Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment

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 x x x ( 2 0 1 6 ) 1 e1 0

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Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment Chih-Hung Wu, Jing-Chen Shih, Chi-Wen Lin* Department of Safety, Health and Environmental Engineering, National Yunlin University of Science and Technology, 123 University Rd., Sec. 3, Douliou, Yunlin 64002, Taiwan, ROC

article info

abstract

Article history:

This work develops an innovative biotrickling filter-microbial fuel cell (BF-MFC) for use in

Received 14 June 2016

electricity production and removing ethyl acetate (EA) that is emitted from a gaseous

Received in revised form

stream. A new membrane design, providing effective delivery of protons released from

15 August 2016

microorganisms that biodegrade EA from the anode to the cathode, was developed using a

Accepted 25 August 2016

polyvinyl alcohol-membrane electrode assembly. As the EA concentration was increased

Available online xxx

from 0.18 g/m3 to 1.44 g/m3, the voltage increased from 49.4 mV to 658 mV, and when EA organic loading rate ranged from 14.41 to 29.58 g/m3/h, the elimination capacity (EC)

Keywords:

reached almost the 100% conversion line. A maximum power density of 49.1 mW/m2 and

Biotrickling filter-microbial fuel cell

an EA elimination capacity of 83.8 g/m3 h were obtained. Microbial community analysis

(BF-MFC)

revealed that two distinct groups of exoelectrogenic microbes and EA-degraders were

Ethyl acetate (EA)

dominated in the conductive coke surface and in the inner tube wall of the BF-MFC,

Polyvinyl alcohol-membrane elec-

respectively.

trode assembly (PVA-MEA)

© 2016 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved.

Electricity generation

Introduction With the rapid development of urban areas and industrial parks, the use of coating paints has increased in recent years. However, most coating paints are solvent-based, and contain organic solvents, such as paint activators and hardeners [1]. Ethyl acetate (EA), can be easily mixed with other organic solvents or water, and thus is commonly used as an industrial solvent in coating paints [2]. EA is a volatile organic compound (VOC) so if it is not captured for further treatment, it may be emitted into the atmosphere. Exhaust emissions of EA from various industrial processes cause

environmental damage and are hazardous to human health. Although physico-chemical methods have been proven to be successful in removing volatile organic compounds (VOCs) from waste gases [3], high cost and potential byproduct formation have limited their use. Biological treatment, such as biofiltration, has long been considered to be a more cost-effective and environmental friendly means than others to treat air flows that contain moderate-to-low concentrations of VOCs [4]. Among various biofiltration devices, biotrickling filters often outperform others such as biofilters; as a continuously and intermittently flowing aqueous phase provides better control over environmental

* Corresponding author. Fax: þ886 5 531 2069. E-mail address: [email protected] (C.-W. Lin). http://dx.doi.org/10.1016/j.ijhydene.2016.08.186 0360-3199/© 2016 Hydrogen Energy Publications LLC. Published by Elsevier Ltd. All rights reserved. Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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conditions, such as nutrients, pH and the purging of hazardous degradation byproducts [5]. In recent years, microbial fuel cells (MFCs) have attracted much attention as they combine electricity generation with pollutant treatment [6,7]. Many configurations of MFCs, including the twochamber MFC, air-cathode MFC, tubular type MFC, and a stack MFC, have been developed [8e10]. Among them, the air-cathode MFC is regarded as one of the best scalable configurations, because it does not require aeration and oxygen is the most sustainable and environmentally friendly electron acceptor [11]. Most MFCs use liquid or solid contaminants as fuel. Few investigations have reported the use of gaseous pollutant except using gaseous toluene [12] and gaseous ethyl acetate, as a fuel source in an MFC [13]. However, such MFCs are small (reactor volume of 25e50 cm3). Evelyn et al. [14] proposed a potential scheme of two-stage MFCs: the first stage removes gaseous pollutants by anoxic biofiltration with the generation of a reduced mediator, and the second stage generates electricity and an oxidized mediator that is recycled to the biofilter. However, no research has been performed on a system that incorporates an MFC with a biofiltration system. This work develops an integrated one-stage biofiltration system for treating gaseous contaminants using a biotrickling filter (BF) that is coupled with an MFC; it has the advantages of both MFC systems and biofiltration technologies. This study tests the first time the feasibility of using conductive coke as the material in a three-dimensional anode increase the production of electricity in the MFC. The performance of the innovative biotrickling filtermicrobial fuel cell (BF-MFC) system under various inlet loads was investigated, with reference to electricity generation, and microbial changes associated with gaseous EA biodegradation.

