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Efficient degradation of indole by microbial fuel cell based Fe2O3-polyaniline-dopamine hybrid composite modified carbon felt anode
Journal of Hazardous Materials 388 (2020) 122123
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Efficient degradation of indole by microbial fuel cell based Fe2O3polyaniline-dopamine hybrid composite modified carbon felt anode
T
Minjie Jiana,b, Ping Xuea,*, Keren Shia, Rui Lia, Lan Maa, Peng Lia a b
National Key Laboratory of High-efficiency Utilization of Coal and Green Chemical Engineering, Ningxia University, Yinchuan, 750021, PR China Ningxia Academy of Metrology & Quality Inspection, Yinchuan, 750200, PR China
G R A P H I C A L A B S T R A C T
A R T I C LE I N FO
A B S T R A C T
Editor: G. Lyberatos
Indole is a high-toxic refractory nitrogen-containing compound that could cause serious harm to the human and ecosystem. It has been a challenge to develop economical and efficient technology for degrading indole. Microbial fuel cell (MFC) has great potential in the removal of organic pollutants utilizing microorganisms as catalysts to degrade organic matter into the nutrients. Herein, a novel anode of Fe2O3-polyaniline-dopamine hybrid composite modified carbon felt (Fe2O3-PDHC/CF) was prepared by electrochemical deposition. The degradation efficiency of indole by the MFC loading Fe2O3-PDHC/CF anode was up to 90.3 % in 120 h operation, while that of the MFC loading CF anode was only 44.0 %. The maximum power density of the MFC loading Fe2O3-PDHC/CF anode was 3184.4 mW·m−2, increasing 113 % compared to the MFC loading CF anode. The superior performances of the MFC with Fe2O3-PDHC surface-modified anode owned to the synergistic effect of high conductive Fe2O3 and admirably biocompatible polyaniline-dopamine. MFC with the Fe2O3-PDHC/CF anode could produce considerable electricity and effectively degrade indole in water, which demonstrated a practical approach for the efficient degradation of refractory organic compounds in wastewater.
Keywords: Indole degradation Modified carbon felt anode Fe2O3-polyaniline-dopamine hybrid composite Microbial fuel cell
1. Introduction Indole is well-known for its extensive application in agrochemical, pesticide, cosmetic, dyestuff and medicine due to its unique biological
⁎
properties (Katapodis et al., 2007). Unfortunately, the considerable expansion of these industries has undesirable effects, large amounts of carcinogenic and teratogenic indole are released into coking, pesticide, pharmaceutical, dyestuff, and coal gasification wastewater to bring
Corresponding author. E-mail address: [email protected] (P. Xue).
https://doi.org/10.1016/j.jhazmat.2020.122123 Received 19 November 2019; Received in revised form 14 January 2020; Accepted 15 January 2020 Available online 16 January 2020 0304-3894/ © 2020 Published by Elsevier B.V.
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on hybrid conducting polymer, or even interpenetrating polymer network (Li et al., 2016). Nowadays, Fe2O3 particles have attracted much more attention of scholars as the modification material for anode of MFC due to their unique advantages such as considerable electrocatalysis, chemical stability and low cost (Li and Zhou, 2018; Sun et al., 2017). However, it is difficult for Fe2O3 particles to attach directly to the electrode. The hybrid of inorganic Fe2O3 with organic polymer will be benefit to overcome its defect and improve the electrochemical property. So far as we know, there is no literature report on the performance of Fe2O3-polyaniline-dopamine hybrid composite modified anode in MFC. The objectives of this work were to degrade indole efficiently, to enhance power generation, and to accelerate electrogenic bacteria growth. In our study, a novel MFC anode material was obtained by modifying the CF anode in-situ with the polyaniline-dopamine membrane deposited Fe2O3 particles. The synergistic effect of Fe2O3 particles and polyaniline-dopamine membrane on improving the electrochemical activity and power generation performance of the MFC loading the modified CF anode was discussed. Compared with the MFC loading the bare CF anode, the indole degradation efficiency and electrochemical performances of that loading the modified CF anode have been enhanced significantly. Besides, the bacterial community on the modified CF anode of indole anolyte was analyzed.
about unpleasant odor and environment pressures, which greatly restricts the development of these industries (Joshi et al., 2017; Li et al., 2017; Shi et al., 2019). Furthermore, high concentrations of indole may cause damages to human and animal lung cells and hemocytes (Arora and Bae, 2014; Qu et al., 2013; Carlson et al., 1972). Many treatment technologies have been studied for treating indole-containing wastewater, such as physical adsorption and chemical oxidation technologies (Zhao et al., 2015a; Cao et al., 2014; Antonopoulou et al., 2014). Although they are widely used to remove indole from wastewater currently, their application has been limited by low removal efficiency and serious secondary contamination, as well as the decline of oxidation rates caused by the accumulation of sludge (Niu et al., 2012). Recently, biological degradation of indole has been investigated and discussed for their eco-friendly (Chen et al., 2013; Meng et al., 2013; Yuan et al., 2011; Gu et al., 2019; Ma et al., 2019), but there is a great inhibition on the performance of the biological treatment method, resulting from relatively high chemical oxygen demand (COD) in the effluents (Li et al., 2001). Microbial fuel cell (MFC) is a potentially effective approach for the simultaneous production of energy and degradation of refractory organics including indole in wastewater based on the conversion of chemical energy into electrical energy using microbial as catalysts (Logan et al., 2006). However, it is difficult for microorganisms on the anode to resist the toxicity of a harsh environment with a high content of indole. Luo et al. (2010) found that using a mixture of 250 mg L−1 indole and 1000 mg L−1 glucose as the fuel in MFC, a maximum voltage of 660 mV and a maximum power density of 51.2 W·m−3 were obtained with the mixture by the MFC. Moreover, when 250 mg L−1 indole was used in the MFC as the carbon source, the output voltage and power density dropped sharply to 220 mV and 3.3 W·m−3 respectively. Because the characteristics of anode could directly affect the biofilm formation and electricity generation, one of the key factors affecting the electrochemical efficiency and commercial application of MFC to degrade refractory organic compounds is the design of anode materials with the excellent performance (De Coster et al., 2017). It has been widely recognized that a high-performance anode material of MFC should be easy for microbial adhesion and highly conductive to facilitate electron transfer from microorganisms to the anode (Du et al., 2017; Sonawane et al., 2017). In the past decade, several carbon-based materials have been proposed and researched as the anode in MFC systems (Chou et al., 2014; Yuan and He, 2015; Sonawane et al., 2014). Among them, carbon felt (CF) has been acknowledged as a useful material for MFC construction because of its advantage of low cost, high surface area, corrosion-resistant, and excellent electrical conductivity (Wang et al., 2013). However, the hydrophobicity of carbon felt could reduce the adhesion of bacteria, which limits the power output and degradation performance of MFC. Some studies are devoted to improving it. Jiang et al. (2017) prepared a new anode using macroporous graphitic carbon foam, on which polydopamine was used as a coating material for increasing the bacterial adhesion capacity and improving the extracellular electron transfer efficiency on the anode. Huang et al. (Huang et al., 2016) combined polyaniline (PANI) with graphene to modify oxidized carbon cloth to solve the problem of low bioelectricity generation. The application of conductive coatings such as polyaniline and polypyrrole increased the life span of bacteria cells and improved the extracellular electron transfer efficiency (Guo et al., 2019; Song et al., 2017). Song et al. (Xie et al., 2016) coated the different individual bacterial cells by polypyrrole, it was found that all the as-coated cells displayed enhanced conductivity and long-time stability. Many investigations have been performed on PANI owing to its good electronic conduction and simple synthesis (Morrin et al., 2005). Nevertheless, PANI conducting polymer as a coating material has the disadvantages of poor stability, not easy processing and insolubility (Iqbal and Ahmad, 2018). To overcome the above shortcomings, aniline and dopamine have been crosslinked to form the PDHC membrane on CF in-situ based
