High performance of microbial fuel cell afforded by metallic tungsten carbide decorated carbon cloth anode

Journal Pre-proof High performance of microbial fuel cell afforded by metallic tungsten carbide decorated carbon cloth anode Da Liu, Qinghuan Chang, Yan Gao, Weicheng Huang, Ziyu Sun, Mei Yan, Chongshen Guo PII:

S0013-4686(19)32114-0

DOI:

https://doi.org/10.1016/j.electacta.2019.135243

Reference:

EA 135243

To appear in:

Electrochimica Acta

Received Date: 14 October 2019 Revised Date:

7 November 2019

Accepted Date: 7 November 2019

Please cite this article as: D. Liu, Q. Chang, Y. Gao, W. Huang, Z. Sun, M. Yan, C. Guo, High performance of microbial fuel cell afforded by metallic tungsten carbide decorated carbon cloth anode, Electrochimica Acta (2019), doi: https://doi.org/10.1016/j.electacta.2019.135243. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

Graphical abstract:

High performance of microbial fuel cell afforded by metallic tungsten carbide decorated carbon cloth anode Da Liub, Qinghuan Changa, Yan Gaoa, Weicheng Huangc, Ziyu Sunb, Mei Yana,b*and Chongshen Guoa*

c

a

School of Chemistry and Chemical Engineering, Harbin Institute of Technology, Harbin, 150001, China

b

School of Life Science and Technology, Harbin Institute of Technology, Harbin, 150001, China

School of Instrumentation Science and Engineering, Harbin Institute of Technology, Harbin, 150001, China * Corresponding authors. E-mail addresses: [email protected] (M. Yan) and [email protected] (C. S. Guo)

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Abstract Developing high efficient anode is of great significances for the application of microbial fuel cells. Tungsten carbide attracts our attention due to its platinum-like metallic conductivity, corrosion resistance and low cost. In this work, tungsten carbide nanoparticles are pasted on carbon cloth as the anode for mediator-less microbial fuel cell. The surface of obtained anode is quickly attached with highly dense biofilm that accounts for a fast extracellular electron transfer rate. Microbial community structure analysis at the genus level shows that the main exoelectrogens are Geobacter, Geothrix and Pseudomonas, all of which can completely decompose acetate and transfer electrons through both direct and indirect extracellular electron transfer pathways. Consequently, it contributes to higher power density (3.26 W m-2), better chemical oxygen demand removal rate (95.5%) and greater coulombic efficiency (83.2%), which are 2.14-fold, 1.22-fold, 1.71-fold of that obtained by the naked carbon cloth anode (1.52 W m-2, 78.1%, 48.6%), respectively. Especially for the coulombic efficiency, it is obviously higher than others’ reported works in the similar microbial fuel cells system, being attributable to the synergistic effect of exoelectrogen. In virtue of the above advantages, tungsten carbide is a potential candidate for the further application of microbial fuel cells. Keywords: tungsten carbide; microbial fuel cell; coulombic efficiency; exoelectrogen; extracellular electron transfer

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1. Introduction Traditional sewage treatment consumes huge electrical power as well as results in waste of substantial energy in organic-rich wastewater [1]. The development of microbial fuel cells (MFCs) covers this shortage as it can convert chemical energy in organic fuels into electricity by microorganisms and meanwhile recycle waste to protect environment [2, 3]. Actually, any source of biodegradable organic matters can be used in MFCs for the power generation, including organic contaminant as well as organic matter present in human, animal and food-processing waste waters [4]. MFCs have potential applications in power supply system for some small electrical devices, biohydrogen production and wastewater treatment [5, 6]. In addition, the current output of MFCs is sensitive to contaminant or microorganism on the electrode surface, and thus it is also applicable as biosensors for biochemical oxygen demand (BOD) and toxic substances [7-9] detection. On the basis of above broad applications, MFCs have attracted much attention of scientific researchers and been widely studied in recent decades. Until now, low power density and high cost are still the main limiting factors of industrialization of MFCs. Many factors that determine the MFC performance have been optimized, such as anodic and cathodic catalysts, ion-exchange membrane, configuration of cells et al [2, 10-15]. Of them, anodic materials as the habitat of microorganisms play a more important role in improving the performance of microbial fuel cells, as low extracellular electron transfer (EET) rate is the bottleneck of development of anodic catalyst. 4

