. The relatively high organic matter contents in terms of both biochemical oxygen demand (BOD5) and chemical oxygen demand (COD), as well as the high value of BOD5/COD ratio indicated that the leachate is biodegradable, and likely not very aged [9]. Interestingly, we expected a lower pH consistent with fresh leachate [10]. That was not the case. It is known that the landfill is emplaced in a site whose soil is sodic-saline with pH of soil extract as high as 11 [10,22,23]. The local soil was likely used to cap the landfill cells during the daily operation of the landfill, possibly releasing sodium salts (carbonate, bicarbonate) as well as hydroxides that increased leachate pH. This explanation is supported by the high values of the electrolytic conductivity of the leachate (Table 1).

Sample collection, sulphate-reducing inoculum, and enrichment of inocula The inoculum enrichments were obtained by three serial transfers of the corresponding cultures, as described below. Samples from soil were collected in the CINVESTAV-IPN gardens to a depth 0.3 m; afterwards they were transferred to anaerobic bottles. The soil samples were transported to the laboratory without oxygen contact. A 5 g of soil sample was suspended in 50 mL of anaerobic saline solution. In turn, 5 mL of sample was transferred to 50 mL metal-reduction medium with acetate, Mn (IV) or Fe (III). Duplicate enrichments were incubated at 30  C for 15 d or 9 d for Mn (IV) and Fe (III), respectively, in the dark condition. The enrichment procedure was repeated 3 times (see Table 2). Metal-reduction medium consisted of (g/L): 2.5 NaHCO3, 0.25 NH4Cl, 0.6 NaH2PO4$H2O, 0.1 KCl, 10 mL vitamin solution and 10 mL mineral solution (Lovley & Phillips, [22]). The MnO2 was synthesized by slowly adding a solution of MnCl2 (30 mM) to basic solution of KMnO4 (20 mM) which was stirred with a magnetic stir bar. This procedure is similar to the technique described by Lovley & Phillips [24]. The Fe(III) oxide was synthesized as follows: a solution 0.4 M of FeCl3$6H2O (pH adjusted to 7.0 with 10 M of NaOH) was added, according to the technique described elsewhere [24]. The MnO2 was synthesized by slowly adding a solution of MnCl2 (30 mM) to basic solution of KMnO4 (20 mM) which was stirred with a magnetic stir bar. This procedure is similar to a previously described technique [24].

Table 1 e Characteristics of municipal leachate. Parameters pH Conductivity (mS/cm) Total Kjeldahl nitrogen (g/L) SO4 2 (g/L) COD (g/L) BOD5 (g/L) BOD5/COD

Value 8.26 36.7 2.9 0.281 12.3 10.6 0.86

± 0.02 ± 0.1 ± 0.03 ± 0.01 ± 0.5 ± 0.2

One MFC was inoculated with a sulphate-reducing (In-SR) inoculum sampled from a sulphate-reductor complete mix reactor. The biomass concentration in the inoculum was ca. 2000 mg VSS/L, where VSS stands for volatile suspended solids. The reactor had a working volume of 2.5 L, was operated at 37  C in a constant temperature room, and mixed with a magnetic stirrer. The wastewater was fed to the seed bioreactor at a flow rate of 120 mL/d. Its composition was (in g/ L): sucrose (5.0), Acetic acid (1.5), NaHCO3 (3.0), K2HPO4 (0.6), Na2CO3 (3.0), NH4Cl (0.6). The feed wastewater was supplemented with a convenient concentration of sodium sulphate estimated as the stoichiometric concentration of sulphate salt required to consume the chemical oxygen demand equivalent of sucrose and acetic acid (with a 15% excess to ensure predominance of sulphate-reduction conditions over methanogenesis) (see Table 3).

Electrochemical characterization of the microbial fuel cells Potential sweep experiments were carried out from opencircuit cell voltage (EMFC-OCP), to the final potential of 0.02 V at a scan rate of 1 mV/s, performed in a potentiostat/galvanostat Voltalab model PGZ402 [25,26]. Values of Rint were estimated from the slopes of corresponding regression lines selected in the linear range of the polarization curves. The current (IMFC), power (PMFC) and volumetric power (PV) were calculated as previously described [27]. The power density (surface area) was normalized to the projected cathode surface area (surface power density PS). The cells were loaded with 80 mL of inocula (In-EFe(III)-S, InEFe(III)-SR, In-EMn(IV) or In-SR) and 20 mL of actual municipal leachate. The initial biomass concentration in the cell inocula was ca. 1000 mg VSS/L.