2. Experimental section 2.1. Materials Indole was obtained from Sigma-Aldrich Industrial Corporation (USA). FeSO4·7H2O and Hexadecyl trimethyl ammonium bromide (CTAB, C19H42BrN, 99 %) were provided by Sinopharm Chemical Reagent Co., Ltd. (China) and Shanghai Macklin Biochemical Co., Ltd. (China), respectively. Aniline and dopamine hydrochloride (98 wt%) were purchased from Adamas Reagent Co., Ltd. (Switzerland) and Sigma-Aldrich Industrial Corporation (USA), respectively. All the reagents were analytical grade unless otherwise stated and were used without further purification. Carbon felt (thickness of 0.5 cm) was prepared from Beijing Sanye Carbon Co., Ltd. Nafion 117 used as a proton exchange membrane was obtained from Shanghai hesen electric Co., Ltd. 2.2. Instruments The surface morphologies of the samples were characterized using a JSM-7500 scanning electron microscope (Rigaku Co.). The voltage data were collected by a data collector (1608FS-Plus, Measurement computing, USA). Cyclic voltammetry (CV) and electrochemical impedance spectroscopy analysis of the MFC were conducted with an electrochemical station (CHI760E, Chenhua Instrument Co., Ltd, China). The concentration of indole was determined by monitoring the absorbance of the supernatant at 250 nm with HPLC (Agilent 1100 series, Agilent, Waldbronn, Germany). 2.3. Preparation of modified CF anode The supporting material CF was cut into small pieces with a size of 4 cm × 4 cm × 0.5 cm and soaked in a 1000 mL beaker of anhydrous ethanol and 0.1 mol·L−1 HCl solution sequentially to remove impurities. Under the water bath at 100 ℃ for 30 min, the purified CF was dried at 80 ℃ for 12 h. The polyaniline-dopamine composite membrane was electropolymerized in the electrolyte of 2 mol·L−1 aniline, 1 mol·L−1 dopamine hydrochloride, and 0.5 mol·L−1 H2SO4 (50 mL) solution, which was injected with nitrogen at a flow rate of 40 mL·min−1 for 15 min. Cyclic voltammetry measurement was performed using a three-electrode system (Wu et al., 2013), in which the CF strung with platinum wire was used as a working electrode, the platinum electrode was used as a counter electrode, and the saturated 2
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2.6. Analytical methods
calomel electrode (SCE) was used as a reference electrode. Under 0.1 mol ammonium persulfate was added as the initiator, CV was operated using an electrochemical station in the potential ranged from 0.7 V to −0.1 V at a scanning rate of 0.1 V·s−1 for 150 scanning cycles. Then the PDHC/CF was obtained by drying in a vacuum oven at 60 ℃ for 10 h to remove the solvent. As both a reductant and a solvent, 4 mL glycerol was added dropwise into a 100 mL three-necked flask, in which 1.5 mmol FeSO4·7H2O and 0.3 mmol CTAB pre-dissolved in 60 mL distilled water was added in the flask. After homogenized by vigorous stirring for 30 min in 50 °C water bath, the mixture was transferred into a 100 mL sealed Teflon autoclave to heat to 145 °C for 8 h in an electric oven. After cooled to room temperature, the resulting precipitate was centrifuged and washed with distilled water and ethanol several times, respectively. Finally, the powder of the product was freeze-dried for 12 h. The preparation of the novel composite anode was done by CV on the electrochemical workstation in a three-electrode arrangement, using the PDHC/CF (4 cm × 4 cm) as the working electrode, a platinum counter electrode, and a saturated calomel electrode reference electrode. 96 mg as-prepared Fe2O3 was ground into a powder and added into the electrolyte of 50 mmol/L PBS (50 mL) solution. CV measurement was operated as pre-deposition in the potential ranged between −0.7 V and 0.7 V at a scan rate of 0.02 V·s−1 for 10 min, then the constant potential was kept at −1.4 V for 10 min. The prepared carbon felt anode modified with Fe2O3-polyaniline-dopamine hybrid composite was denoted as Fe2O3-PDHC/CF.
All the electrical analytical tests were conducted after three months of operation. CV measurements were carried out using a three-electrode electrochemical model in MFC reactors at a scan rate of 0.1 V·s−1. The Fe2O3-PDHC/CF and CF anodes were served as the working electrode respectively. Cathode acted as a counter electrode, and SCE was used as a reference electrode. Electrochemical impedance spectroscopy (EIS) was carried out over a wide frequency range from 10 kHz to 0.1 Hz with an AC perturbation of 5 mV. The as-prepared anodes were acted as the working electrode, while an Ag/AgCl electrode and cathode of MFC were used as reference and counter electrode, respectively. Each resistance was obtained using ZsimpWin software. Anodic biofilm was scraped after three months of operation. The Fe2O3-PDHC/CF anode was cut into pieces and microbe biofilm on the anode was carefully scraped. DNA of bacteria was extracted by using E.Z.N.A™ Mag-Bind Soil DNA Kit (Omega Biotech Co. Ltd., USA) per the operating instruction. The V3 region of 16S rDNA was amplified with the 341–534 primer set (F: CCTACGGGAGGCAGCAG, R: ATTACCGCG GCTGCTGG). The amplicons were then sequenced using the Illumina MiSeq sequencing platform in Sangon Biotech (Shanghai, China). The sequencing data were processed and analyzed using the QIIME pipeline. R language was used for visualization of the results and statistical tests. 3. Results and discussion 3.1. Design and characterization of anodes
2.4. Construction and operation of MFC The anode plays a dual functional role in MFC where microorganisms will grow and multiply and electrons will transfer outward. Different anode materials directly affect the output power density of MFC. Therefore, the selection and preparation of anode materials are crucially important for designing high-performance MFC. The preparation of the Fe2O3-PDHC/CF anode material is shown in Scheme 1. The electrochemically synthesized polyaniline-dopamine membrane has played a crucial role in the deposition of Fe2O3 for it provides sufficient active sites and improves the hydrophilic of the CF surface. Fe2O3 particles which are applied to accelerate the extracellular electron transfer combinate with PANI-DA by CV method. The Fe2O3PDHC/CF material is beneficial to the attachment, growth and reproduction, and electron transfer outward of electrogenic bacteria. The scanning electron microscopy (SEM) images of CF and Fe2O3PDHC/CF anodes before inoculation were shown in Fig. 1a and b. Fig. 1c was the SEM image of Fe2O3-PDHC/CF under high magnification. As shown in Fig. 1a, the surface of CF fiber was not rough, while the surface roughness of Fe2O3-PDHC/CF anode was further increased (Fig. 1b), which made the specific area of the modified anode enlarged. Partial polymer film connected between the carbon felt fibers also increased the surface area of the surface-treated anode. The combination of Fe2O3 particles and the PDHC film might be due to the binding force of abundant catechol, amino, and imido groups of the polymer chain. After bacterial colonization, a piece of the anode was sacrificed for SEM imaging. Attachment of clubbed bacterial cells on the surface of various anodes was shown in Fig. 1 (d–f). Distinct to the bare CF anode with only a few bacterial cells on its surface (Fig. 1d), the biofilm on the Fe2O3-PDHC/CF anode was much thicker and larger in the area (Fig. 1e), which attributed to the hydrophilic functional groups of PANI-DA. It was consistent with Palacios-Cuesta’s experimental result that the affinity between the bacteria and the surface could be modulated by incorporate hydrophilic functional groups (Zhao et al., 2013). The improved biocompatibility of the anode was beneficial to the firm adhesion of bacterial cells on its surface and the improvement of direct electron transfer from microbial to the anode via outer membrane ctype cytochromes (Zhao et al., 2015b). In addition to the fact that Fe2O3-PDHC/CF anode exhibited a higher bacterial loading than CF anode, a large number of bacterial cells could also be observed in the
Different anodes with an effective area of 1 cm2 (1 cm × 1 cm) and the same CF cathodes (4 cm × 4 cm) were assembled to the doublechamber MFC made of Plexiglas as MFC reactors. All MFC reactors were composed of an anode chamber (5 cm × 4 cm × 6 cm, net volume 120 mL), a cathode chamber (5 cm × 6 cm × 6 cm, net volume 180 mL) and a proton exchange membrane (PEM) which was pretreated by H2O2 (5 %) and H2SO4 (5 %) in turn. The anode nutrient solution consisted of 200 mg L−1 indole, 0.13 g·L−1 KCl, 0.31 g·L−1 NH4Cl, 3.32 g·L−1 NaH2PO4·2H2O, and 10.32 g·L−1 Na2HPO4·12H2O. N2 was constantly aerated in the anode chamber for about 10 min to remove the dissolved oxygen. Catholyte consists of 18.65 g·L−1 K3Fe(CN)6, 200 mg L−1 indole, 0.13 g·L−1 KCl, 0.31 g·L−1 NH4Cl, 3.32 g·L−1 NaH2PO4·2H2O, and 10.32 g·L−1 Na2HPO4·12H2O. 30 mL anodic bacteria inoculation fluid which had been cultivated for 2 months in a growth medium composed of 200 mg L−1 indole and 50 mmol·L−1 PBS was added in both of the chambers of the MFC reactor. All reactors were operated with an external load of 1000 Ω in a constant temperature incubator at 30 ± 1 ℃, and the voltage was self-recording with a data acquisition system every 10 min. Two parallel reactors were constructed for each anode including the plain carbon felt anode used for blank as duplicate tests. 2.5. Indole degradation and performance of MFC The MFC as described above was constructed and operated for more than three months. The sample was taken from the MFC reactor every 6 h and centrifuged at 10,000 r/min for 10 min to determine indole concentration in the supernatant. Polarization curves and the maximum power density were obtained by varying the external resistance from 1000 Ω to 100 Ω, and the corresponding voltage was recorded with a 30 min interval time by an exquisite multimeter. The current density was calculated using the equation: j = E/(R·AAn), where j (A·m−2) was the current density, E (V) was the voltage, R (Ω) was the load resistance, and AAn (m2) was the active area of the anode. From this, the power density of the MFC by taking the product of the voltage and current were calculated by the equation: P = j·E (Palacios-Cuesta et al., 2015). Both the current and power densities were normalized to the anode surface area of 1 cm2. 3
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Scheme 1. Schematic of the fabrication of the Fe2O3-PDHC/CF anode.