With respect to the anode, the performance of MFC is determined by the bacterial activity on the electrode surface, the interfacial electron transfer ability from bacteria to the electrode, the conductivity and the biocompatibility (which determines the amount of bacteria colonization) of the electrode [16, 17]. Based on these criteria, the extensively developed anode materials are various structural and functionalized carbon materials, including traditional carbon cloth, carbon paper, carbon felt, graphite rod et al, as well as non-conventional carbonaceous materials, such as single walled carbon nanotubes, multi-walled carbon nanotubes and graphene based anodes [16, 18, 19]. Nevertheless, low accessible surface area and electrochemical activity of traditional carbonaceous materials restrict their application in MFC. Although carbon nanotube and graphene based anodes possess higher surface area and better conductivity than traditional carbonaceous materials, complicated fabrication method and high cost impede large-scale production. Metal based anodes such as gold, silver, copper, nickel and stainless steel, etc. have high conductivity (two to three orders of magnitude high that of carbon [20]), however, low corrosion resistant and biocompatibility make them unsuitable for use within MFCs [21]. Consequently, it is necessary to develop an anode with excellent conductivity, high surface area, low cost, good biocompatibility and stability for MFCs. Transition metal carbides possess platinum-like electronic property and have been widely used as substitutes of noble metal catalyst in many reactions, such as hydrazine decomposition, ammonia synthesis and decomposition, isomerization, hydrogenation evolution, oxygen reduction and biomass conversions, especially in the 5

C-C, C-O-C and C-O-H bonds cleavage reactions [22-26]. Molybdenum carbide (Mo2C) [27] as one of the transition metal carbides was applied as anodic catalysts for microbial fuel cell based on Klebsiella pneumoniae. The maximum power density of single-cube MFC with 6.0 mg cm-2 Mo2C is 0.27 W m-2, comparable to that of the MFC using 0.5 mg cm-2 Pt as anodic catalyst (0.40 W m-2). Except this, Mo2C/CNTs [28], Ni3Mo3C [29], Ni/β-Mo2C [30], Mo2C@CF [31], HD-Mo2C/MoO2 [32] and Mo2C/CCT [33] were also applied as anodes in microbial fuel cells. However, the performances of MFCs are not satisfied. In this paper, tungsten carbide (WC) attracts our attention due to its noble metal-like metallic conductivity, corrosion resistance and low cost [34-36]. Although it has exhibited high electrocatalytic activity for several common microbial fermentation products and high performance as the anode of MFCs [37, 38], more details about the role of WC and the mechanism of EET should be discussed. In order to decompose organic matters completely and extract more electrons to external circuit, more abundant species of bacteria should be screened and they work together to improve the energy conversion efficiency. Hence, in this work, tungsten carbide nanoparticles are pasted on carbon cloth (WC/CC) as the anode for microbial fuel cells with mixed bacterial inoculation. The good biocompatibility of WC made fast attachment of highly active biofilm and the MFC with WC/CC anode outputted stable and high voltages. The excellent conductivity and good interfacial charge transfer ability accelerated EET and gave maximum power density of 3.26 W m-2 and coulombic efficiency of 83.2%, much higher than that obtained by carbon cloth anode (1.52 W m-2 and 48.6%). 6