Materials and methods Experimental set-up and operation The rectangular BF-MFC system was constructed by incorporating BF into an MFC, as presented in Fig. 1. The BF-MFC, constructed using acrylic glass, was divided into three sections, which were the upper sprinkler section (8 cm  8 cm  8 cm), the central conductive filter section (8 cm  8 cm  15 cm  2 layer), and the bottom drainage section (8 cm  8 cm  5 cm). The BF-MFC included a packing bed that contained conductive carrier material (coke), the main anode (graphite rod, 1.6 cm in diameter  15 cm in length, real surface area of 79.4 cm2), and a cathode (carbon cloth, 6 cm in width  13 cm in length). The central conductive filter section was packed with conductive coke yielding a total bed depth of 30 cm and an effective packed-bed volume of around 1.92 L. Appurtenances that were adjunct to the main BF-MFC were the gas supply system and the circulating water system. A graphite rod was positioned vertically and centered inside the BF-MFC, and its central conductive section was packed with conductive coke granules as carriers for growing microbes. The conductive coke recovered electrons that were

released by the biodegradation of contaminants, and these electrons were then transferred to the graphite rod. The unique anode design, allowing full contact between the coke and the graphite considered as a three-dimensional anode of the MFC system, yielded a large surface area of the anode. A new membrane design, providing effective delivery of the protons that were released from the anode to the cathode, was developed using a polyvinyl alcohol membrane electrode assembly (PVA-MEA), which combined proton exchange membrane into cathode in the MFC. The cathode side of PVA-MEA was installed outside of the BF-MFC and thus exposed to atmospheric air. Section 2.2 presents details of the PVA-MEA. The anode and cathode were connected using titanium wire (0.4 mm) with an external resistance of 1 kU in a loop configuration. The BF-MFC system was operated as the air and liquid flows directed downward. Compressed air was passed through oil and air filters to remove oil, particulate matter and microbes. After purification, the air to the BF-MFC was controlled. Ethyl acetate (EA) solvent (99.5%, ECHO Chemical, Taiwan), used as the target contaminant, was continuously injected by a syringe pump (Fusion 100, Chemyx, USA) into the influent air stream, where it vaporized and entered the gasmixed chamber for further mixing. The flow rates of both the gas and solvent streams were controlled by using previously calibrated flow-meters to obtain the desired gas flow rate and contaminant concentration at the BF-MFC entrance. A liquid feed was continuously recirculated over the trickledbed by using a sprinkler nozzle that was controlled by a solenoid valve and a centrifugal pump. Table 1 provides the operating parameters.

Preparation of PVA-MEA Polyvinyl alcohol hydrogel (PVA-H), with its functional groups of [(e(CH2)2)] and [(CeOH)], can be served as a proton conductor [15]. PVA-H elastomer (PVA-HE), a solid polymeric ionic conductor, can be obtained by physical crosslinking reaction proceeded by freezing and thawing processes [16]. In our PVA-MEA preparation, PVA-H was obtained by firstly dissolving PVA granules (BF-26, Chang Chun Petrochemical Co., Ltd, Taiwan) in deionized water and then autoclaving the dissolved PVA at high temperature and pressure. One hundred milliliters of 10% PVAH were then poured into a container mold (30 cm  20 cm) with stirring to prevent the formation of air bubbles. After the PVA-H had been uniformly distributed in the mold, the mold was placed in a freezer, and the PVA-H was frozen at 30  C for 12 h. Thereafter, the water-soluble PVA-HE was obtained while thawing at room temperature; it was then covered with a carbon cloth (30 cm  20 cm; 0.7 mm thick, made of CW1001, from KoTHmex, Taiwan), which adhered to its surface. The mold with the PVA-HE that was covered with the carbon cloth acted as a cathode, which was then placed in a freezer and frozen at 30  C for 12 h, before being thawed against at room temperature. The physical crosslinking reaction proceeded in a freeze-thawing cycle, forming water-insoluble PVA-HE from water-soluble PVA-H. The water-insoluble PVA-HE was then stored in a dryer at 50  C to eliminate the water, yielding a solid PVA-MEA.