interior of the fibers, indicating that the microbe loading capacity was increased. The increased bacterial loading mass on the anode could improve the extracellular electron transfer efficiency between the microbial and the modified CF anode through intimate contact (Saratale et al., 2017). It was interesting to note that some Fe2O3 particles were encased in the bacterial membrane and the biofilms bind to them tightly were significantly thicker, with remarkably increased microbes loading around them (Fig. 1f). The images revealed that the presence of Fe2O3 introduced onto the surface of CF modified with polyanilinedopamine film could promote the formation of electroactive biofilms, and more microorganisms could be adsorbed on the anode, which acted
as a biocatalyst to hydrolyze the substrate to produce more protons and electrons in MFC (Xue et al., 2019). Therefore, the MFC loading Fe2O3PDHC/CF anode was expected to exhibit a higher degradation efficiency of indole and electricity generation performance.
3.2. Bacterial community To evaluate the microbial community richness and species diversity in the MFC loading Fe2O3-PDHC/CF anode in indole solution, 50 of the most abundant genera were constructed in a heatmap, in which intuitionistic relative abundance could be shown. In terms of the
Fig. 1. SEM images of anodes before inoculation (a, bare CF; b, Fe2O3-PDHC/CF; c, Fe2O3-PDHC/CF with high magnification) and after running (d, bare CF; e, Fe2O3PDHC/CF; f, Fe2O3-PDHC/CF with high magnification). 4
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Fig. 2. A tree diagram of the classification system of the microbial sample on Fe2O3-PDHC/CF anode at the genus level. Different colors represented different taxonomic levels, which were in order from left to right. The size of the circle represented species abundance, and near the fulcrum were the taxonomic name and its corresponding abundance value respectively. On the far right was the distribution of species in the top 30 abundance.
degrade large amounts of indole to nutrients. It was the direct factor to improve the electrical performance and indole degradation efficiency of the anode. So far, the MFC reactor loading the Fe2O3-PDHC/CF anode has operated over 18 months holding good performance and the microorganisms inside did not show observable decay.
microbial structure, the dominant phyla identified in the sample were Proteobacteria accounting for 93.4 % (Fig. 2), including Alcaligenes, Achrombacter and other electroactive bacteria. According to the detailed composition of the biofilm at the genus level showed in Fig. 3, the biofilms were dominated by Alcaligenes (63.3 %), which played a particularly important role in extracellular electron transfer (Chen et al., 2017). Besides, it was regarded to be associated with the oxidation of substrate via cometabolism and possessed the ability to resist the toxicity of indole, which might be the main reason for its predominance in the sample. Different from the literature (Ren et al., 2011), there were only a small number of other electricity-producing bacteria such as Delftia (2.48 %) and Pseudomonas (0.37 %), indicating that the impact of indole addition on species except the Proteobacteria phylum was detrimental and Achromobacter had a strong ability to degrade indole. The novel composite anode Fe2O3-PDHC/CF was beneficial to the enrichment, growth, and reproduction of microorganisms that could resist the toxicity of indole by rapid electroactive biofilms formation and
3.3. Electricity generation performance of MFC To assess the electricity generation properties of the novel anode, Fe2O3-PDHC/CF anode was applied in MFC, and the initial concentration of indole acolyte was set to be 200 mg L−1. CF anode was used for performance comparison. Two of the MFC reactors were tested at an external resistance of 1000 Ω. The start-up profiles of the two MFC reactors were shown in Fig. 4, exhibiting that the start-up time of the MFC loading surface-treated anode was shorter than the MFC containing unmodified CF anode. It decreased by 57.9 % from 76 h (CF) to 32 h (Table 1). The shortened start-up time meant that the growth 5
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Fig. 3. Hierarchical cluster analysis of microbial communities on Fe2O3-PDHC/CF anode at the genus level. The species clustering tree was on the left. Table 1 Performance of MFC reactors using different anodes. Anode
t (h)
Vmax (mV)
Pmax (mW·m−2)
Indole degradation efficiency (%)
CF Fe2O3-PDHC/ CF
44 32
443 ± 22 632 ± 39
1498.0 ± 26 3184.4 ± 45
44.0 90.3
process of bacteria from the logarithmic growth phase to the quiescent growth phase could be accelerated by modification of anode. Moreover, the profiles of output voltages shown in Fig. 4 also suggested that MFC containing modified anode prepared by CV and electrochemical deposition ran for a longer cycle. The results above could be attributed to the admirable biological compatibility of the PDHC membrane and the sharp increase of the specific surface area of anode material, which promoted the formation of the electroactive biofilms and improved the electrical properties of MFC. As shown in Figs. 4 and 5, the highest output voltage and the maximum power density of the MFC loading the Fe2O3-PDHC/CF anode
Fig. 4. Profiles of outputted cell voltages in MFC using different anodes during operation.
6
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Fig. 5. Polarization and power density curves as a function of current density for MFC operated using different anodes.
Fig. 7. The Nyquist curves of MFC equipped with different anodes in indole degradation.
reached 632 ± 39 mV and 3184.4 ± 45 mW·m−2 respectively, 43 % and 113 % higher than that of the MFC loading CF anode of 443 ± 22 mV and 1498.0 ± 26 mW·m−2 (Table 1). The present result should be attributed to the Fe2O3 deposited on the PDHC membrane made up for the defect of dopamine such as limited electrical conductivity and poor stability in strongly polar organic solvents (Li et al., 2016). Therefore, the electron transfer of the anode was enhanced and the electrical performance of the MFC was improved.
a remarkable decrease in the resistance of MFC reactors whose anodes were treated by electro-polymerization, for both of the Rct and the Rs of Fe2O3-PDHC/CF anode were lower than the CF anode. The values of Rs for CF and Fe2O3-PDHC/CF anodes were estimated to be 65.4 Ω and 27.3 Ω, respectively. Besides, the Fe2O3-PDHC/CF anode exhibited an Rct of 57.1 Ω, which was 100.7 % lower than the CF anode (114.6 Ω). It was suggested that the lower total internal resistance of the Fe2O3PDHC/CF anode was attributed to the synergistic effect between Fe2O3 and polyaniline-dopamine, which could accelerate the extracellular electron transfer between the modified anode and the bacterial biofilm. Moreover, the increase of the specific surface area of the Fe2O3-PDHC/ CF anode had a considerable effect on the internal resistance decrease and the Pmax increase (Hernández-Flores et al., 2015b). As a result, the maximum power density of the MFC loading modified anode was far higher than that loading the bare CF anode.