2. Materials and methods 2.1 Chemicals Tungsten carbide powder was bought from Shanghai Chaowei Nano Technology Co. Ltd., (Shanghai, China). Carbon cloth was obtained from Shanghai Miaohan Building Technology Co. Ltd., (Shanghai, China). CMI700 cation exchange membranes were obtained from Membrane International (USA). Nafion D520 solutions (5%) were purchased from DuPont (USA). The H-shaped dual-chamber MFCs were obtained from Wenoote (Suzhou, China). DNeasy Powersoil Kit was acquired from Qiagen (Germany). The other chemical reagents were purchased from Sigma-Aldrich (Shanghai, China), such as NaH2PO4·2H2O, Na2HPO4·12H2O, NH4Cl, KCl, CH3COONa and K3[Fe(CN)6]. 2.2 Characterization The Hitachi S-4800 scanning electron microscope (SEM) was used to observe the morphologies of the bacterial and anode materials. For SEM test, the anode covered by biofilm was immobilized in 4% polyformaldehyde solution for 30 min at 4 o

C, rinsed three times with PBS solution, and then dehydrated using graded ethanol

solution (once with 30, 50, 70, 85 and 95%, twice with 100%). Transmission electron microscopy (TEM) and high-resolution transmission electron microscopy (HRTEM) were performed by a FEI Tecnai G2 F30 instrument operated at an accelerated voltage of 200 KV. X-ray diffraction (XRD) patterns were recorded on an Empyrean (Holland) diffractometer in the 2θ range from 5 to 90°. X-ray photon spectroscopy 7

(XPS) spectra were used to identify the elements on the surface of the samples by an ESCALAB 250Xi (Thermo Fisher Scientific Inc. USA). The electrical resistivity was tested by Physical Property Measurement System (PPMS) DynaCool. Cyclic voltammetry (CV), differential pulse voltammetry (DPV) and electrochemical impedance spectroscopy (EIS) were performed with a 1260 Impedance/gain-phase Analyzer (Solartron Metrology Inc., USA) and CHI 760E electrochemical workstation (Shanghai Chenhua, China). All of the tests were executed in a three-electrode electrochemical cell including a working electrode, an Ag/AgCl reference electrode, and a platinum plate counter electrode. CV was recorded between 0.8 and 0.2 V with a scan rate of 1 mV s-1. DPV was carried out from -0.8 to 0.2 V with amplitude 60 mV, pulse width 200 ms and potential increment 6 mV. For EIS, the frequency range was from 100 kHz to 0.01 Hz with the direct current potential of 0.2 V and alternating current amplitude of 10 mV. 2.3 MFC setup and operation All of the MFCs were constructed by H-shaped two chambers with a volume of 100 ml, which were connected by cation exchange membranes (Ultrex CMI7000, Membrane International Inc., USA). The anode chamber was performed with a carbon cloth or WC/CC (tungsten carbide nanoparticles were pasted on both sides of carbon cloth with 5 wt% Nafion solution as the binder; the average loading was 1.15 mg cm-2) anode (1cm×1cm), filling with 100 mL of anolyte containing sodium acetate (2 g L-1), a mineral (82.1 mg L-1, including 0.25 mg L-1 Fe2+), and vitamin (0.2 mg L-1) in 50 mM phosphate buffer solution (PBS). The cathode was equipped with a commercial 8

carbon brush electrode and filled with 100 mL of catholyte containing potassium ferricyanide (50 mM) and potassium chloride (50 mM). For MFC start-up, the inoculation fluid was from a mixture of bacteria-enriched effuent with well-started MFCs and anaerobic sludge. All MFCs were operated with an external loading resistance of 1000 Ω at 37 oC

and the output voltage was collected every 10 min

using a Data Acquisition System (Model 2700 with 7702 modules, Keithley Instruments, Inc. USA). The polarization and power density curves were acquired at the stable state of the MFCs by measuring the stable voltage while varying the external resistance from 200 to 2000 Ω. Both current density and power density were normalized to the anode surface area (2.0 cm2). Both influent and effluent were collected after an entire cycle, and then filtered through 0.22 µm pore-diameter cellulose acetate filters to analyze chemical oxygen demand (COD) with DRB 200 and DR 3900 HACH Instruments Inc., USA. COD removal was calculated according to the following formula: COD removal rate% = (CODinfluent-CODeffluent)/CODinfluent× 100%. Coulombic efficiency (CE) was calculated on the basis of CE = 8∫Idt/FVan∆COD, here I (A) is the output current of the entire cycle, F is the Faraday’s constant (96485 C/mol), Van (L) is the volume of anodic chamber (0.10 L), ∆COD (g/L) is the difference between influent and effluent (CODinfluent-CODeffluent). 2.4 Microbial community analysis After 20 d of steady and repeatable voltage output, the anode was removed from the chamber to extract bacterial DNA with Power Soil DNA Isolation Kit (MoBio Laboratories, Inc., Carlsbad, CA) following the manufacturer’s instruction. DNA 9