Batch operation of the microbial fuel cells The batch MFCs were loaded with municipal leachate and either inoculum enriched in Mn(IV)-reducing bacteria, or inoculum enriched in Fe (III)-reducing bacteria, or sulphate reducing seed. A control without inoculum was also run. The organic matter concentration of the influent in MFCs was ca. 2.4 g COD/L. The cells were loaded with 80 mL of enriched in Mn(IV)-reducing bacteria; the initial biomass concentration in the cell inoculum was ca. 1000 mg VSS/L. The cells were operated for two Periods; in Period I the cells were run until a decrease organic matter concentration was observed. At the end of Period I, the cell was loaded with municipal leachate (ca. 2.4 g COD/L) although the electrodes and membrane as well as the microbial community remained the same, and further operated for what we denominated Period II. At the start of Period I the cells were operated for 24 h at open circuit voltage. Afterwards, each cell was connected to its external resistance and were batch-operated for a total 300 h, at ambient temperature (23  C average) without mixing. The circuit of each MFC was fitted with a corresponding external resistance of 100 U. The main variable responses of this experiment were the average volumetric power (PV-ave), the efficiency of organic matter removal (hCOD), and the coulombic efficiency (hCoul).

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operation were calculated by numerical integration versus time using the trapezoidal rule [32,33]. The hCoul is the ratio between the actual amount of produced electrons (CRS) to the electrons that could be produced from the substrate if all the substrate were channeled into electricity (CTS), as follows:

Table 2 e Characteristics of microbial fuel cells with different inocula and different connections of their two faces (electrodes). Type inocula

Type connection

In-EFe(III)-S

In-EFe(III)-SR

In-EMn(IV)-S

In-SR

RuxMoySez EMFC,OCP (V) PV-max (mW/m3) Rint (U)

Face I Face II Seriesa Parallelb Face I Face II Series Parallel Face I Face II Series Parallel Face I Face II Series Parallel

0.542 0.578 0.672 0.549 0.612 0.635 0.699 0.592 0.618 0.555 0.665 0.557 0.620 0.648 0.745 0.632

10 615 12 018 10 377 14 521 9713 12 636 12 778 15 825 9001 11 320 10 685 16 359 4622 8219 6842 9293

22 45 18 22 18 13 31 11 21 23 36 11 23 18 38 16

hCoul ð%Þ ¼

CRS $100 CTS

(3)

Zt CRS ¼

IMFC dt

(4)

0

CTS ¼

  Fi $bCOD $ CODi  CODf $VMFC MCOD

(5)

where F: Faraday's constant (96 485 Coulombs/mol e), bCOD: number of moles of electrons harvested from the COD (4 mol e per mol of COD), CODi: initial COD (g/L), CODf: final COD (g/ L), VMFC: MFC operation volume (L), MCOD: COD's molecular weight (32 g/mol). The calculation of CRS was performed by numerical methods. Since the current intensity time course is a polygonal plot versus time, the trapezoidal rule for numerical integration was used [32,33].

Notes: EMFC-OCP, open circuit potential; PV-max, maximum volumetric power; Rint, internal resistance. a The two electrode assemblies were connected in series. b The two electrode assemblies were connected in parallel.