3.4. Electrochemical tests The electrochemical properties of the anodes were assessed further using cyclic voltammetry and electrochemical impedance spectroscopy. Cyclic voltammograms of the anodes in 0.1 mol·L−1 PBS were shown in Fig. 6. It was observed that the cyclic voltammogram of the Fe2O3PDHC/CF anode showed a large peak area and significant peak current of oxidation and reduction. This meant that the Fe2O3-PDHC/CF anode had greater electrical activity and larger electrochemical activity surface area. It was generally believed that electron conversion occurs through the bacterial biofilm anode, and stronger biofilm generated higher current (Franks et al., 2010; He and Mansfeld, 2009). On the other hand, the CF anode with poor biological compatibility revealed an inconspicuous redox activity. The electrochemical behavior of anode materials was examined by electrochemical impedance spectroscopy analysis. As shown in Fig. 7, the EIS data fitted as well-defined single semicircles over the high-frequency region represented solution resistance (Rs) (Hernández-Flores et al., 2015a). The charge-transfer resistance (Rct) was calculated by the semicircle fit in the Nyquist curve. The results indicated that there was
3.5. Degradation of indole The degradation of MFC versus time was shown in Fig. 8. After about 40 h of growth, the degradation efficiency of indole speeded up due to the stable formation of biofilms and the entry of microorganisms into the logarithmic growth period. In a period of 120 h, the maximum degradation of the MFC loading Fe2O3-PDHC/CF anode reached about 90.3 %, while that of the CF-MFC was 44.0 % barely (Table 1). These results revealed that the adhesion and growth of microorganisms that were conducive to indole degradation could be effectively improved by the Fe2O3-PDHC/CF synthesized through the electrochemical method, for the reason that the indole degradation efficiency of the MFC loading surface-treated anode was higher than that of plain CF. Furthermore,
Fig. 6. Cyclic voltammetry curves of different anodes in anolyte with a scanning rate of 0.1 V·s−1.
Fig. 8. Indole degradation using MFC equipped with different anodes. 7
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the combination of the Fe2O3 and polyaniline-dopamine made the composite anode possess the synergistic effect which facilitated the biocompatibility and charge transfer of the modified anode, so the indole degradation and bioelectricity generation of the MFC were both improved compared with that of the CF-MFC.
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Phys. 15, 5867–5872. Jiang, H.M., Yang, L., Deng, W.F., Tan, Y.M., Xie, Q.J., 2017. Macroporous graphitic carbon foam decorated with polydopamine as a high-performance anode for microbial fuel cell. J. Power Sources 363, 27–33. Huang, L.H., Li, X.F., Ren, Y.P., Wang, X.H., 2016. In-situ modified carbon cloth with polyaniline/graphene as anode to enhance performance of microbial fuel cell. Int. J. Hydrogen Energy 41, 11369–11379. Guo, D., Wei, H.F., Song, R.B., Fu, J.J., Lu, X.Z., Jelinek, R., Min, Q.H., Zhang, J.R., Zhang, Q.C., Zhu, J.J., 2019. N, S-doped carbon dots as dual-functional modifiers to boost bio-electricity generation of individually-modified bacterial cells. Nano Energy 63, 103875. Song, R.B., Wu, Y.C., Lin, Z.Q., Xie, J., Tan, C.H., Loo, J.S.C., Cao, B., Zhang, J.R., Zhu, J.J., Zhang, Q.C., 2017. Living and conducting: coating individual bacterial cells with in situ formed polypyrrole. Angew. Chem. Int. Ed. 56, 10516–10520. Xie, J., Zhao, C.E., Lin, Z.Q., Gu, P.Y., Zhang, Q.C., 2016. Nanostructured conjugated polymers for energy-related applications beyond solar cells. Chem. Asian J. 11, 1489–1511. Morrin, A., Wilbeer, F., Ngamna, O., Moulton, S.E., Killard, A.J., Wallace, G.G., Smyth, M.R., 2005. Novel biosensor fabrication methodology based on processable conducting polyaniline nanoparticles. Electrochem. commun. 7, 317–322. Iqbal, S., Ahmad, S., 2018. Recent development in hybrid conducting polymers: synthesis, applications and future prospects. J. Ind. Eng. Chem. 60, 53–84. Li, S.S., Li, W.J., Jiang, T.J., Liu, Z.G., Chen, X., Cong, H.P., Liu, J.H., Huang, Y.Y., Li, L.N., Huang, X.J., 2016. Iron oxide with different crystal phases (α- and γ‑Fe2O3) in electroanalysis and ultrasensitive and selective detection of lead (II): an advancing approach using XPS and EXAFS. Anal. Chem. 88, 906–914. Li, M., Zhou, S.Q., 2018. α-Fe2O3/polyaniline nanocomposites as an effective catalyst for improving the electrochemical performance of microbial fuel cell. Chem. Eng. J. 339, 539–546. Sun, D.Z., Yu, Y.Y., Xie, R.R., Zhang, C.L., Yang, Y., Zhai, D.D., Yang, G.D., Liu, L., Yong, Y.C., 2017. In-situ growth of graphene/polyaniline for synergistic improvement of extracellular electron transfer in bioelectrochemical systems. Biosens. Bioelectron. 87, 195–202.
4. Conclusion In conclusion, a novel Fe2O3-PDHC/CF anode has been prepared via cyclic voltammetry and electrochemical deposition. By depositing the high conductive Fe2O3 onto the hydrophilic and biocompatible polyaniline-dopamine membrane, the resistance of the anode was effectively reduced due to the accelerated extracellular electron transfer between bacteria and anode. Furthermore, the modified anode material was conducive to the adsorption of microorganisms and the rapid formation of electroactive biofilms which were benefit for bioelectricity generation and the indole removal capacity of MFC. Additionally, Proteobacteria phylum which degraded indole into nutrients could be enriched by the composite anode. 90.3 % of indole was degraded in 120 h by the MFC loading Fe2O3-PDHC/CF anode, and the maximum power density of which was as high as 3184.4 mW·m−2, which was amongst the highest values reported for MFC of indole anolyte. Therefore, the modification strategy of Fe2O3-PDHC/CF anode could be a promising candidate for the degradation of refractory organic pollutants in water by MFC. CRediT authorship contribution statement Minjie Jian: Conceptualization, Methodology, Formal analysis, Writing - original draft. Ping Xue: Validation, Resources, Writing review & editing. Keren Shi: Visualization. Rui Li: Supervision, Writing - review & editing. Lan Ma: Investigation, Writing - review & editing. Peng Li: Writing - review & editing. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The authors sincerely acknowledge the financial support from the National Natural Science Foundation of China (No. 21961028) and the Science and Technology Support Program of Ningxia Province of China (NX 2015076). References Katapodis, P., Moukouli, M., Christakopoulos, P., 2007. Biodegradation of indole at high concentration by persolvent fermentation with the thermophilic fungus Sporotrichum thermophile. Int. Biodeterior. Biodegrad. 60, 267–272. Joshi, D.R., Zhang, Y., Zhang, H., Gao, Y.X., Yang, M., 2017. Characteristics of microbial community functional structure of a biological coking wastewater treatment system. J. Environ. Sci. 63, 105–115. Li, G.H., Nandgaonkar, A.G., Wang, Q.Q., Zhang, J.N., Krause, W.E., Wei, Q.F., Lucia, L.A., 2017. Laccase-immobilized bacterial cellulose/TiO2functionalized composite membranes: evaluation for photo- and bio-catalytic dye degradation. J. Membrane Sci. 525, 89–98. Shi, J.X., Han, Y.X., Xu, C.Y., Han, H.J., 2019. Anaerobic bioaugmentation hydrolysis of selected nitrogen heterocyclic compound in coal gasification wastewater. Bioresour. Technol. 278, 223–230. Arora, P.K., Bae, H.H., 2014. Identification of new metabolites of bacterial transformation of indole by gas chromatography–mass spectrometry and high-performance liquid chromatography. Int. J. Anal. Chem. 4, 1–5. Qu, Y.Y., Xu, B.W., Zhang, X.W., Ma, Q., Zhou, H., Kong, C.L., Zhang, Z.J., Zhou, J.T., 2013. Biotransformation of indole by whole cells of recombinant biphenyl dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase. Biochem. Eng. J. 72, 54–60. Carlson, J.R., Yokoyama, M.T., Dickinson, E.O., 1972. Induction of pulmonary edema and emphysema in cattle and goats with 3-methylindole. Science 176, 298–299.
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Chen, J.F., Zhang, L.H., Hu, Y.Y., Huang, W.T., Niu, Z.Y., Sun, J., 2017. Bacterial community shift and incurred performance in response to in situ microbial self-assembly graphene and polarity reversion in microbial fuel cell. Bioresour. Technol. 242, 220–227. Ren, Z.Y., Ramasamy, R.P., Cloud-Owen, S.R., Yan, H.J., Mench, M.M., Regan, J.M., 2011. Time-course correlation of biofilm properties and electrochemical performance in single-chamber microbial fuel cells. Bioresour. Technol. 102, 416–421. Franks, A.E., Malvankar, N., Nevin, K.P., 2010. Bacterial biofilms: the powerhouse of a microbial fuel cell. Biofuels 1, 589–604. He, Z., Mansfeld, F., 2009. Exploring the use of electrochemical impedance spectroscopy (EIS) in microbial fuel cell studies. Energy Environ. Sci. 2, 215–219. Hernández-Flores, G., Poggi-Varaldo, H.M., Solorza-Feria, O., Ponce Noyola, M.T., Romero-Castañón, T., Rinderknecht-Seijas, N., 2015a. Tafel equation based model for the performance of a microbial fuel cell. Int. J. Hydrogen Energy 41, 17421–17432. Hernández-Flores, G., Poggi-Varaldo, H.M., Solorza-Feria, O., Ponce Noyola, M.T., Romero-Castañón, T., Rinderknecht-Seijas, N., 2015b. Tafel equation based model for the performance of a microbial fuel cell. Int. J. Hydrogen Energy 41, 17421–17432.