concentration was confirmed by a spectrophotometer (NanoDrop 2000c, Thermo, USA). For details, please see our previous report [39]. 3. Results and discussion 3.1 Characterizations of tungsten carbide The microscopic morphology of tungsten carbide was observed by SEM and TEM images, both of them show the irregular nanoparticles of WC and the size is ranging from 100 to 400 nm (Fig. 1a, b). The EDX mapping results certificate the uniform distribution of C and W elements (Fig. S1) within the particles. High-resolution TEM image shows regular lattice fringe with d-spacing of 0.25 nm, corresponding to the (100) facet of WC (Fig. 1c). X-ray diffraction pattern confirms the crystalline structure of WC nanoparticles (Fig. 1d). All of the diffractive peaks match well with the standard PDF card (JCPDS#51-0939), indicating a pure phase of hexagonal WC [35]. Three main diffraction peaks at the angle of 31.5o, 35.6o and 48.3o are related to the (001), (100) and (101) facets of WC, respectively. X-ray photon spectroscopy was employed to investigate the chemical state of the WC particles. Fig. 1e shows the full-range XPS spectrum of WC, showing the existence of C, W and O elements. The high-resolution of core-level W 4f spectra could be divided into two spin-orbit doublet peaks with a separation of 2.1 eV (Fig. 1f). The peaks at 32.0 and 34.1 eV corresponds to W4+(4f7/2) and W4+(4f5/2), which can be assigned to the W-C chemical bonds of WC [40]. Another doublet peaks at 35.7 and 37.8 eV are corresponding to W6+(4f7/2) and W6+(4f5/2) respectively. The presence of W6+ may be 10

related to the adsorbed oxygen or formation of amorphous WOx layer as absence of reflective peaks from WOx species in the XRD pattern. All of the above characterizations well proved the WC nature of nanoparticles used in this work. 3.2 Electrochemical measurements of electrodes The above WC nanoparticles were pasted on carbon cloth with 5 wt% Nafion solution as the binder to get WC/CC anode for the microbial fuel cells study, while CC electrode was used as the control. The electrochemical activity of WC/CC and CC was tested by cyclic voltammetry in fresh anolyte at a scan rate of 1 mV s-1. As shown in Fig. 2a, the anode of WC/CC has a little higher capacitive current than that of CC, implying more active sites of WC nanoparticles for electro-catalytic redox reactions. The conductivity and the electron transfer ability of WC/CC and CC electrodes were evaluated by electrochemical impedance spectroscopy. The EIS tests were performed in 5 mM PBS containing 5 mM potassium ferricyanide. The results were depicted as Nyquist curves in Fig. 2b and then analyzed according to an equivalent circuit shown in inset of Fig. 2b. Both of the ohmic resistance (Rs) and charge transfer resistance (Rct) for WC/CC (26.0 Ω and 43.2 Ω, respectively) were much lower than that for CC (47.6 Ω and 273.1 Ω, respectively). This means higher conductivity and faster interfacial charge transfer ability of WC/CC between the electrode and electrolyte, which can be attributed to the superior electronic conductivity and platinum-like behavior of tungsten carbide [34, 41, 42]. In addition, the electrical resistivity of the pressed powder of WC nanoparticles is 9.0×10-4 Ω·m at 300 K and the density functional theory calculations in recent report also demonstrated the metallic behavior of WC 11