Analytical methods and calculations

Results and discussion

The COD and VSS of the liquors of the sulphate-reducing seed bioreactor and cell liquors were determined according to the Standard Methods [28]. Manganese (Mn II) contents were analysed by the method of Brewer & Spencer [29] as modified by Armstrong et al. [30] whereas the presence of Mn (IV) was assessed with a benzidine acetate reagent [31]. The hCOD was calculated as hCOD ð%Þ ¼

ðCODi  CODf Þ $100 CODi

Electrochemical characterization of microbial fuel cells The first set of experiments consisted of the evaluation of the effect of the type of inoculum (In-EFe(III)-S, In-EFe(III)-SR, In-EMn(IV) and In-SR) on the electrochemical characteristics of the MFC-G. Each face of the MFC-G was characterized by separate (I and II), in series, and in parallel electric arrangements. Parallel connection of faces increased the maximum volumetric power PV-max up to 14 521, 15 825, 16 359 and 9293 mW/m3 (with In-EFe(III)-S, In-EFe(III)-SR, In-EMn(IV) and In-SR, respectively) (Fig. 1 and Table 2), compared with series connection where PV-max of 10 377, 12 778, 10 685 and 6842 mW/m3 (inocula in the same order as above). Parallel connection significantly decreased the Rint of the cells and almost doubled volumetric power. The PV-max for the MFC-G (In-EFe(III)-S, In-EFe(III)-SR, In-EMn(IV) and In-SR) when faces were

(1)

where CODi initial chemical oxygen demand and CODf final chemical oxygen demand. The volumetric power was estimated with Eq. (2) below PV ¼

E2MFC VMFC $Rext

(2)

where EMFC is the voltage, Rext is the external resistance, and VMFC is the cell volume. The average values during the batch

Table 3 e Average performance of microbial fuel cells during batch operation. Parameter

In-EFe(III)-S Period I

EMFC-ave(V) PV-ave (mW/m3) PS-ave (mW/m2) ICCM-ave (mA) hCOD (%) hCoul (%)

0.347 13 304 333 3.54 71 62

± 0.107 ± 4755 ± 119 ± 0.86

In-EFe(III)-SR

Period II 0.370 13 746 344 3.71 71 78

± 0.010 ± 715 ± 14 ± 0.10

Period I 0.317 10 783 270 3.16 52 77

± 0.087 ± 4752 ± 118 ± 0.86

In-EMn(IV)

Period II 0.377 11 636 291 3.37 63 80

± 0.037 ± 2125 ± 53 ± 0.37

Period I 0.313 9926 248 3.13 76 51

± 0.038 ± 2308 ± 58 ± 0.39

In-SR

Period II 0.250 ± 6699 ± 167 ± 2.50 ± 76 48

0.055 2842 71 0.55

Period I 0.136 ± 0.055 2146 ± 1666 54 ± 42 1.36 ± 0.55 68 24

Period II 0.183 3402 85 1.83 68 36

± 0.031 ± 1079 ± 27 ± 0.31

Notes: EMFC-ave, Average cell voltage; PV-ave: Average volumetric power; PS-ave: Average power density; IMFC-ave: Average cell current intensity; hCOD: Chemical oxygen demand removal; hCoul: Columbic efficiency. Standard deviations reported in the Table correspond to variation with time of each parameter.

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Fig. 1 e Schematic diagram a microbial fuel cell (material electrode granular graphite).

connected in series and parallel were higher than those reported in the literature [16,34,35]. Our PV-max was superior to that reported by Ortega-Martinez et al. [34] for the characterization of a novel, multi-face parallelepiped MFC-P (Pt for ORR); this cell was equipped with a ‘sandwich’ cathode-membraneanode assemblage in five of their faces. When the 5 faces of the MFC-P were connected in series and parallel, the PV-max achieved values were 62 and 570 mW/m3, respectively. On the other hand, Puig et al. [16] also characterized an air-cathode MFC loaded with landfill leachate and estimated a PV-max of 278.2 mW/m3. Ieropoulos et al. [35] compared the performance of two small size MFCs connected in parallel using acetate as the substrate and a seed that consisted of anaerobic sludge; the characterization studies gave a PV-max of 860 mW/m3. The relatively higher PV-max in our MFCs could be attributed to the increase of the total electrode surface area by the application of granular graphite, and this, in turn, could have improved the electron transfer microbe-to-anode process [8]. Also, our work demonstrated that parallel connection of cell faces was more appropriate. Furthermore, the use of enriched inoculum seemed to be related to the highest power values in our work. It is known that enrichment procedures as those used in our work lead to the enrichment in dissimilatory metal reducing bacteria that are capable of the reduction of soil metal oxides such as MnO2, FeOOH and very often exhibit exoelectrogenic (electrochemical activity) properties [36e38]. This, in turn, is related to improved electron transfer to anode and improved cell characteristics and performance [36,37].