Wu, Y.L., Zhang, X.L., Li, S.H., Lv, X.Y., Cheng, Y., Wang, X.M., 2013. Microbial biofuel cell operating effectively through carbon nanotube blended with gold-titania nanocomposites modified electrode. Electrochim. Acta 109, 328–332. Palacios-Cuesta, M., Cortajarena, A.L., Garcia, O., Rodriguez-Hernandez, J., 2015. Patterning of individual Staphylococcus aureus bacteria onto photogenerated polymeric surface structures. Polym. Chem. 6, 2677–2684. Zhao, C., Gai, P.P., Liu, C.H., Wang, X., Xu, H., Zhang, J.R., Zhu, J.J., 2013. Polyaniline networks grown on graphene nanoribbons-coated carbon paper with a synergistic effect for high-performance microbial fuel cells. J. Mater. Chem. A 1, 12587–12594. Zhao, C.E., Wu, J.S., Kjelleberg, S., Loo, J.S.C., Zhang, Q.C., 2015b. Employing a flexible and low-cost polypyrrole nanotube membrane as an anode to enhance current generation in Microbial Fuel Cells. Small 11, 3440–3443. Saratale, G.D., Saratale, R.G., Shahid, M.K., Zhen, G.Y., 2017. A comprehensive overview on electro-active biofilms, role of exoelectrogens and their niches in microbial fuel cells (MFCs). Chemosphere 178, 534–547. Xue, W.D., Li, F.X., Zhou, Q.X., 2019. Degradation mechanisms of sulfamethoxazole and its induction of bacterial community changes and antibiotic resistance genes in a microbial fuel cell. Bioresour. Technol. 289, 121632.
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Journal of Hazardous Materials journal homepage: www.elsevier.com/locate/jhazmat
Efficient degradation of indole by microbial fuel cell based Fe2O3polyaniline-dopamine hybrid composite modified carbon felt anode
T
Minjie Jiana,b, Ping Xuea,*, Keren Shia, Rui Lia, Lan Maa, Peng Lia a b
National Key Laboratory of High-efficiency Utilization of Coal and Green Chemical Engineering, Ningxia University, Yinchuan, 750021, PR China Ningxia Academy of Metrology & Quality Inspection, Yinchuan, 750200, PR China
G R A P H I C A L A B S T R A C T
A R T I C LE I N FO
A B S T R A C T
Editor: G. Lyberatos
Indole is a high-toxic refractory nitrogen-containing compound that could cause serious harm to the human and ecosystem. It has been a challenge to develop economical and efficient technology for degrading indole. Microbial fuel cell (MFC) has great potential in the removal of organic pollutants utilizing microorganisms as catalysts to degrade organic matter into the nutrients. Herein, a novel anode of Fe2O3-polyaniline-dopamine hybrid composite modified carbon felt (Fe2O3-PDHC/CF) was prepared by electrochemical deposition. The degradation efficiency of indole by the MFC loading Fe2O3-PDHC/CF anode was up to 90.3 % in 120 h operation, while that of the MFC loading CF anode was only 44.0 %. The maximum power density of the MFC loading Fe2O3-PDHC/CF anode was 3184.4 mW·m−2, increasing 113 % compared to the MFC loading CF anode. The superior performances of the MFC with Fe2O3-PDHC surface-modified anode owned to the synergistic effect of high conductive Fe2O3 and admirably biocompatible polyaniline-dopamine. MFC with the Fe2O3-PDHC/CF anode could produce considerable electricity and effectively degrade indole in water, which demonstrated a practical approach for the efficient degradation of refractory organic compounds in wastewater.
Keywords: Indole degradation Modified carbon felt anode Fe2O3-polyaniline-dopamine hybrid composite Microbial fuel cell
1. Introduction Indole is well-known for its extensive application in agrochemical, pesticide, cosmetic, dyestuff and medicine due to its unique biological
⁎
properties (Katapodis et al., 2007). Unfortunately, the considerable expansion of these industries has undesirable effects, large amounts of carcinogenic and teratogenic indole are released into coking, pesticide, pharmaceutical, dyestuff, and coal gasification wastewater to bring
Corresponding author. E-mail address: [email protected] (P. Xue).
https://doi.org/10.1016/j.jhazmat.2020.122123 Received 19 November 2019; Received in revised form 14 January 2020; Accepted 15 January 2020 Available online 16 January 2020 0304-3894/ © 2020 Published by Elsevier B.V.
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on hybrid conducting polymer, or even interpenetrating polymer network (Li et al., 2016). Nowadays, Fe2O3 particles have attracted much more attention of scholars as the modification material for anode of MFC due to their unique advantages such as considerable electrocatalysis, chemical stability and low cost (Li and Zhou, 2018; Sun et al., 2017). However, it is difficult for Fe2O3 particles to attach directly to the electrode. The hybrid of inorganic Fe2O3 with organic polymer will be benefit to overcome its defect and improve the electrochemical property. So far as we know, there is no literature report on the performance of Fe2O3-polyaniline-dopamine hybrid composite modified anode in MFC. The objectives of this work were to degrade indole efficiently, to enhance power generation, and to accelerate electrogenic bacteria growth. In our study, a novel MFC anode material was obtained by modifying the CF anode in-situ with the polyaniline-dopamine membrane deposited Fe2O3 particles. The synergistic effect of Fe2O3 particles and polyaniline-dopamine membrane on improving the electrochemical activity and power generation performance of the MFC loading the modified CF anode was discussed. Compared with the MFC loading the bare CF anode, the indole degradation efficiency and electrochemical performances of that loading the modified CF anode have been enhanced significantly. Besides, the bacterial community on the modified CF anode of indole anolyte was analyzed.