[43]. This further confirmed the above results. Moreover, Wang [40] have reported that the synergetic effect between WC and W-O layers promoted interfacial charge transfer and separation. The amorphous WOx layer on WC surface deduced by XPS (related to the presence of W6+) in this work is just right accordance with the above result. The fast charge transfer ability is essential for electrons transfer from electricigens to external circuit in microbial fuel cells. 3.3 MFC performance The H-shaped dual-chamber of microbial fuel cell was constructed with WC/CC or CC anode and carbon brush cathode. The anode was inoculated by a mixture of anaerobic sludge and bacteria-enriched effuent with well-started MFCs. Sodium acetate was substrate in the anolyte while the potassium ferricyanide was electron acceptor in the catholyte. The output voltage curves of MFCs were shown in Fig. 3a. After 2.5 d of operation, the voltage of MFC with WC/CC anode increased sharply and reached a maximum voltage of 0.60 V for the first cycle, while the CC anode reached only 0.49 V and decreased rapidly, implying that unstable biofilm covered the carbon cloth for the first cycle. The growth of microorganisms in a batch culture could be made up of four phases: lag, exponential, stationary, and death [44]. This can be reflected indirectly by the first cycle of the voltage output curve (Fig. S3). As the metallic property of WC improves the conductivity of the anode, thus the electrons extracted from acetate sodium by the bacteria can be transferred to external circuit by WC/CC quickly and generate current. During the first 2 days, the bacteria adhere to the surface of WC/CC and the good biocompatibility of WC shortens this lag phase in 12

comparison with the naked CC. The second exponential phase is the exponential growth of bacterial number and the formation of biofilm. The lag phase plus exponential phase are the start-up time of the MFCs. Once a stable biofilm formed, the cell outputs stable voltages and enters the stationary phase. The reproduction and death of bacteria reach a balance. When the culture medium is consumed, the growth of bacteria enters the dead phase. However, the rate of bacterial death is much slower than the rate of exponential growth. As long as the culture medium is refreshed timely, the cell can output a steady and repeatable voltage curve. During the long-term operation of MFCs for 60 d, WC/CC anode displayed steady voltage output and the voltage can still reached to 0.60 V even in the last cycle. Whereas CC anode showed fluctuant voltages, and the voltage just reached to 0.41 V in the last cycle, being only 84% that of the first cycle. These results verify that tungsten carbide nanoparticles improved the stability of the anode, which is probably due to the high biocompatibility of WC and stable electrochemical active biofilm coverage on its surface. After two cycles of steady and repeatable voltage output, the polarization curves were measured and shown in Fig. 3b. The MFC equipped with WC/CC anode exhibited higher open circuit voltage and lower absolute value of slope than that with CC anode, illustrating that WC nanoparticles lowered the biological catalytic over-potential of the anode. The maximum power density of WC/CC is 3.26 W m-2, being 2.14-fold that of CC (1.52 W m-2). Even after 60 d of operation, the maximum power density of WC/CC is 2.78 W m-2, keeping 85.3% of the original performance (Fig. S4). By contrast, the maximum power density of CC decreased to 0.89 W m-2, 13

only 58.6% of the best result. This further confirmed the long-term stability of WC/CC anode. To verify that the high performance of MFC is attributed to the anode rather than cathode, both anodic and cathodic polarization curves were recorded at the same time. As shown in Fig. 3c, apparently, the cathodic polarization curves are similar while anodic polarization curves are much distinct from each other. This certificates the above statement and further confirms the efficacy of WC nanoparticles. In view of energy recovery efficiency, COD removal rate and coulombic efficiency are also important parameters to be considered. Here, the MFC equipped with WC/CC anode afforded 95.5% of COD removal efficiency, which is much higher than that with CC anode (78.1%). Unexpectedly, WC/CC achieved 83.2% of coulombic efficiency and it was 71.1% higher than that with CC (48.6%) anode. Moreover, this is also the highest one in the similar MFCs system reported in recent years (Table 1). Among those, most of the CE values are below 50%. The high value in this work may be related to the high activity of surface covered biofilm, which will be discussed in the following part. 3.4 The electrochemical activity of anodic biofilm The microscopic morphology of carbon cloth is uniform carbon fibers with smooth surfaces (Fig. S2a), being unfavorable for the bacterial adhesion. When tungsten carbide nanoparticles were pasted on its surface (Fig. S2b), both the roughness and biocompatibility would be improved. Then, WC/CC and CC anodes were inoculated with mixed bacterial culture in MFCs. After 2.5 d of operation, the biofilms were characterized by SEM images. As shown in Fig. 4a, on the surface of 14