Batch operation of microbial fuel cells loaded with actual leachate and enriched inoculum Fig. 2 shows the time course of cell potential (MFC-G; either inocula In-EFe(III)-S, In-EFe(III)-SR, In-EMn(IV), In-SR or without inoculum) when the two faces were connected in parallel. The batch runs lasted for ca. 300 h. The MFC were connected to an

external resistance (Rext) of 100 U. The grey area in Fig. 2 shows the maximum, open circuit potential (ECCM-OCP) (the first 24 h). Two periods or cycles of electricity generation with 2.4 g/L municipal leachate were carried out (Period I and Period II in Fig. 3 and Table 3). It was apparent that the MFC loaded with In-SR improved its performance in Period II, suggesting an incell enrichment of the biocatalysts. At least four main techniques of inoculum enrichment for MFC that typically lead to the selection for electrochemically active bacteria (EAB) in microbial cultures are distinguished: (i) chemical enrichment outside the MFC, using chemical electron acceptors ([39e44]; (ii) enrichment in the MFC, or in-cell methods [38,45,46]; (iii) enrichment in microbial electrolysis cell (MEC) or potentialpoised MFC ([37,47]; and (iv) hybrid methods, that usually combine two or more of the above or miscellaneous techniques [37,48]. In-cell enrichment techniques are based on the fact that MFC operating parameters can have a significant effect on cell performance as well as on the enrichment of exoelectrogenic organisms and the ability to achieve high rates of electricity production. Thus, the operation of the MFC can become a selective pressure by itself that leads to the development of cultures enriched in EABs [38,45,46,49e52]. As mentioned before, it seems that the effect of in-cell enrichment was more significant for the MFC seeded with In-SR than that of the cells seeded with previously enriched inocula (Fig. 3). Likely, the inocula In-EFe(III) soil and In-EFe(III) SR were already enriched in EAB by the chemical method. On the other hand, the In-SR was probable poorer in EAB ab initio, so the in-cell enrichment could have played a more pronounced positive effect. The PV-ave obtained in the cells for the different inocula (InEFe(III)-S, In-EFe(III)-SR, In-EMn(IV), In-SR and without inoculum) were 13 304, 10 783, 9926, 2146 and 53 mW/m3. The highest average PV in our cells was higher than that reported by Puig et al. [16] and Vazquez-Larios et al. [27]. Puig et al. [16] treated a landfill leachate in an air-single MFC fitted with Pt catalyst, for

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a

15000

0.4

12000 9000

Face I

0.3

6000

Face II

EMFC-G (V)

0.6

Parallel

Series

0.5

0.2

b

Parallel

Series

15000 12000

0.5

Face II

0.4

9000 Face I

0.3

6000

0.2

0

0

0

2

4

6

10 12 14 16 18 20 IMFC-G (mA)

0

15000

0.3

9000

Face I

6000

EMFC-G (V)

Face II

PV (mW/m3)

12000

0.4

15 20 IMFC-G (mA)

25

30 12000

Parallel

d 9000

0.6

Series

0.5

10

0.7

Parallel

0.6

5

0.8

18000

c

0.7

0

0

8

0.8

3000

0.1

Series

0.5

Face II

0.4

6000

0.3

Face I

0.2

0.2 3000

0.1 0

5

10

15 20 IMFC-G (mA)

25

3000

0.1 0

0

0

PV (mW/m3)

3000

0.1

EMFC-G (V)

18000

0.7

PV (mW/m3)

0.6 EMFC-G (V)

0.8

18000

0.7

PV (mW/m3)

0.8

0 0

30

5

10 IMFC-G (mA)

15

20

Fig. 2 e Polarization curves by linear sweep potential studies in electrochemical characterization of microbial fuel cells, (a) inoculum enriched in Fe (III)-reducing bacteria (soil origin) In-EFe(III)-S, (b)) inoculum enriched in Fe (III)-reducing bacteria (sulphate reducing origin) In-EFe(III)-SR, (c) inoculum enriched in Mn (IV)-reducing bacteria In-EMn(IV), and (d) sulphate reducing inoculum In-SR. Keys: convex curves stand for volumetric power, read on the right axis; descending parabolic curves represent the E-I relationship, read on the left axis; curve in blue-hyphen stand for parallel connection of the two faces of the cell; red-dot stands for series connection of the faces; continuous grey corresponds to face II alone, and continuous black stands for face I alone.