about unpleasant odor and environment pressures, which greatly restricts the development of these industries (Joshi et al., 2017; Li et al., 2017; Shi et al., 2019). Furthermore, high concentrations of indole may cause damages to human and animal lung cells and hemocytes (Arora and Bae, 2014; Qu et al., 2013; Carlson et al., 1972). Many treatment technologies have been studied for treating indole-containing wastewater, such as physical adsorption and chemical oxidation technologies (Zhao et al., 2015a; Cao et al., 2014; Antonopoulou et al., 2014). Although they are widely used to remove indole from wastewater currently, their application has been limited by low removal efficiency and serious secondary contamination, as well as the decline of oxidation rates caused by the accumulation of sludge (Niu et al., 2012). Recently, biological degradation of indole has been investigated and discussed for their eco-friendly (Chen et al., 2013; Meng et al., 2013; Yuan et al., 2011; Gu et al., 2019; Ma et al., 2019), but there is a great inhibition on the performance of the biological treatment method, resulting from relatively high chemical oxygen demand (COD) in the effluents (Li et al., 2001). Microbial fuel cell (MFC) is a potentially effective approach for the simultaneous production of energy and degradation of refractory organics including indole in wastewater based on the conversion of chemical energy into electrical energy using microbial as catalysts (Logan et al., 2006). However, it is difficult for microorganisms on the anode to resist the toxicity of a harsh environment with a high content of indole. Luo et al. (2010) found that using a mixture of 250 mg L−1 indole and 1000 mg L−1 glucose as the fuel in MFC, a maximum voltage of 660 mV and a maximum power density of 51.2 W·m−3 were obtained with the mixture by the MFC. Moreover, when 250 mg L−1 indole was used in the MFC as the carbon source, the output voltage and power density dropped sharply to 220 mV and 3.3 W·m−3 respectively. Because the characteristics of anode could directly affect the biofilm formation and electricity generation, one of the key factors affecting the electrochemical efficiency and commercial application of MFC to degrade refractory organic compounds is the design of anode materials with the excellent performance (De Coster et al., 2017). It has been widely recognized that a high-performance anode material of MFC should be easy for microbial adhesion and highly conductive to facilitate electron transfer from microorganisms to the anode (Du et al., 2017; Sonawane et al., 2017). In the past decade, several carbon-based materials have been proposed and researched as the anode in MFC systems (Chou et al., 2014; Yuan and He, 2015; Sonawane et al., 2014). Among them, carbon felt (CF) has been acknowledged as a useful material for MFC construction because of its advantage of low cost, high surface area, corrosion-resistant, and excellent electrical conductivity (Wang et al., 2013). However, the hydrophobicity of carbon felt could reduce the adhesion of bacteria, which limits the power output and degradation performance of MFC. Some studies are devoted to improving it. Jiang et al. (2017) prepared a new anode using macroporous graphitic carbon foam, on which polydopamine was used as a coating material for increasing the bacterial adhesion capacity and improving the extracellular electron transfer efficiency on the anode. Huang et al. (Huang et al., 2016) combined polyaniline (PANI) with graphene to modify oxidized carbon cloth to solve the problem of low bioelectricity generation. The application of conductive coatings such as polyaniline and polypyrrole increased the life span of bacteria cells and improved the extracellular electron transfer efficiency (Guo et al., 2019; Song et al., 2017). Song et al. (Xie et al., 2016) coated the different individual bacterial cells by polypyrrole, it was found that all the as-coated cells displayed enhanced conductivity and long-time stability. Many investigations have been performed on PANI owing to its good electronic conduction and simple synthesis (Morrin et al., 2005). Nevertheless, PANI conducting polymer as a coating material has the disadvantages of poor stability, not easy processing and insolubility (Iqbal and Ahmad, 2018). To overcome the above shortcomings, aniline and dopamine have been crosslinked to form the PDHC membrane on CF in-situ based
2. Experimental section 2.1. Materials Indole was obtained from Sigma-Aldrich Industrial Corporation (USA). FeSO4·7H2O and Hexadecyl trimethyl ammonium bromide (CTAB, C19H42BrN, 99 %) were provided by Sinopharm Chemical Reagent Co., Ltd. (China) and Shanghai Macklin Biochemical Co., Ltd. (China), respectively. Aniline and dopamine hydrochloride (98 wt%) were purchased from Adamas Reagent Co., Ltd. (Switzerland) and Sigma-Aldrich Industrial Corporation (USA), respectively. All the reagents were analytical grade unless otherwise stated and were used without further purification. Carbon felt (thickness of 0.5 cm) was prepared from Beijing Sanye Carbon Co., Ltd. Nafion 117 used as a proton exchange membrane was obtained from Shanghai hesen electric Co., Ltd. 2.2. Instruments The surface morphologies of the samples were characterized using a JSM-7500 scanning electron microscope (Rigaku Co.). The voltage data were collected by a data collector (1608FS-Plus, Measurement computing, USA). Cyclic voltammetry (CV) and electrochemical impedance spectroscopy analysis of the MFC were conducted with an electrochemical station (CHI760E, Chenhua Instrument Co., Ltd, China). The concentration of indole was determined by monitoring the absorbance of the supernatant at 250 nm with HPLC (Agilent 1100 series, Agilent, Waldbronn, Germany). 2.3. Preparation of modified CF anode The supporting material CF was cut into small pieces with a size of 4 cm × 4 cm × 0.5 cm and soaked in a 1000 mL beaker of anhydrous ethanol and 0.1 mol·L−1 HCl solution sequentially to remove impurities. Under the water bath at 100 ℃ for 30 min, the purified CF was dried at 80 ℃ for 12 h. The polyaniline-dopamine composite membrane was electropolymerized in the electrolyte of 2 mol·L−1 aniline, 1 mol·L−1 dopamine hydrochloride, and 0.5 mol·L−1 H2SO4 (50 mL) solution, which was injected with nitrogen at a flow rate of 40 mL·min−1 for 15 min. Cyclic voltammetry measurement was performed using a three-electrode system (Wu et al., 2013), in which the CF strung with platinum wire was used as a working electrode, the platinum electrode was used as a counter electrode, and the saturated 2
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2.6. Analytical methods
calomel electrode (SCE) was used as a reference electrode. Under 0.1 mol ammonium persulfate was added as the initiator, CV was operated using an electrochemical station in the potential ranged from 0.7 V to −0.1 V at a scanning rate of 0.1 V·s−1 for 150 scanning cycles. Then the PDHC/CF was obtained by drying in a vacuum oven at 60 ℃ for 10 h to remove the solvent. As both a reductant and a solvent, 4 mL glycerol was added dropwise into a 100 mL three-necked flask, in which 1.5 mmol FeSO4·7H2O and 0.3 mmol CTAB pre-dissolved in 60 mL distilled water was added in the flask. After homogenized by vigorous stirring for 30 min in 50 °C water bath, the mixture was transferred into a 100 mL sealed Teflon autoclave to heat to 145 °C for 8 h in an electric oven. After cooled to room temperature, the resulting precipitate was centrifuged and washed with distilled water and ethanol several times, respectively. Finally, the powder of the product was freeze-dried for 12 h. The preparation of the novel composite anode was done by CV on the electrochemical workstation in a three-electrode arrangement, using the PDHC/CF (4 cm × 4 cm) as the working electrode, a platinum counter electrode, and a saturated calomel electrode reference electrode. 96 mg as-prepared Fe2O3 was ground into a powder and added into the electrolyte of 50 mmol/L PBS (50 mL) solution. CV measurement was operated as pre-deposition in the potential ranged between −0.7 V and 0.7 V at a scan rate of 0.02 V·s−1 for 10 min, then the constant potential was kept at −1.4 V for 10 min. The prepared carbon felt anode modified with Fe2O3-polyaniline-dopamine hybrid composite was denoted as Fe2O3-PDHC/CF.
All the electrical analytical tests were conducted after three months of operation. CV measurements were carried out using a three-electrode electrochemical model in MFC reactors at a scan rate of 0.1 V·s−1. The Fe2O3-PDHC/CF and CF anodes were served as the working electrode respectively. Cathode acted as a counter electrode, and SCE was used as a reference electrode. Electrochemical impedance spectroscopy (EIS) was carried out over a wide frequency range from 10 kHz to 0.1 Hz with an AC perturbation of 5 mV. The as-prepared anodes were acted as the working electrode, while an Ag/AgCl electrode and cathode of MFC were used as reference and counter electrode, respectively. Each resistance was obtained using ZsimpWin software. Anodic biofilm was scraped after three months of operation. The Fe2O3-PDHC/CF anode was cut into pieces and microbe biofilm on the anode was carefully scraped. DNA of bacteria was extracted by using E.Z.N.A™ Mag-Bind Soil DNA Kit (Omega Biotech Co. Ltd., USA) per the operating instruction. The V3 region of 16S rDNA was amplified with the 341–534 primer set (F: CCTACGGGAGGCAGCAG, R: ATTACCGCG GCTGCTGG). The amplicons were then sequenced using the Illumina MiSeq sequencing platform in Sangon Biotech (Shanghai, China). The sequencing data were processed and analyzed using the QIIME pipeline. R language was used for visualization of the results and statistical tests. 3. Results and discussion 3.1. Design and characterization of anodes