WC/CC anode, highly dense biofilm not only covered all the carbon fibers but also connected adjacent ones. WC nanoparticles were not fully covered up by the biofilm but mingled with them. Thus, WC can transfer electrons and assist catalyzing decomposition of organic matters. The continuous biofilm implanted with WC nanoparticles and framework of carbon fibers constitute an outstanding anode. The electrons can be transferred from bacteria to neighboring bacteria or to WC, and then via carbon fibers to external circuit, thus improving EET and generating stable and high voltages. By contrast, the bacteria adhered on the naked carbon cloth anode not totally covered all the fibers yet (Fig. 4b), resulting in low and sharply dropped voltages for the first cycle. After several stable cycles of output voltages for MFCs, EIS tests were performed to evaluate the interfacial charge transfer ability of WC/CC and CC anodes with biofilm. The charge transfer resistance for WC/CC with biofilm is 174.2 Ω, being lower that for CC after biofilm coverage (686.9 Ω). The low Rct means fast extracellular electron transfer rate. Moreover, CV curves were tested in anolyte to further examine the electrochemical activity of the biofilm. As shown in Fig. 4d, typical sigmoidal curves appeared in both of WC/CC and CC curves. When the potential was higher than -0.4 V, the current density of CC increased sharply and then reached a limiting current of 3.78 A m-2. In contrast, for WC/CC anode, the CV curve showed similar shape but with higher limiting current of 9.3 A m-2, which was 2.46 times greater than that for CC. In addition, the area of curve for WC/CC was 1.84 times higher than that for CC, indicating that biofilm covered on WC/CC anode gave rise to more active sites and higher conductivity. The above results certificate 15

that WC modification favors electroactive bacteria adhesion and accelerates extracellular electron transfer. To analyze the catalytic processes, more sensitive differential pulse voltammetry was performed. Under the non-turnover condition (Fig. 4e), the dominant redox center at the potential of -0.35 V (WC/CC) or -0.32 V (CC) was assigned to the outer membrane triheme cytochrome PpcA. The weak broad peak from -0.55 V to -0.40 V for WC/CC belonged to the outer membrane c-type cytochromes OmcB, OmcS and OmcZ. The other obvious redox centers at -0.27 V (WC/CC) or -0.25 V (CC) were attributed to other outer membrane c-type cytochromes or unknown species. PpcA might be the reservoir of electrons while the outer membrane c-type cytochromes and unknown species may serve as mediators of electron transfer [45], all of which together contributed to the fast EET. The peak current density of WC/CC with biofilm under non-turnover condition was 7.52 A m-2. When the medium in anode chamber was replaced by fresh anolyte, the peak current density was 6.85 A m-2 (Fig. S3a), 8.9% lower than that before, suggesting that a few soluble electron transfer mediators generated by bacteria were discarded when refreshing the anolyte. Nevertheless, the output voltages of MFC rose to the maximum values in short time and the peak current density of DPV in this condition returned to 7.48 A m-2 (Fig. S3b), illustrating that soluble mediators were regenerated again during microbial metabolism. On the contrary, WC/CC anode before inoculation under turnover condition only generated 0.5 A m-2 of current density (Fig. 4f). This illustrated that majority of EET pathways came from the anode biofilm and minority was constituted by soluble mediators in the anolyte. 16