treatment in the MFCs. At least, four differences due to pH conditioning (lowering pH) of the leachate that could have effects on MFC characteristics and performance can be listed: (i) change of the ORR in the cathode: It has been reported that the cathodic semireaction in MFCs operated with neutral or alkaline wastewaters exhibit an ORR of the type [53].

2 þH2 O

12O

=

þ 2e /2OH

Eo0 ¼ þ0:820 V

(6)

At lower pHs, the more known ORR with protons takes place in the cathode of the MFCs [54]; the Eo value þ 1.229 V was corrected for the ratio Q at pH ¼ 7, i.e., þ 2 þ2H

12O

=

two periods. Indeed, in their Period I the organic matter content of the influent was 0.507 g COD/L and they registered a very low PV-ave of only 6.1 mW/m3. In Period II they increased the organic matter concentration up to 8.51 g COD/L and they found a PV-ave of 220 mW/m3 that fluctuated in the range
zquez-Larios et al. [27] 106e344 mW/m3. On the other hand, Va operated a two-face MFC whose main features were the assemblage or sandwich’ arrangement of the anode-PEMcathode; during the batch operation of the cells loaded with a model extract typical of leachate from the hydrogenogenic fermentation of organic solid wastes and a sulphate-reducing inoculum, a PV-ave of 479 mW/m3 was observed. That is, the power value was low to moderate. It seems that the treatment of leachates from the dark fermentation of wastes for biohydrogen generation, would also be feasible using MFCs and enriched inocula because the organic matter profile of landfill leachates and those from dark fermentation of wastes are similar. Indeed, both types of leachates contain organic acids as the main contributors to their organic matter contents [2,3]. Our Group has published a few successful experiments on treatment of dark fermentation leachates or extracts from biohydrogen production, using MFCs [1,8,27,34,36]. Another issue that is worth discussing is the possible conditioning of leachate by lowering its pH prior to its

þ 2e/H2 O Eo0 ¼ þ1:022 V

 .  2  ½O2  Hþ Eo0 ¼ Eo  ð0:05915=2Þ log ½H2 O ¼ Eo  0:05915pH ¼ 0:815 V

(7)

(8)

since water and oxygen concentration activities are equal to 1, and pH ¼ 7 Irrespective of the organic matter oxidation at the anode, it is customary to consider the oxidation of the reduced nicotinamide adenine dinucleotide (NADH) at the anode as the

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Fig. 3 e Time course of voltage outputs of the microbial fuel cell using an inoculum enriched in Fe (III)-reducing bacteria (either one soil origin, In-EFe(III)-S and sulphate-reducing origin, In-EFe(III)-SR), inoculum enriched in Mn (IV)-reducing bacteria (In-EMn(IV)), inoculum sulphate reducing (In-SR), and without inoculum.

representative semi-reaction in the anodic chamber (NADH is the typically the last microbial electron acceptor, and involved in the electron transfer to the anode; [53,55,56], i.e. NADþ þHþ þ2e /NADH Eo0 ¼ 0:320 V

(9)

o0

So, the overall theoretical E of the MFCs will be

(0.86  (0.320)) V ¼ 1.18 V, and

(0.815  (0.320)) V ¼ 1.135 V at neutral-to-alkaline and acidic conditions of the cell anolytes, respectively. In principle, both theoretical potentials are very close, the difference is less than 5%. One might speculate that this difference is negligible compared to the decreases on actual potentials due to irreversibilities of several kinds (total losses of 30e50% with respect to the thermodynamic potentials [53]. (ii) possible development of more significant pH gradients at pH 7 or lower, whereas the pH gradients when the MFC is operated at the original (alkaline) pH of the leachate would be mitigated, likely due to presence of carbonates, bicarbonates, and hydroxyl anions. A large pH gradient could inhibit the function of biocatalysts and decrease voltage efficiency in MFCs [57]. In a research work, it was shown that the use of carbonate species as OH carriers from the cathode to the anode compartment lead to a significant potential increase (ca. 120 mV) along with a decrease of two pH units in the pH gradient between the anodic and cathodic chambers of the MFC [57]. (iii) decrease of the conductivity of leachate at pH 7 or lower: basic chemistry concepts indicate that several anions

such as bicarbonate, hydroxyl, etc., will have reduced concentrations at pH 7 compared to alkaline conditions (by chemical neutralization with protons to form either CO2, H2O, etc.). Moreover, organic acid species typically present in the leachates such acetatic, propionic, butyric acids, at lower pH will shift to their unionized forms rather to the anion forms at higher pH (for instance, unionized acetic acid versus acetate, and so on, the chemical speciation determined by the pH and the pKa of the acid). The patterns discussed above, in turn, could lead to a decrease of the electrolytic conductivity of the leachate. On the other hand, it has been reported positive effects on potentials of MFC (and lowering internal resistances of MFCs) when the liquor or medium in the cell has high conductivitIes. One issue is that higher electrical conductivities could lower the ohmic resistance of the MFCs, lowering the overall internal resistance [2]. So, liquors with decreased electrolytic conductivities are expected to be related to higher internal resistances and poorer potentials and delivered powers [58]. (iv) different behaviour of the Nafion membrane at different pHs: our MFCs were equipped with Nafion separators. Nafion membranes are known to be proton exchange membranes and poorer exchangers of other cations or anions [53]. So, at slightly alkaline and alkaline pHs, selected cation and preferably anion exchange membranes are expected to perform better than Nafion membranes. Indeed, previous research has shown that the high cost, highly-selective Nafion proton exchange membrane for hydrogen fuel cells is not ideal for MFCs treating wastewater, because at neutral pHs cations are moving from the anode to the cathode rather than protons; moreover, at alkaline pHs, movements of anions and not protons are expected to keep the

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electroneutrality in the device [59e62]. By symmetric thought, at lower pHs, Nafion membranes could be more adequate. So, regarding this fourth issue, lowering leachate pH would have a positive effect on the characteristics and performance of our MFCs. The highest value of PV-ave achieved in our work was nearly 30% of the corresponding value for anaerobic digestion of wastes, a well established commercial energy-generating process. The power thresholds typical of the anaerobic digestion of municipal wastewaters are in the range 5e50 W/m3 [63]. Although the powers delivered by our MFCs are attractive, actual implementation of full scale treatment with MFCs in order to compete with commercially available treatment technologies is still a challenge. Single, large MFCs are not feasible, at least at present time. For a commercial application, in order to achieve the required power, potential, current intensity, and volume to treat large flowrates of wastewater, as well as to be comparable to established waste processes such as anaerobic digestion, a modular approach is required. On the one hand, the sum of the volumes of the individual MFCs should equal the overall volume estimated by the flowrate of wastewater and hydraulic time retention considerations [53]. On the other hand, series connection of MFCs will give a reasonable potential [64,65]. In principle the potentials are additive, based on Ohm's law for electromotive forces in series. For instance, assuming a 0.6 V for individual MFCs, 10 similar MFCs should be connected in series in order to deliver 6 V. Also, for delivering high current intensities, parallel connection of MFCs is recommendable (again based on Ohm's laws). The latter has the additional advantage that the overall internal resistance will be given by the inverse sum of resistances, according to Ohm's laws for circuits in parallel [34,36,66] and, in consequence, the overall internal resistance value of the parallel combination will be considerably lower. A proof follows: let us assume that ‘N’ MFCs of equal volume and characteristics are connected in parallel with the same internal resistance Rint each (tween cells). According to Ohm's laws, it holds the following 1=Rparallel set ¼ 1=Rint þ 1=Rint þ … þ 1=Rint t ¼ N=Rint

(10)

Rparallel set ¼ R nt =N

(11)

Thus, an actual MFC setup for commercial applications will be an array of multiple MFCs. The array is also known as stacking and assemblage of MFCs. Challenges to this still remain. As we mentioned above, one approach to increase MFC voltages would be to connect multiple MFC in series, forming a stacked system. However, overshooting or voltage reversal of MFCs connected in series has been reported [67]. The stack usually undergoes voltage reversal, resulting in a lower or nearly zero stack voltage. Voltage reversal has been shown to occur when anode potentials become unbalanced, for example when substrate concentration is low in one cell relative to an adjacent cell. In this case, the biocatalysts are less active at the lower substrate concentration. Thus, the anode potential of that cell becomes positive and similar to the cathode potential of the adjacent cell. Moreover, voltage reversal can also occur under high

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current even without substrate depletion. Voltage reversal occurring in only one of multiple MFCs connected in series generally results in a failure of the whole system [ [59] [68], [69]]. Another way to increase the voltage and avoid the connection in series of MFCs, is to couple a parallel array of MFCs to a transformer of voltage. However, the transformer output will have a lower power that the input (likely 20% lower), and a current intensity output approximately the current intensity input divided by the ratio of potential increase. Therefore, the contributions of Electrical and Electronic Engineerings are required for successful, reliable arrays of MFCs. Other challenges related to construction costs (cathodic catalyst and separators are the most expensive components of MFCs [53], inter alia, are also significant issues that have delayed the scale-up and full scale applications of MFCs. To the best of our knowledge, it is the first time that volumetric powers as high as 13 W/m3 along with organic matter removal efficiencies of 76% are reported in the treatment of actual leachates in MFC. Our results constitute a promising step towards sustainable remediation of recalcitrant leachates.

Conclusion The application of inocula enriched in Fe(III) and Mn (IV)reducing bacteria significantly improved the performance of cells that used RuxMoySez as a cathodic catalyst for the ORR.In general parallel connection of electrode faces significantly decreased the Rint. The RuxMoySez can be an attractive alternative cathodic catalyst for MFCs that generate electricity from leachate. The highest value of PV-ave achieved in our work was about 30% of the corresponding value for anaerobic digestion of wastes, a well established commercial treatment and energygenerating process.

Acknowledgements ICyTDF now SECITI-DF (PICCO 10-28) and CINVESTAV-IPN (Mexico) financial support to this research is gratefully acknowledged. CONACYT granted a graduate scholarship to ALV-L and support as Infrastructure Project No. 188281 to HMP-V, Environmental Biotechnology and Reable Energy Group. The authors wish to thank the help of Research Assistants and Technicians from the Environmental Biotechnology and Reable Energies R&D Group and the Hydrogen and Fuel Cell Group, both from CINVESTAV del IPN.

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Notation bCOD: number of moles of electrons harvested from one mol of COD (4) BOD5: biochemical oxygen demand COD: chemical oxygen demand CODf: final COD CODi: initial COD CRS: actual amount of charge (electrons) produced from the degradation of substrate CTS: maximum amount of charge (electrons) that could be produced from the substrate if all the substrate were channeled to electricity generation Eo: standard reduction potential Eo0 : standard reduction potential at biological conditions, similar to Eo except of the proton concentration which is set at 107 M EAB: electrochemically active bacteria EMFC-ave: average potential

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EMFC-max: maximum power density EMFC-OCP: open circuit potential of the cell F: Faraday's constant IMFC: current intensity In-EFe(III): inoculum enriched in Fe (III)-reducing bacteria In-EMn(IV): inoculum enriched in Mn(IV)-reducing bacteria In-SR: sulphate reducing inoculum MCOD: COD's molecular weight (32 g mol1) MFC: microbial fuel cell MFC-G: microbial fuel cell with granular graphite as anode, with chalcogenide catalyst in the cathode N: number of MFCs in a parallel array NADH: nicotineamide dinucleotide, reduced form ORR: oxygen reduction reaction PEM: proton exchange membrane

PS-ave: average power density PS-max: maximum power density (superficial) PV: volumetric power PV-ave: average volumetric power PV-max: maximum volumetric power Rext: external resistance Rint: Internal resistance VSS: volatile suspended solids Greek characters hCOD: chemical oxygen demand removal efficiency hCoul: coulombic efficiency