2.4. Construction and operation of MFC The anode plays a dual functional role in MFC where microorganisms will grow and multiply and electrons will transfer outward. Different anode materials directly affect the output power density of MFC. Therefore, the selection and preparation of anode materials are crucially important for designing high-performance MFC. The preparation of the Fe2O3-PDHC/CF anode material is shown in Scheme 1. The electrochemically synthesized polyaniline-dopamine membrane has played a crucial role in the deposition of Fe2O3 for it provides sufficient active sites and improves the hydrophilic of the CF surface. Fe2O3 particles which are applied to accelerate the extracellular electron transfer combinate with PANI-DA by CV method. The Fe2O3PDHC/CF material is beneficial to the attachment, growth and reproduction, and electron transfer outward of electrogenic bacteria. The scanning electron microscopy (SEM) images of CF and Fe2O3PDHC/CF anodes before inoculation were shown in Fig. 1a and b. Fig. 1c was the SEM image of Fe2O3-PDHC/CF under high magnification. As shown in Fig. 1a, the surface of CF fiber was not rough, while the surface roughness of Fe2O3-PDHC/CF anode was further increased (Fig. 1b), which made the specific area of the modified anode enlarged. Partial polymer film connected between the carbon felt fibers also increased the surface area of the surface-treated anode. The combination of Fe2O3 particles and the PDHC film might be due to the binding force of abundant catechol, amino, and imido groups of the polymer chain. After bacterial colonization, a piece of the anode was sacrificed for SEM imaging. Attachment of clubbed bacterial cells on the surface of various anodes was shown in Fig. 1 (d–f). Distinct to the bare CF anode with only a few bacterial cells on its surface (Fig. 1d), the biofilm on the Fe2O3-PDHC/CF anode was much thicker and larger in the area (Fig. 1e), which attributed to the hydrophilic functional groups of PANI-DA. It was consistent with Palacios-Cuesta’s experimental result that the affinity between the bacteria and the surface could be modulated by incorporate hydrophilic functional groups (Zhao et al., 2013). The improved biocompatibility of the anode was beneficial to the firm adhesion of bacterial cells on its surface and the improvement of direct electron transfer from microbial to the anode via outer membrane ctype cytochromes (Zhao et al., 2015b). In addition to the fact that Fe2O3-PDHC/CF anode exhibited a higher bacterial loading than CF anode, a large number of bacterial cells could also be observed in the
Different anodes with an effective area of 1 cm2 (1 cm × 1 cm) and the same CF cathodes (4 cm × 4 cm) were assembled to the doublechamber MFC made of Plexiglas as MFC reactors. All MFC reactors were composed of an anode chamber (5 cm × 4 cm × 6 cm, net volume 120 mL), a cathode chamber (5 cm × 6 cm × 6 cm, net volume 180 mL) and a proton exchange membrane (PEM) which was pretreated by H2O2 (5 %) and H2SO4 (5 %) in turn. The anode nutrient solution consisted of 200 mg L−1 indole, 0.13 g·L−1 KCl, 0.31 g·L−1 NH4Cl, 3.32 g·L−1 NaH2PO4·2H2O, and 10.32 g·L−1 Na2HPO4·12H2O. N2 was constantly aerated in the anode chamber for about 10 min to remove the dissolved oxygen. Catholyte consists of 18.65 g·L−1 K3Fe(CN)6, 200 mg L−1 indole, 0.13 g·L−1 KCl, 0.31 g·L−1 NH4Cl, 3.32 g·L−1 NaH2PO4·2H2O, and 10.32 g·L−1 Na2HPO4·12H2O. 30 mL anodic bacteria inoculation fluid which had been cultivated for 2 months in a growth medium composed of 200 mg L−1 indole and 50 mmol·L−1 PBS was added in both of the chambers of the MFC reactor. All reactors were operated with an external load of 1000 Ω in a constant temperature incubator at 30 ± 1 ℃, and the voltage was self-recording with a data acquisition system every 10 min. Two parallel reactors were constructed for each anode including the plain carbon felt anode used for blank as duplicate tests. 2.5. Indole degradation and performance of MFC The MFC as described above was constructed and operated for more than three months. The sample was taken from the MFC reactor every 6 h and centrifuged at 10,000 r/min for 10 min to determine indole concentration in the supernatant. Polarization curves and the maximum power density were obtained by varying the external resistance from 1000 Ω to 100 Ω, and the corresponding voltage was recorded with a 30 min interval time by an exquisite multimeter. The current density was calculated using the equation: j = E/(R·AAn), where j (A·m−2) was the current density, E (V) was the voltage, R (Ω) was the load resistance, and AAn (m2) was the active area of the anode. From this, the power density of the MFC by taking the product of the voltage and current were calculated by the equation: P = j·E (Palacios-Cuesta et al., 2015). Both the current and power densities were normalized to the anode surface area of 1 cm2. 3
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Scheme 1. Schematic of the fabrication of the Fe2O3-PDHC/CF anode.
interior of the fibers, indicating that the microbe loading capacity was increased. The increased bacterial loading mass on the anode could improve the extracellular electron transfer efficiency between the microbial and the modified CF anode through intimate contact (Saratale et al., 2017). It was interesting to note that some Fe2O3 particles were encased in the bacterial membrane and the biofilms bind to them tightly were significantly thicker, with remarkably increased microbes loading around them (Fig. 1f). The images revealed that the presence of Fe2O3 introduced onto the surface of CF modified with polyanilinedopamine film could promote the formation of electroactive biofilms, and more microorganisms could be adsorbed on the anode, which acted
as a biocatalyst to hydrolyze the substrate to produce more protons and electrons in MFC (Xue et al., 2019). Therefore, the MFC loading Fe2O3PDHC/CF anode was expected to exhibit a higher degradation efficiency of indole and electricity generation performance.
3.2. Bacterial community To evaluate the microbial community richness and species diversity in the MFC loading Fe2O3-PDHC/CF anode in indole solution, 50 of the most abundant genera were constructed in a heatmap, in which intuitionistic relative abundance could be shown. In terms of the
Fig. 1. SEM images of anodes before inoculation (a, bare CF; b, Fe2O3-PDHC/CF; c, Fe2O3-PDHC/CF with high magnification) and after running (d, bare CF; e, Fe2O3PDHC/CF; f, Fe2O3-PDHC/CF with high magnification). 4
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Fig. 2. A tree diagram of the classification system of the microbial sample on Fe2O3-PDHC/CF anode at the genus level. Different colors represented different taxonomic levels, which were in order from left to right. The size of the circle represented species abundance, and near the fulcrum were the taxonomic name and its corresponding abundance value respectively. On the far right was the distribution of species in the top 30 abundance.
degrade large amounts of indole to nutrients. It was the direct factor to improve the electrical performance and indole degradation efficiency of the anode. So far, the MFC reactor loading the Fe2O3-PDHC/CF anode has operated over 18 months holding good performance and the microorganisms inside did not show observable decay.
microbial structure, the dominant phyla identified in the sample were Proteobacteria accounting for 93.4 % (Fig. 2), including Alcaligenes, Achrombacter and other electroactive bacteria. According to the detailed composition of the biofilm at the genus level showed in Fig. 3, the biofilms were dominated by Alcaligenes (63.3 %), which played a particularly important role in extracellular electron transfer (Chen et al., 2017). Besides, it was regarded to be associated with the oxidation of substrate via cometabolism and possessed the ability to resist the toxicity of indole, which might be the main reason for its predominance in the sample. Different from the literature (Ren et al., 2011), there were only a small number of other electricity-producing bacteria such as Delftia (2.48 %) and Pseudomonas (0.37 %), indicating that the impact of indole addition on species except the Proteobacteria phylum was detrimental and Achromobacter had a strong ability to degrade indole. The novel composite anode Fe2O3-PDHC/CF was beneficial to the enrichment, growth, and reproduction of microorganisms that could resist the toxicity of indole by rapid electroactive biofilms formation and
3.3. Electricity generation performance of MFC To assess the electricity generation properties of the novel anode, Fe2O3-PDHC/CF anode was applied in MFC, and the initial concentration of indole acolyte was set to be 200 mg L−1. CF anode was used for performance comparison. Two of the MFC reactors were tested at an external resistance of 1000 Ω. The start-up profiles of the two MFC reactors were shown in Fig. 4, exhibiting that the start-up time of the MFC loading surface-treated anode was shorter than the MFC containing unmodified CF anode. It decreased by 57.9 % from 76 h (CF) to 32 h (Table 1). The shortened start-up time meant that the growth 5
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Fig. 3. Hierarchical cluster analysis of microbial communities on Fe2O3-PDHC/CF anode at the genus level. The species clustering tree was on the left. Table 1 Performance of MFC reactors using different anodes. Anode
t (h)
Vmax (mV)
Pmax (mW·m−2)
Indole degradation efficiency (%)
CF Fe2O3-PDHC/ CF
44 32
443 ± 22 632 ± 39
1498.0 ± 26 3184.4 ± 45
44.0 90.3
process of bacteria from the logarithmic growth phase to the quiescent growth phase could be accelerated by modification of anode. Moreover, the profiles of output voltages shown in Fig. 4 also suggested that MFC containing modified anode prepared by CV and electrochemical deposition ran for a longer cycle. The results above could be attributed to the admirable biological compatibility of the PDHC membrane and the sharp increase of the specific surface area of anode material, which promoted the formation of the electroactive biofilms and improved the electrical properties of MFC. As shown in Figs. 4 and 5, the highest output voltage and the maximum power density of the MFC loading the Fe2O3-PDHC/CF anode
Fig. 4. Profiles of outputted cell voltages in MFC using different anodes during operation.
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Fig. 5. Polarization and power density curves as a function of current density for MFC operated using different anodes.