3.5 Microbial community analysis 16S rRNA gene sequence analysis was performed to analyze the microbial community of the MFC anode biofilm. At the genus level, the predominant bacteria in the WC/CC anode biofilm were Geobacter, Geothrix, and Pseudomonas. The relative abundance of them is 60.5%, 15.2% and 5.9%, respectively. Geobacter as the well-known dissimilatory metal reduction bacteria undergoes direct EET mechanism, giving long distances electron transfer rather than soluble shuttles [46]. Geothrix can completely oxidize acetate and other organic compounds to generate electricity [47]. However, unlike Geobacter, it can secret two different soluble electron shuttles with separate redox potentials (-0.2 V and 0.3 V versus the standard hydrogen electrode) [46, 48]. Geothrix cells were coated with extracellular matrix, which probably prevent loss of the shuttles into external medium until weeks elapsed. They may be able to directly transfer electrons to electrode without shuttles, but the accumulation of mediators over time further enhanced the rate of electron transfer [47]. The current of DPV under non-turnover condition at about -0.4 V vs. Ag/AgCl may be partly contributed by the electron shuttles secreted by Geothrix. This also explained the tiny reduction of the peak current of DPV in refreshed medium (Fig. S3a). Pseudomonas as an electrochemically active bacteria could secret excellent electron shuttles for EET. The major advantages of Pseudomonas over many other exoelectrogens (such as Geobacter, Shewanella, etc.) are high adaptability to various environmental conditions and capability of applying a wide-spectrum of substrates for electricity generation in MFCs [49, 50]. The above exoelectrogens transfer electrons through 17

different pathways including direct and indirect EET mechanisms without addition of extra mediators. The diversity of bacteria guarantees the stability of anode biofilm and completely decomposition of substrates, resulting in high power density, high COD removal rate and excellent coulombic efficiency. On the contrary, the relative abundance of Geobacter, Geothrix, and Pseudomonas in CC anode biofilm is 74.0%, 0.1% and 0.9% respectively. Although the content of Geobacter on CC anode is higher than that on WC/CC anode, the synergistic effect of Geobacter, Geothrix, and Pseudomonas is more efficient in energy recovery aparently. The decoration of carbon cloth anode with tungsten carbide nanoparticles increases the biocompatibility and makes the surface rapidly enriched with highly active exoelectrogens (Geobacter, Geothrix, Pseudomonas, etc.). The exoelectrogens completely degraded acetate and transfered the electrons to electrode by long distance direct contact through bacteria, WC nanoparticles and carbon fibers, or indirect pathways mediated by outer membrane c-type cytochromes or electron shuttles secreted by exoelectrogens. These are the reasons for the fast extracellular electron transfer and

resultant high performance of MFCs (high power density, COD

removal and coulombic efficiency). Especially for CE, the value obtained in this work is 83.2%, being much higher than previously reported ones (usually lower than 50%). The high conductivity, good biocompatibility and low cost (noble metal free) make tungsten carbide applicable in microbial fuel cells. 4. Conclusions 18

In summary, tungsten carbide nanoparticles decorated carbon cloth was employed as the anode of microbial fuel cell. The surface of obtained WC/CC anode was ready attached by exoelectrogens (Geobacter, Geothrix, Pseudomonas, etc.) and endowed it with high conductivity and electrochemical catalytic activity. On the merits of above, MFC started-up quickly and the MFC outputted high and stable voltages (higher than 0.6 V). As control, the MFC with naked CC anode only generated low and fluctuant voltages (lower than 0.5 V). The MFC with WC/CC anode showed high power density (3.26 W m-2), better COD removal rate (95.5%) and excellent coulombic efficiency (83.2%), which are 2.14-fold, 1.22-fold, 1.71-fold of CC anode (1.52 W m-2, 78.1%, 48.6%), respectively. This underlying reason accounting for superior performance was the metallic conductivity and good biocompatibility of tungsten carbide and synergistic effect of exoelectrogen. Acknowledgements This work was supported by China Postdoctoral Science Foundation [No. 2017T100247] and the National Natural Science Foundation of China [No. 51572059]. Appendix A. Supplementary material

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28

Figures and Table

Fig. 1

Fig. 2

29

Fig. 3

Fig. 4 30

Fig. 5

31

Table 1 Power Anode

Inoculation

Feed

Configuration

CE

density

Ref.