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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 x x x ( 2 0 1 6 ) 1 e1 0

3

Legend 6 7

iii 5

16

8 12 4

13

9 10

3

i 14 15

2

ii i

Air compressor

2

Oil filter

3 4

Air filter Mass flow controller

5

Syringe pump

6

Gas mixed chamber

7

Sprinkler

8

Coke

9

Graphite rod (anode)

10

Gas sampling site

11

Water tank

12

Resistance

13

PVA-MEA (cathode)

14

Digital multimeter

15

Water sampling site

16

Rotameter

i

Gas flow line

ii

Water flow line Electron flow line

iii

11

1

1

Fig. 1 e Schematic of the biotrickling filter-microbial fuel cell.

Table 1 e Basic operational characteristics of the experimental unit. Operating parameters Inlet ethyl acetate concentration Air flow rate Empty bed contact time (EBRT) Liquid recirculation velocity Ethyl acetate loading rate Superficial air velocity

Chemical and dissolved oxygen analysis

Data (unit) 3

50e900 ppmv (0.18e3.24 g/m ) 2.5 L/min 46 s 3.75 m3/m2/h 14.41e264.63 g/m3/h 23.43 m3/m2/h

Measurement of microorganisms, packing media and biomass in packed bed The microorganisms that were used in this study were obtained from an oil cracking wastewater treatment plant of Nanya Plastics Co. Ltd., Yunlin County, Taiwan. They were acclimated and kept for more than three months in an aerobic flask with a mineral medium that contained EA as the sole carbon source. The inorganic compounds in mineral medium solution (MSM) were NH4Cl, 0.95 g/L; MgCl2$6H2O, 0.53 g/L; FeCl3$6H2O, 0.972 g/L; CaCl2$2H2O, 0.018 g/L; CuCl2$2H2O, 0.01 g/L; CoCl2$6H2O, 0.2 g/L; ZnCl2, 0.047 g/L; MnCl2$4H2O, 0.03 g/L; Na2MoO4$2H2O, 0.03 g/L and NiCl2$6H2O, 0.02 g/L. Phosphate buffered solutions (PBS) consisted of K2HPO4 and KH2PO4, were employed as supporting electrolyte. Conductive coke granules that were packed in the BF-MFC chamber were obtained from the China Steel Corporation (Kaohsiung, Taiwan). The physico-chemical properties of the granules included a grain size of 2e4 cm, a specific surface area of 0.6e0.8 m2/g, a porosity of 33e55%, a bulk density of 400e520 kg/m3 and a resistance of 1.47 ± 0.17 U. The inoculum procedure for the BF-MFC and the methods of measuring biomass were those of Balasubramanian et al. [17].

To investigate the performance of the biotrickling filter, the inlet and outlet EA concentrations were measured. Moreover, potential byproducts of EA degradation such as ethanol and acetic acid were analyzed. Air samples were withdrawn from inlet and outlet locations in the BF-MFC using a 250 mL gastight syringe with a Luer-lok valve (Hamilton, USA). The EA concentration was analyzed on a gas chromatograph that was equipped with a flame ionization detector (GC-FID, GC-2014, Shimadzu, Japan) and a Stabliwax-DA capillary column (30 m  0.53 mm  1 mm, Restek, USA). The carrier gas was helium (99.98% pure) and the makeup gas was nitrogen. The oven was maintained at a constant temperature of 60  C, while the injector and detector temperatures were set at 150 and 180  C, respectively. The EA inlet mass loading rate L (g m3 h1) in Eq. (1), the elimination capacity (EC) (g m3 h1) in Eq. (2), and the removal efficiency (RE) (%) of the BF-MFC in Eq. (3) were obtained from the relationships among the influent (Cg in, g m3) and effluent (Cg out, g m3) gas phase concentrations, the gas flow rate (Qg, m3/h), and the packed-bed volume (V, m3) of the BF-MFC. The dissolved oxygen (DO) levels in the solution of anode chamber were measured using a NeoFox oxygen probe (Ocean Optics Inc., USA). Inlet loading (L, g/m3 h) L¼

Cg

 Qg V

in

(1)

Elimination capacity (EC, g/m3 h) EC ¼

Cg

in

 Cg V


out

 Qg

(2)

Removal efficiency (RE, %)

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

4

RE ¼

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 x x x ( 2 0 1 6 ) 1 e1 0

Cg

in

 Cg Cg


out

 100

(3)

Results and discussion

in

Electrochemical analysis Voltage was measured every 2 min using a multi-digital meter (CHY-48R, CHY, Taiwan). The BF-MFC anode was sampled for cyclic voltammetry (CV) analysis with a constant potential rectifier (SP150, Biologic, France). CV experiment was conducted with the anode placed in the solution obtained from the anode chamber of an ethyl acetate-fed MFC at the end of experiment. The scan rate used was 10 mV/s over the range from 1.0 to 1.0 V. All experiments were repeated 3 times and the third cycle was selected. Internal resistance was obtained using the polarization slope method and the power density peak method, as described by Logan [18]. The polarization curves and the power density curves were obtained by varying the external resistance from 10 U to 3000 kU during stable MFC operation every 10 min after each resistance load was changed. The current was computed using Ohm's Law. The current density was calculated by dividing the current by the surface of the graphite rod of the anode. The calculated current density was then multiplied by the voltage to obtain the power density.

Scanning electron microscopic analysis The morphologies of the biofilms that formed on the surfaces of the PVA-MEA and the anode were observed using a scanning electron microscope (SEM, JEOL, JSM-6700F, Japan). When samples of biofilm were extracted from the anode chamber or the PVA-MEA of the BF-MFC, the samples were immediately sliced using a sterile blade, and washed three times in deionized water, before being immersed in 2.5% glutaraldehyde solution for 3 h. They were then dehydrated stepwise using a series of acetone solutions (50, 60, 70, 80, 90, 95, 100% and 100%), each for 30 min. Notably, the 100% solution was used twice. The electrode samples were then immersed in isoamyl acetate for 2 h and lyophilized, before being finally sputter-coated with a thin layer of gold for examination by SEM.

Effects of acclimation and open and closed circuits on RE of EA A BF-MFC system was used to measure and compare the RE of waste gases that contained EA and the generation of electricity under open-circuit and closed-circuit conditions. During the experiment, the initial bacterial concentration was set to 45 g/L (volume of 1 L). With the continuously sprinkled circulating water, free-living microorganisms gradually became attached to the coke surface, and the EA in the biomass solution was the source of carbon in the development of a biofilm. Fig. 2 shows that the RE of EA was in the range of only 11e12% in both the open-circuit and the closed-circuit in the BF-MFC system, because the microorganisms did not become attached to the coke in the first four days of acclimation. However, in an open circuit, when a biofilm began to form, the electrons that were released by the microorganisms were not delivered to the anode because they could only be transferred within the microorganisms [20]. Thus, in an opencircuit, the RE was only 79.8% (Day 11e46). In a closed-circuit, when free-living microorganisms began to develop a biofilm on the anode and the microorganism biodegradation of the EA generated electrons, these electrons were delivered following one of three following pathways according to whether the biofilm was in contact with the anode [21], the nanowires of the exoelectrogenic bacteria were in contact with the anode, or a mediator entered from the external environment [22]. In a closedcircuit, electrons from the microorganisms on the anode continued to be delivered through the MFC system to the cathode; these electrons participated in a redox reaction with oxygen and protons on the cathode, so the electrons and protons were continuously consumed. To survive and generate biomass, the microorganisms, particularly those on the anode, had to consume organic compounds to obtain electrons that were lost during metabolism [23], so they continuously biodegraded the EA to obtain energy. Therefore, the RE of the EA increased by 14% and reached 93.8% in a closed-circuit (Day 11eDay 46).

PCR-DGGE analysis of microbial community Removal efficiency (%)

Attached biofilm and sludge samples were collected from the surface of the anode and the PVA-MEA at the end of each test run. Genomic DNA was extracted directly using an AxyPrep™ Bacterial Genomic DNA Miniprep Kit (Axygen Biosciences, Union City, CA, USA), following the manufacturer's instructions. Region V3 of the 16S rDNA, corresponding to nucleotide positions 334e514 of the Escherichia coli gene, was amplified using the primers EUB1 (50 -CAGACTCCTACGGGAGGCAGCAG-30 ) and UNV2 (50 -GTATTACCGCGGCTGCTGGCAC-30 ). PCR-DGGE (polymerase chain reaction-denaturing gradient gel electrophoresis) and 16S rDNA gene sequencing for community analysis were performed as described in our earlier paper [19].

100 80 60 40 20 0

0

Closed circuit Open circuit 10

20 30 Time (d)

40

50

Fig. 2 e Removal efficiency of EA in BF-MFC under the open-circuit and closed-circuit conditions.

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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Effects of EA concentration on voltage and RE of EA The effects of EA concentration on the generation of electricity and RE under were investigated at an EBRT of the BF-MFC system of 46 s, a water circulation rate of 400 mL/min, an air flow rate of 2.5 L/min, and an EA concentration of 0.18e3.24 g/ m3 (50e900 ppmv). According to Fig. 3, when the EA concentration was set to 0.36 g/m3 (100 ppmv) during acclimation, microorganisms did not develop on the conductive coke surface. Under the specified condition, the holes in the fresh coke contained a small amount of oxygen, which consumed the electrons that were released by the microorganisms were consumed directly by the oxygen. Therefore, during acclimation, the voltage progressively increased from a negative value (80.9 mV) to a positive one (222.9 ± 9.5 mV), and the mean RE increased from 8.14% to 95.23%. As microorganisms gradually developed on the coke surface, they gradually consumed the oxygen in the holes of the coke. Therefore, the oxygen stopped receiving the electrons, instead were directly transferred to the anode. Ntwampe et al. [24] indicated that dissolved oxygen (DO) penetration depth decreased with increasing biofilm thickness, which resulted in the formation of anaerobic zones in the biofilms. The DO decreased from 6.5 mg/L in the water to almost zero at 250 mm depth of the biofilm in their measurements. In our BF-MFC, actually an attached growth mode system, the central conductive section was packed with conductive coke granules as carriers for growing microbes as biofilms. The coke collected electrons that were released by the biodegradation of EA, and these electrons were then conveyed to the graphite rod. As the EA concentration was reduced from 0.36 g/m3 to 0.18 g/m3, the average RE increased from 95.23% to 99.07%. However, the voltage declined drastically from 225.5 ± 4.2 mV to 49.4 ± 3.1 mV because the EA concentration of the BF-MFC system was very low, and the microorganisms on the anode could not generate power because the supply of electrons (carbon source) was limited. As the EA concentration was increased from 0.18 g/m3 to 1.44 g/m3, the EA in the system sufficed to enable the microorganisms to biodegrade and

Acclimation 0.183 0.363 0.723 1.083 1.443 1.803 2.163 2.523 2.883 g/m g/m g/m g/m g/m g/m g/m g/m g/m

3.24 g/m3

600

80

Voltage (mV)

500 400

60

300 40

200 100

Voltage Removal efficiency

0 -100

0

20

40

60

80

100

120

140

20

Removal efficiency (%)

100

700

0

Time (d) Fig. 3 e Voltage and removal efficiency under different EA concentrations in the BF-MFC system.

5

release electrons. Under these conditions, the voltage increased from 49.4 ± 3.1 mV to 658 ± 38.0 mV, the RE ranged between 99.07% and 73.86%, and the Coulombic efficiency (CE) ranged from 3.49% to 3.62% (Table 2). As the EA concentration was increased from 1.80 g/m3 to 3.24 g/m3, the RE declined markedly from 65.31% to 32.69%, the voltage fell rapidly from 635.0 ± 9.7 mV to 276.2 ± 4.0 mV, and the CE decreased from 3.04% to 0.71%, revealing that the microorganisms could not adapt to the short-term effects of the high EA concentration. The CE was relatively low compared to those of in waste water treatment application found in the literature [25,26]; however, the removal efficiency of the EA increased by 14% as shown in Fig. 2, revealing the contribution of electricity generation to the removal of EA. Moreover, this research is unique and significant because there is few report available about enhance effect of the removal of gaseous pollutants using MFCs. This result is similar to that obtained by Arutchelvan et al. [27], who found that high substrate concentrations influence the metabolic rate of microorganisms and thereby affect the RE and output voltage. According to an analysis of the circulating water of BFMFC, the microorganisms biodegraded the EA of 26.2 mg/L to form ethanol and acetic acid as the byproducts (Fig. 4). Ethanol and acetic acid were initially formed when the microbes degraded the EA, and were themselves eventually degraded by microbes. The finding is consistent with results reported by several researchers [28,29]. The biodegradation of ethanol forms accumulating acetaldehyde, which may inhibits the biodegradation of the EA by the microorganisms [30]. However, acetaldehyde was not detected in our experiment, probably due to the low concentration of EA tested. Fig. 4 also shows an increase pattern of voltage output with byproduct formation for biodegradation of EA. It should be noted that the voltage output was influenced by the presence of byproducts as indicating by persistent voltage output. However, voltage output gradually dropped while concentrations of byproducts and EA decreased. According to Fig. 5 and Table 2, when the EA organic loading rate ranged from 14.41 to 29.58 g/m3/h, the elimination capacity (EC) reached almost the 100% conversion line. Under these conditions, the RE of the BF-MFC system remained between 95.40% and 99.07%, and the reaction is regarded as a first-order diffusion-limited reaction [30]. However, when the EA organic loading exceeded 53.96 g/m3/h, this reaction became a zero-order reaction in the biofilm [29], reducing the RE. When the organic loading of EA slowly increased, the highest EC obtained was 97.18 g/m3/h, and the mean EC was 95.77 g/m3/h.

Electrochemical analysis at various EA concentrations In this experiment, conductive coke was used as a filler in a closed circuit BF-MFC system, in which the biodegradation and electricity generation were assessed with various EA concentrations. In Fig. 6, the EA concentration increased from 0.18 to 3.24 g/m3. As the EA concentration increased from 0.18 g/m3 to 1.44 g/m3, the voltage increased such that the maximum average voltage was 658.3 ± 38.0 mV, the maximum power density was 49.1 mW/m2, the current density was

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

6

25 20 15

200

10

Concentration (mg/L)

300

100

5

0

0 0

1

2

3

4

5

6

7

Time (h)

Fig. 4 e Voltage output and byproduct formation for biodegradation of EA.

200

0 10

%

co

i on ers nv

e li n

100 80

150

60

100

40

50 0

Elimination capacity Removal efficiency 0

50

100 150 200 Inlet loading (g/m3/h)

250

20

Removal efficiency (%)

250

Elimination capacity (g/m3/h)

598.6 572.6 ± 9.7 114.8 1733.3 38.2 576.9 2.16 26.0 84.7 658.2 635.0 ± 9.7 125.6 1896.4 45.7 690.5 3.04 23.2 86.8 680.6 658.3 ± 38.0 130.1 1964.6 49.1 741.0 3.62 22.3 85.3 559.1 534.4 ± 23.3 105.8 1597.4 32.4 489.9 3.95 24.7 87.9 368.2 342.1 ± 11.3 66.7 1007.3 12.9 194.8 3.92 26.1 89.1 251.6 225.5 ± 4.2 24.0 363.0 3.4 50.6 3.82 26.1 155.5 76.8 49.4 ± 3.1 1.8 27.0 0.1 1.1 3.49 27.4 697.4

30 Voltage Ethyl acetate Ethanol Acetic acid

400

Voltage (mV)

447.0 418.7 ± 9.9 88.2 1332.3 22.6 340.8 1.20 28.3 77.1

307.2 276.2 ± 4.0 57.2 864.6 9.5 143.5 0.71 31.0 85.7

500

522.6 495.1 ± 4.9 102.2 1543.8 30.3 457.6 1.59 27.5 81.0

900 32.69 264.63 86.51 800 43.28 229.89 95.17 700 46.88 203.30 95.31 600 58.40 166.41 97.18 500 65.31 146.14 95.45 400 73.86 113.45 83.80 300 81.31 88.62 72.05 200 89.38 53.96 48.23 100 95.40 29.58 28.21 50 99.07 14.41 14.27

2.88 2.52 2.16 1.80 1.44 0.18

0.36

0.72

1.08

Concentrations of EA (g/m3)

Table 2 e Bioelectrochemical characteristics and removal efficiencies of BF-MFCs under various EA concentrations.

Parameters

For substrate analysis Ethyl acetate concentration (ppmv) Removal efficiency (%) Loading rate (g/m3/h) Elimination capacity (g/m3/h) For electrochemical analysis Open-circuit voltage (mV) Average voltage (mV, at steady state, 1 kU) Current density (mA/m2) Volumetric current density (mA/m3) Maximum power density (mW/m2) Maximum volumetric power density (mW/m3) Coulombic efficiency (%) Difference of open/closed-circuit voltage (mV) Internal resistance (U)

3.24

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 x x x ( 2 0 1 6 ) 1 e1 0

0

Fig. 5 e Relationship between loading and elimination capacity of EA by BF-MFC system. 130.1 mA/m2, and the internal resistance was 85.3 U. Table 2 presents the other electrochemical parameters that pertain to the changes in the EA concentration. Fig. 6 and Table 2 show that as the EA concentration increased from 1.44 to 3.24 g/m3, the maximum power density dropped significantly from 49.1 to 9.5 mW/m2 and the voltage decreased from 658.3 ± 38.0 to 276.2 ± 4.0 mV. Accordingly, owing to the high EA concentrations, the substrate inhibited, and thereby reduced the efficiency of biodegradation by the microorganisms [27]. In this study, the polarization curve in Fig. 6 (a, b) was to evaluate the internal resistance of the system, yielding the results in Table 2. These results indicate that as the EA concentration increased below 1.44 g/m3, the internal resistance declined (from 697.4 to 85.3 U); the average voltage of the system was 658.3 ± 38.0 mV and the open-circuit voltage was 680.6 mV. A cyclic voltammogram was obtained using the phosphate buffered solution and with a new anode (without a biofilm), no redox couples were detected (Fig. 7). However, oxidation and reduction peaks were present when using an anode with biofilm. These results make it appear probably that the major mechanism of electricity generation in the batch experiment was by direct transfer of electrons to the electrode by bacteria containing enzymes (i.e., outer membrane protein) directly attached to their cell membranes. The finding is consistent

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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 x x x ( 2 0 1 6 ) 1 e1 0

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Fig. 6 e Power generation (a, b) and polarization curve (c, d) for the BF-MFC under various EA concentrations. energy for growth, increasing the release of electrons by biodegradation. In this situation, since the biofilm covered the surface of the anode, the surface of the biofilm directly consumed the oxygen in the EA-contaminated air stream [35]. Therefore, no plenty of oxygen can transport further to the inner region of biofilm and then to consume electrons in the anode. Accordingly, after the microorganisms biodegraded the substrates, the released electrons were directly delivered to the anode, reducing the internal resistance [36].

2

Current (mA)

1 0 -1 -2 -3 -4 -1.2

With a biofilm Without a biofilm -0.8

-0.4

0.0

0.4

0.8

1.2

Potential (mV, versus Ag/AgCl)

Fig. 7 e Cyclic voltammograms of a new anode (without a biofilm) and an anode with a biofilm.

with results reported by Liu et al. [31]. The three oxidation peaks present in the cyclic voltammogram were presumably attributed to that bacteria excreted the outer membrane proteins (dehydrogenase, alcohol dehydrogenase (ADH) and aldehyde dehydrogenase 2 (ALDH2)) during EA biodegradation (a single reduction peak) [30,32,33], thereby resulting in the formation of byproducts (ethanol, acetic acid, and acetaldehyde). Fig. 8 shows that when the microorganisms gradually formed a biofilm on the surface of the anode, the biofilm became more tolerant of the substrates [34], facilitating the use by the microorganisms of the substrates as a source of

Structural analysis of microbial communities in BF-MFC system In this study, polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE) was used to obtain the distribution of the microbial communities on the anode of a BF-MFC system with an EA concentration of 1.08 g/m3. Fig. 9(a) reveals that the microbial species on the surface of the graphite rod (Lane 1) were associated with bands b, d, f, g, i, j, k, l, m, q, r, and s. The microbial species on the coke surface (Lanes 2e4) were associated with bands a, c, d, e, f, g, i, k, l, m, o, p, r, v, w, x, and y. The microbial species on the inner tube wall in the BF-MFC system (Lanes 5e6) were associated with bands e, f, g, i, k, m, o, p, t, u, v, w, and y. The microbial species in the circulating water (Lane 7) were associated with bands e, g, i, k, m, n, p, r, t, v, w, and y, of which bands g, i, k, and m were consistently observed on the graphite rod surface, coke

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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Fig. 8 e SEM image of coke surface for microbe attachment during (a) 1 day, (b) 7 days, (c, e) 14 days, and (d, f) 21 days. (aed: 100£; e: 500£; f: 4000£).

(a) 1 2 3 4 5 6 7

Gel (40%) b d f h j l n p r t v

1 2 3 4 5 6 7 a c e g i k m o q s u w

x Gel (70%)

(b)

y

Lane 1 (Middle, graphite rod surface) Lane 2 (Top, coke surface)

Lane.3 (Middle, coke surface) Lane.4 (Bottom, coke surface) Lane.5 (Top, DL-BTF-MFCs wall) Lane.6 (Bottom, DL-BTF-MFCs wall) Lane.7 (Circulation water) 0.48

0.57

0.66 Coefficient

0.74

0.83

Fig. 9 e DGGE profiles of microbial communities in anode chamber at different sampling points of the BF-MFC system. DGGE profiles (a) and cluster analysis (b).

surface, inner wall tube, and in the circulating water tank. Therefore, these species became the dominant species that used EA as a carbon source in biodegrading EA. Studies have established that exoelectrogenic bacteria transfer electrons through their nanowires, the mediator (such as pyocyanin) that is formed by the bacteria [37], or upon the addition of chemical mediators (such as neutral red or thionine) [38]. After the nanowires or mediators transfer the electrons from the microorganisms across the cell membrane, the electrons are delivered to the cathode for a reduction reaction with oxygen and protons to generate electricity. When microorganisms attach themselves to the anode, the microbial communities receive electrons that are generated by the

microorganisms in the MFC system and thus gradually develop into communities of exoelectrogenic bacteria [39]. Fig. 8(a) reveals that bacterial bands p, t, v, and w appeared only on the inner tube wall (Lanes 5e6) and in the circulating water tank (Lane 7), so they can be classified as microbial communities that biodegrade EA without generating electricity. Conversely, bands d, f, and r appeared only on the surfaces of the graphite rod and coke, so they can be classified as microbial communities that generate electricity. Based upon the cluster analysis in Fig. 9(b), the microbial communities in the BF-MFC system can be categorized into two groups - those that develop on the anode surface, biodegrade EA, and produce electricity (bands g, i, k, and m) and those that developed in the circulating water tank and on the inner tube wall in the BF-MFC system and biodegrade EA without generating electricity (bands p, t, v, and w). The degree of similarity between these two groups was 59.4%. With respect to the similarity between microbial communities in the circulating water and in various regions of the tube wall, the degree of similarity between communities on the top and bottom of the tube wall was 83%, and that between those in these two regions of the tube wall and in circulating water was 79.5%, indicating that the microbial communities in the circulating water consumed the dissolved EA or its biodegradation byproducts in the water, as a source of energy to survive. Fig. 8 compares the structural and dendrograming variations of the microbial communities that developed in various regions of the anode. At the inlet, air entered the top of the BF-MFC system, traveling toward the bottom, so the biofilm that developed in the top region of the coke surface was more easily affected by the EA impact. Accordingly, the differences between the microbial communities in the top and those in both the middle and bottom regions were considerable. The degree of similarity between these two microbial communities was 69.9%. In summary, Fig. 8 shows that the exoelectrogenic bacteria could only accept electrons in the presence of electrode. Therefore, the two types of microbial communities were exoelectrogenic bacteria that developed on the surface of the graphite rod or the electrically conductive coke, and nonexoelectrogenic bacteria that developed on the inner tube wall and in the circulating water tank.

Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186

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 x x x ( 2 0 1 6 ) 1 e1 0

Conclusion Owing to the porosity and conductivity of the conductive coke, the electrons from the microorganisms could be delivered to the coke surface through the biofilm. Additionally, because of the direct contact between the graphite rod and the conductive coke, these electrons were transferred directly to the cathode. Moreover, when the circulating water was sprinkled in BF-MFC and the PVA-MEA was implemented in the BF-MFC system, the protons in the circulating water were delivered through the PVA-MEA to the cathode and participated in a reduction reaction with oxygen and electrons to generate electricity. These results demonstrate the feasibility of the one-stage BF-MFC system for generating electricity associated with biodegrading EA from waste gas. Overall, the incorporation of PVA-MEA as a cathode in the BF-MFC has promising potential for application of MFC systems in treating gaseous contaminants.

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Acknowledgements [17]

The authors would like to thank the Ministry of Science and Technology of the Republic of China, Taiwan, for financially supporting this research under Contract No. MOST 102-2221E-224-002-MY3.

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Please cite this article in press as: Wu C-H, et al., Continuous production of power using microbial fuel cells with integrated biotrickling filter for ethyl acetate-contaminated air stream treatment, International Journal of Hydrogen Energy (2016), http://dx.doi.org/10.1016/ j.ijhydene.2016.08.186