Fig. 7. The Nyquist curves of MFC equipped with different anodes in indole degradation.
reached 632 ± 39 mV and 3184.4 ± 45 mW·m−2 respectively, 43 % and 113 % higher than that of the MFC loading CF anode of 443 ± 22 mV and 1498.0 ± 26 mW·m−2 (Table 1). The present result should be attributed to the Fe2O3 deposited on the PDHC membrane made up for the defect of dopamine such as limited electrical conductivity and poor stability in strongly polar organic solvents (Li et al., 2016). Therefore, the electron transfer of the anode was enhanced and the electrical performance of the MFC was improved.
a remarkable decrease in the resistance of MFC reactors whose anodes were treated by electro-polymerization, for both of the Rct and the Rs of Fe2O3-PDHC/CF anode were lower than the CF anode. The values of Rs for CF and Fe2O3-PDHC/CF anodes were estimated to be 65.4 Ω and 27.3 Ω, respectively. Besides, the Fe2O3-PDHC/CF anode exhibited an Rct of 57.1 Ω, which was 100.7 % lower than the CF anode (114.6 Ω). It was suggested that the lower total internal resistance of the Fe2O3PDHC/CF anode was attributed to the synergistic effect between Fe2O3 and polyaniline-dopamine, which could accelerate the extracellular electron transfer between the modified anode and the bacterial biofilm. Moreover, the increase of the specific surface area of the Fe2O3-PDHC/ CF anode had a considerable effect on the internal resistance decrease and the Pmax increase (Hernández-Flores et al., 2015b). As a result, the maximum power density of the MFC loading modified anode was far higher than that loading the bare CF anode.
3.4. Electrochemical tests The electrochemical properties of the anodes were assessed further using cyclic voltammetry and electrochemical impedance spectroscopy. Cyclic voltammograms of the anodes in 0.1 mol·L−1 PBS were shown in Fig. 6. It was observed that the cyclic voltammogram of the Fe2O3PDHC/CF anode showed a large peak area and significant peak current of oxidation and reduction. This meant that the Fe2O3-PDHC/CF anode had greater electrical activity and larger electrochemical activity surface area. It was generally believed that electron conversion occurs through the bacterial biofilm anode, and stronger biofilm generated higher current (Franks et al., 2010; He and Mansfeld, 2009). On the other hand, the CF anode with poor biological compatibility revealed an inconspicuous redox activity. The electrochemical behavior of anode materials was examined by electrochemical impedance spectroscopy analysis. As shown in Fig. 7, the EIS data fitted as well-defined single semicircles over the high-frequency region represented solution resistance (Rs) (Hernández-Flores et al., 2015a). The charge-transfer resistance (Rct) was calculated by the semicircle fit in the Nyquist curve. The results indicated that there was
3.5. Degradation of indole The degradation of MFC versus time was shown in Fig. 8. After about 40 h of growth, the degradation efficiency of indole speeded up due to the stable formation of biofilms and the entry of microorganisms into the logarithmic growth period. In a period of 120 h, the maximum degradation of the MFC loading Fe2O3-PDHC/CF anode reached about 90.3 %, while that of the CF-MFC was 44.0 % barely (Table 1). These results revealed that the adhesion and growth of microorganisms that were conducive to indole degradation could be effectively improved by the Fe2O3-PDHC/CF synthesized through the electrochemical method, for the reason that the indole degradation efficiency of the MFC loading surface-treated anode was higher than that of plain CF. Furthermore,
Fig. 6. Cyclic voltammetry curves of different anodes in anolyte with a scanning rate of 0.1 V·s−1.
Fig. 8. Indole degradation using MFC equipped with different anodes. 7
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the combination of the Fe2O3 and polyaniline-dopamine made the composite anode possess the synergistic effect which facilitated the biocompatibility and charge transfer of the modified anode, so the indole degradation and bioelectricity generation of the MFC were both improved compared with that of the CF-MFC.
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4. Conclusion In conclusion, a novel Fe2O3-PDHC/CF anode has been prepared via cyclic voltammetry and electrochemical deposition. By depositing the high conductive Fe2O3 onto the hydrophilic and biocompatible polyaniline-dopamine membrane, the resistance of the anode was effectively reduced due to the accelerated extracellular electron transfer between bacteria and anode. Furthermore, the modified anode material was conducive to the adsorption of microorganisms and the rapid formation of electroactive biofilms which were benefit for bioelectricity generation and the indole removal capacity of MFC. Additionally, Proteobacteria phylum which degraded indole into nutrients could be enriched by the composite anode. 90.3 % of indole was degraded in 120 h by the MFC loading Fe2O3-PDHC/CF anode, and the maximum power density of which was as high as 3184.4 mW·m−2, which was amongst the highest values reported for MFC of indole anolyte. Therefore, the modification strategy of Fe2O3-PDHC/CF anode could be a promising candidate for the degradation of refractory organic pollutants in water by MFC. CRediT authorship contribution statement Minjie Jian: Conceptualization, Methodology, Formal analysis, Writing - original draft. Ping Xue: Validation, Resources, Writing review & editing. Keren Shi: Visualization. Rui Li: Supervision, Writing - review & editing. Lan Ma: Investigation, Writing - review & editing. Peng Li: Writing - review & editing. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgments The authors sincerely acknowledge the financial support from the National Natural Science Foundation of China (No. 21961028) and the Science and Technology Support Program of Ningxia Province of China (NX 2015076). References Katapodis, P., Moukouli, M., Christakopoulos, P., 2007. Biodegradation of indole at high concentration by persolvent fermentation with the thermophilic fungus Sporotrichum thermophile. Int. Biodeterior. Biodegrad. 60, 267–272. Joshi, D.R., Zhang, Y., Zhang, H., Gao, Y.X., Yang, M., 2017. Characteristics of microbial community functional structure of a biological coking wastewater treatment system. J. Environ. Sci. 63, 105–115. Li, G.H., Nandgaonkar, A.G., Wang, Q.Q., Zhang, J.N., Krause, W.E., Wei, Q.F., Lucia, L.A., 2017. Laccase-immobilized bacterial cellulose/TiO2functionalized composite membranes: evaluation for photo- and bio-catalytic dye degradation. J. Membrane Sci. 525, 89–98. Shi, J.X., Han, Y.X., Xu, C.Y., Han, H.J., 2019. Anaerobic bioaugmentation hydrolysis of selected nitrogen heterocyclic compound in coal gasification wastewater. Bioresour. Technol. 278, 223–230. Arora, P.K., Bae, H.H., 2014. Identification of new metabolites of bacterial transformation of indole by gas chromatography–mass spectrometry and high-performance liquid chromatography. Int. J. Anal. Chem. 4, 1–5. Qu, Y.Y., Xu, B.W., Zhang, X.W., Ma, Q., Zhou, H., Kong, C.L., Zhang, Z.J., Zhou, J.T., 2013. Biotransformation of indole by whole cells of recombinant biphenyl dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase. Biochem. Eng. J. 72, 54–60. Carlson, J.R., Yokoyama, M.T., Dickinson, E.O., 1972. Induction of pulmonary edema and emphysema in cattle and goats with 3-methylindole. Science 176, 298–299.
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Chen, J.F., Zhang, L.H., Hu, Y.Y., Huang, W.T., Niu, Z.Y., Sun, J., 2017. Bacterial community shift and incurred performance in response to in situ microbial self-assembly graphene and polarity reversion in microbial fuel cell. Bioresour. Technol. 242, 220–227. Ren, Z.Y., Ramasamy, R.P., Cloud-Owen, S.R., Yan, H.J., Mench, M.M., Regan, J.M., 2011. Time-course correlation of biofilm properties and electrochemical performance in single-chamber microbial fuel cells. Bioresour. Technol. 102, 416–421. Franks, A.E., Malvankar, N., Nevin, K.P., 2010. Bacterial biofilms: the powerhouse of a microbial fuel cell. Biofuels 1, 589–604. He, Z., Mansfeld, F., 2009. Exploring the use of electrochemical impedance spectroscopy (EIS) in microbial fuel cell studies. Energy Environ. Sci. 2, 215–219. Hernández-Flores, G., Poggi-Varaldo, H.M., Solorza-Feria, O., Ponce Noyola, M.T., Romero-Castañón, T., Rinderknecht-Seijas, N., 2015a. Tafel equation based model for the performance of a microbial fuel cell. Int. J. Hydrogen Energy 41, 17421–17432. Hernández-Flores, G., Poggi-Varaldo, H.M., Solorza-Feria, O., Ponce Noyola, M.T., Romero-Castañón, T., Rinderknecht-Seijas, N., 2015b. Tafel equation based model for the performance of a microbial fuel cell. Int. J. Hydrogen Energy 41, 17421–17432.
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