(mW m-2) FeS2/rGO

mixture

acetate

Dual-chambe

9.34%

3220

[39]

48%

803±6

[51]

46%

2590±120

[52]

15.34±0.062 233.5±11.

[53]

r PDA50

mixture

acetate

modified

Single-chamb er

stainless steel mesh LSC-TiO2

mixture

acetate

@C 3D-PCP

Single-chamb er

Shewanella

lactated Single-chamb

oneidensis

er

%

6

Single-chamb

48%

2920

[54]

40.5±4.0%

605

[55]

44.9%

1130

[56]

16.7%

358

[57]

MR-1 CP-Ni

mixture

acetate

er Bio-Pd 2

mixture

acetate

Dual-chambe r

AMB

mixture

acetate

Single-chamb er

CGA

mixture

acetate

Dual-chambe 32

r CNT

mixture

~

hydrogel acetate

O2

132

[58]

24.5%

1120

[59]

Single-chamb

48.47±0.98

1460

[60]

er

%

Single-chamb

44.1±2.8%

280.56

[61]

7.65%

767.3

[62]

15.4%

461.6

[63]

18.38%

450±10

[64]

83.2%

3260

This

Dual-chambe r

Shewanella

acetate

putrefaciens GZMA

32%

r

CNTs@Ti mixture

Pt/WO3

Dual-chambe

mixture

acetate

er 75 wt%

mixture

glucose Single-chamb

MnO2/HN

er

T E50+100a

mixture

acetate

Dual-chambe r

MFC-20

mixture

acetate

mTb WC/CC

Single-chamb er

mixture

acetate

Dual-chambe r

a

work

carbon paper coated with 50 and 100 nm Au each side

b

NdFeB anode with 20 mT magnets

33

Fig. 1 (a, b, c) SEM, TEM and HRTEM images of tungsten carbide, (d) XRD patterns of WC nanoparticles, (e) The full-range of XPS spectra, (f) High-resolution of W 4f XPS spectra. Fig. 2 (a) CV curves of WC/CC and CC anodes under scan rate of 1 mV s-1 in fresh anolyte, vs. Ag/AgCl (b) Nyquist plots of WC/CC and CC anodes before inoculation in 5 mM PBS including 5 mM K3[Fe(CN)6], the inset is the equivalent circuit. Fig. 3 (a) The output voltages of MFCs, (b) Polarization curves and power density of MFCs, (c) Anodic and cathodic polarization curves of MFCs, (d) COD removal (black) and coulombic efficiency (red) of MFCs based on WC/CC or CC anode. Fig. 4 SEM images of (a) the WC/CC and (b) CC anode after 2.5 d of inoculation with mixture cultivation, (c) Nyquist plots of EIS data for WC/CC and CC anodes in 5 mM PBS including 5 mM K3[Fe(CN)6], and inset is the equivalent circuit, (d) CV curves of WC/CC and CC anodes after biofilm coverage under scan rate of 1 mV s-1 in anolyte, vs. Ag/AgCl, (e) DPV of WC/CC and CC anodes after biofilm coverage under non-turnover conditions, (f) DPV of WC/CC and CC anodes before biofilm coverage under turnover condition, Condition: amplitude 60 mV, pulse width 200 ms and potential increment 6mV, vs. Ag/AgCl. Fig. 5 Microbial community composition of MFCs anode biofilms at the genus level Table 1 The MFCs performaces reported in recent years

34

Highlights


tungsten carbide is of metallic conductivity, high biocombatibility and low cost




tungsten carbide tremendously enhanced MFC performance in energy recovery




83.2% of coulombic efficiency was realized by MFC with WC/CC anode




the main exoelectrogens are Geobacter, Geothrix and Pseudomonas




the biofilm on WC/CC anode transfer electrons by direct and indirect pathways

Declaration of interests ☒ 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. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: