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Self-supported microbial carbon aerogel bioelectrocatalytic anode promoting extracellular electron transfer for efficient hydrogen evolution
Accepted Manuscript Self-supported microbial carbon aerogel bioelectrocatalytic anode promoting extracellular electron transfer for efficient hydrogen evolution Wei-Kang Wang, Bo Tang, Jian Liu, Huijie Shi, Qunjie Xu, Guohua Zhao PII:
S0013-4686(19)30356-1
DOI:
https://doi.org/10.1016/j.electacta.2019.02.099
Reference:
EA 33690
To appear in:
Electrochimica Acta
Received Date: 2 April 2018 Revised Date:
22 February 2019
Accepted Date: 25 February 2019
Please cite this article as: W.-K. Wang, B. Tang, J. Liu, H. Shi, Q. Xu, G. Zhao, Self-supported microbial carbon aerogel bioelectrocatalytic anode promoting extracellular electron transfer for efficient hydrogen evolution, Electrochimica Acta (2019), doi: https://doi.org/10.1016/j.electacta.2019.02.099. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. 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.
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Graphical Abstract
ACCEPTED MANUSCRIPT Self-supported Microbial Carbon Aerogel Bioelectrocatalytic Anode Promoting Extracellular Electron Transfer for Efficient Hydrogen Evolution Wei-Kang Wang†,§, Bo Tang†,§, Jian Liu†,§, Huijie Shi†, Qunjie Xu*,‡, , Guohua
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Zhao*,†,
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Shanghai Key Lab of Chemical Assessment and Sustainability, Department of Chemistry, Tongji University, Shanghai 200092, People’s Republic of China. Shanghai Key Laboratory of Materials Protection and Advanced Materials in
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Electric Power, Shanghai University of Electric Power, Shanghai 200090, China. Shanghai Institute of Pollution Control and Ecological Security,
W.K. Wang, B.Tang and J. Liu: These authors contributed equally.
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Shanghai200092, P.R. China.
Corresponding author:
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*E-mail: [email protected], [email protected]
ACCEPTED MANUSCRIPT ABSTRACT: Hydrogen production by microbial electrolysis cells (MECs) is an
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attractive and promising technology for sustainable energy. The bioelectrocatalytic
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activity of bioanode plays an essential role in improving the supply of electrons to
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cathode. Herein, a self-supported three-dimensional (3D) porous carbon aerogel (CA)
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bioanode was successfully applied in a MEC system for efficient hydrogen
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production. The 3D porous structure of CA greatly increased the bacterial incubation,
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then favored the extracellular electron transfer (EET) owing to its high specific
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surface area, excellent electrical conductivity and enhanced interaction with
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microbial. As a result, the hydrogen production of Bio-CA||Pt (0.37 µmol·cm-2·h-1)
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was 5 times higher than that of bio-carbon fiber (Bio-CF)||Pt (0.007µmol·cm-2·h-1) at
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the bias voltage of 0.3 V. Such a MEC with self-supported 3D porous microbial CA
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bioanode as a promising biotechnology will be further investigated for pollutant
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degradation and hydrogen production.
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Keywords: self-supported; carbon aerogel; bioelectrocatalytic; extracellular electron
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transfer; hydrogen evolution;
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ACCEPTED MANUSCRIPT 1. Introductin
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Hydrogen is a typical sustainable energy carrier for developing low carbon emission
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economy. Microbial electrolysis cells (MECs) are considered as a sort of
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environmental biotechnologies simultaneously for wastewater treatment and
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hydrogen production[1-3] for its high efficiency, cost effectiveness, and utilization of
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bio-electrons[4]. However, MECs for hydrogen production has suffered the low
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power density of bio-anode so far. Numerous efforts have been made to improve the
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performance of MECs via exploring the limiting factors[5], such as anode
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materials[6, 7], proton exchange membrane[8], efficiency of cathode[9] and so
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on[10-14]. And, the electron transfer efficiency of bio-anode has been recognized to
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be the key factor to enhancing the performance of MECs.
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Thus, developing of bio-anode materials with an excellent conductivity, high
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surface area, three-dimensional (3D) structure, and good bio-compatibility is
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promising solution to the problem. On conventional bio-anode materials in MECs
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such as carbon cloth (CC) and carbon fiber (CF)[15-18], the oxidation of organic
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species occurs with sluggish kinetics, leading to relatively low current densities and
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poor electron transfer to the cathode[3]. Aimed at improving the electron transfer on
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bio-anodes, carbon nanotube and graphene have been applied to modify bio-anodes
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owing to their good electrical conductivity[19]. Furthermore, 3D porous materials,
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such as carbon nanotube−textile and graphene sponges, have also been proved to
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improve current densities via increasing the quantity of incubated bacteria[20-25].
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However, besides of the high cost and instability in anaerobic conditions, more
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ACCEPTED MANUSCRIPT importantly, the usage of adhesives that immobilize electron conductor materials
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onto the anode greatly increased interface contact resistance, resulting in the limited
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electron transfer[26, 27]. Thus, some researches have been done for preparation of
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bio-anode by using biomass instead of commercial carbon-based materials[28, 29].
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Therefore, self-supported porous carbon bio-anode with high surface area, the
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abundance, 3D structure, environmental compatibility, chemical inertness, and high
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conductivity are desired for application of MECs.
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To date, carbon aerogels (CAs) are widely used as electrode materials[30-32].
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The morphologies and properties of CAs can be controled by the sol-gel reaction
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chemistry[32]. Thus, CAs exhibit not only have anaerobic stability and little
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interfacial contact resistance, but also the perfect electrical conductivity and
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biocompatible porosity derived from the tunable 3D hierarchical morphology with
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ultrafine sizes and conductive framework[31, 33]. For instance, electrical
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conductivity in CAs occurs through the movement of charge carriers via individual
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carbon particles and ‘‘hopping’’ of these carriers between adjacent carbon
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particles[31]. Meanwhile, CAs possess abundant micro and mesoporous structure
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with large BET surface area up to 500~600 m2/g, which benefits microbial
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attachment and the adsorption of organic species[34, 35].
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In this work, a self-supported 3D CA bio-anode electrode was successfully
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synthesized and applied in a MEC system. Also, the mechanism of enhanced direct
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contact-based EET and bio-catalysis on self-supported 3D CA bioanode was
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explored. Moreover, the current density and bio-anode potential of MEC with HER
ACCEPTED MANUSCRIPT was studied. To the best of our knowledge, this is the first attempt to develop a
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self-supported 3D CA bio-anode to achieve the efficient hydrogen evolution from
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MEC system. Meanwhile, these resluts may provide novel ideas of designing new
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systems for hydrogen production from bio-electro-catalysis.
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2. Materials and Methods
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2.1 Fabrication of microbial carbon aerogel anode
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The fabrication procedures of microbial carbon aerogel electrode are schematically
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shown in Figure 1a. 1, 3-dihydroxy benzene, formaldehyde, deionized water, and
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sodium carbonate were homogeneously mingled at a molar ratio of 1:2:17.5: 0.0008
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till colorless and transparent solution was obtained. Later the mixture was transferred
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into a cubical glass with the interlayer distance about of 5 mm, followed by aged at
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30 °C for 24 h, 50 °C for 24 h, and 90 °C for 72 h consecutively. The consequent
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organic wet gel was immerged into acetone for 72 h to remove water. Then, the wet
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aerogel was transformed to carbon aerogel (CA) in a tubular oven via pyrolysis, kept
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at 950 oC for 4 h under N2 atmosphere with the flow rate of 100 mL min-1 and the
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heating rate of 1 oC min-1.
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The as-prepared CA was polished with abrasive paper (320#) into the size of 13
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mm × 28 mm × 3 mm, then it was attached with a titanium wire (d=0.5 mm) as the
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conductor. A dual chambered MEC was constructed with two glass bottles connected
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anode was inoculated with the anaerobic sludge from a local pond. The anode
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chamber was filled with nutrient solution (per 1 L of deionized water: 1.64 g
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CH3COONa, 18.30 g K2HPO4·3H2O, 2.70 g KH2PO4, 0.5 g NaCl, 0.1 g NH4Cl, 0.1
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g MgSO4·7H2O, and 1 mL trace elements). The phosphate buffer solution in the
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cathode contained 16.46 g L-1 K3[Fe(CN)6]; 18.30 g L-1 K2HPO4·3H2O and 2.70 g
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L-1 KH2PO4). The solutions of both chambers were replaced per 48 h and then
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purged with N2 gas to remove the dissolved oxygen, to keep anaerobic condition.
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Commercial carbon fiber felt was calcined under 450 °C for 30 min, tailored into the
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same size as carbon aerogel, and then cultured into Bio-CF with the same method
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mentioned above.
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2.2 MEC set-up and inoculums
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Continuous bulk 3D structured carbon aerogel (CA) material was synthesized by
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polymerization method with 1, 3-dihydroxy benzene and formaldehyde, and dried at
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ambient temperature and pressure. The as-prepared CA bio-anode was then
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inoculated with the anaerobic sludge and operated in electricity generation mode as
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sequencing batch. The microbial CA electrode was accomplished till the stable
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anode potential was obtained for three consecutive times. A MEC with two chambers
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connected of 28 mL liquid was connected by a cation exchange membrane. The
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anode chamber was filled with phosphate buffer solution containing 20 mM of
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ACCEPTED MANUSCRIPT CH3COONa and trace elements, while the cathode chamber with phosphate buffer
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solution containing 50 mM of K3[Fe(CN)6. Two electrodes were connected with a
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resistance of 1 kΩ for determining the cell voltage. The solutions of both chambers
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were replaced per 48 h and then purged with nitrogen gas to remove the dissolved
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oxygen, thus keeping anaerobic condition. Commercial carbon fiber felt was
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calcined under 450 °C for 30 min, tailored into the same size as carbon aerogel and
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cultured into Bio-CF in the same method aforementioned.
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2.3 Characterization
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The morphologies of the samples were characterized by a field emission scanning
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electron microscope (FE-SEM, Hitachi S-4800, Hitachi Co., Japan). The chemical
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composition was characterized by X-ray photoelectron spectroscopy (XPS, PHI
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5600 XPS spectroscopy, Ulvac-Phi Co., Japan). The water contact angle on the
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surface of CA and CF electrodes was measured by a contact angle meter (JC2000A,
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Zhongchen, China). All electrochemical measurements were executed in a
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three-electrode cell system of the CHI 660c (Chenhua Co., China) electrochemical
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workstation at the ambient temperature. A Pt foil and a saturated calomel electrode
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(SCE) were applied as the counter electrode and the reference electrode, respectively.
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The structural features of the CA sample were explored by nitrogen
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adsorption-desorption isotherms using a BET analyzer (TRISTAR 3000,
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Micromeritics
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Co.,
U.S.).
Electrochemical
impedance
spectroscopy
(EIS)
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range from 105 to 10-2 Hz. The hydrogen production from MEC was detected by an
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online gas chromatography (GC, GC7900, Tianmei Co., China) with a thermal
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conductivity detector.
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3. Results and Discussion
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3.1 Surface morphology and composition characteristics of the Bio-CA anode
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The procedure for constructing the microbial CA anode electrode is illustrated
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in Figure 1, by a modified method[36]. The wet aerogel was transformed to carbon
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aerogel (CA) in a tubular oven via pyrolysis and activation. As shown in Figure
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2a-d, as-prepared anode materials are clearly observed from the SEM images.
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Compared to the CF electrode (Figure 2c), Figure 2a shows that the surface of CA
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was relatively rough and possessed porous structure so that it can provide a great
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quantity of attachment points for bacteria. Moreover, such porous structure is
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conducive to the absorption of the organic species[37]. As shown in Figure 3, CA
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achieved the specific surface area up to 566 m2/g and exhibited a wide pore size
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distribution (<5 nm and 50 nm), in agreement with the results of SEM images. In
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order to further demonstrate the porous structure for bacteria attachment, the Bio-CA
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and Bio-CF electrodes samples were subjected to SEM imaging. Figure 2b shows
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that the bacteria attached to the surface and channel of CA substrate were uniformly
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ACCEPTED MANUSCRIPT dispersed due to the roughness and porous structure of CA, which conduces to the
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adsorption of organic species for the utilization of the bacteria[37, 38]. In contrast,
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the bacteria were aggregated on certain locations of the CF surface which showed
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the smooth surface and non-porous structure (Figure 2d). Moreover, the amount of
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incubated bacteria attached on the CA electrode was more than that of CF electrode
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at same area (Figure 2c and 2d). This result indicates that the roughness and porous
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structure of CA were suitable for the attachment and growth of bacteria.
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The graphitization degree of CA and CF electrodes are analyzed using Raman
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spectrum shown in Figure 4a. The peaks around wavenumber of 1355 and 1592
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cm-1 belong to the characteristic D (defect) and G (graphitic) bands of carbon,
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respectively. The D band ( 1355 cm-1, the breathing mode of κ-point phonons of A1g
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symmetry) and the G band (the E2g phonon of sp2 carbon atoms) reflect the disorder
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degree of the carbon materials and the graphitization degree of the carbon materials,
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respectively. The results indicate that the CA had a greater graphitization degree
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from the relative peak width compared with the CF. Meanwhile, the chemical states
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of C and O are analyzed by XPS. The obtained CA mainly contained C and O
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elements from the XPS survey spectrum (Figure 4b). For the CA and CF, both C 1s
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spectrum (Figure 4c and 4d) could be deconvoluted into four carbon species, i.e.,
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C-C (284.5 eV), C-O (285.0 eV), C=O (287.2 eV), and O-C=O (288.6 eV),
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respectively. Moreover, the high C/O atom ratio of the CA implies its good electron
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conductivity, which was proven in Table S1. These results also confirm that the CA
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had a greater graphitization degree than that of CF, which is in agreement with the
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Raman results. The wettability of CA and CF electrodes was investigated by measuring water
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contact angles. Figure 5a-e show that the water contact angle on the CA electrode
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decreases with different contact time. On the contrary, the water contact angle on the
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CF electrode did not change in a long-term measurement (Figure 5f-j). These results
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indicate that CA is more hydrophilic than CF[36]. Thus, CA is considered as better
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electrode than CF due to its greater graphitization degree and hydrophilic interaction,
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according to the analytical results of Raman and XPS spectrum.
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3.1 Electrochemical activities of the the Bio-CA anode
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Therefore, the electrochemical performances of as-prepared electrodes for
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MECs were also evaluated. By varying the external load, the polarization curves and
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power density curves were recorded for further evaluation of MECs performance[39].
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As shown in Figure 6a, a smaller polarization curve slope of Bio-CA was obtained,
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which indicated a less electric resistance. Besides, the power density of MEC with
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Bio-CA anode reached up to 4890 mW/m2, which was 4.67 times higher than that of
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Bio-CF (1047 mW/m2) anode, indicating that Bio-CA displayed a stronger electric
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production capacity[39, 40]. In addition, the direct contact-based EET was examined
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by cyclic voltammetry (CV) analysis. CV test for microbial anode (Figure 6b)
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further showed that redox peaks occurred after microorganism attachment, indicating
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ACCEPTED MANUSCRIPT that the microorganism possessed electrochemical activity[39]. OmcZ is an outer
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membrane protein (cytochrome c) with 8 hemes for direct electron transfer of
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microbes and possesses a wide redox potential ranging from -0.66 to -0.30 V (vs
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SCE)[41]. Potential peaks of the MEC with Bio-CF were at -0.39 V, -0.33 V, and
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-0.24 V (vs SCE), respectively. Among them, peak at -0.39 V was corresponded to
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the cytoplasmic cytochrome c (PpcA) extracted by G. Sulfurreducens[42]. Moreover,
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the electrochemical impedance spectroscopy (EIS) measurement (Figure 6c) showed
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that after bacteria attachment, the charge transfer resistance (Rct) of CA reduced from
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12 Ω to 1 Ω, and 300 Ω to 43 Ω for CF electrode. And, the impedance data was fitted
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with an electrical model as shown in Figure S1. This result manifests that the
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attachment of microorganisms can distinctly reduce Rct and that CA is more
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conducive and exhibit more rapid charge transfer than CF[29, 43-45]. The potential
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change of anodes after refilling nutrient solution (0.41 g/L acetate sodium) for
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microbes is shown in Figure 6d. The average potential of CA, CF, Bio-CA and
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Bio-CF reached +0.408 V, +0.393 V, -0.266 V and -0.227 V (vs SHE), respectively,
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which indicated that the attachment of bacteria reduced the anode potential by ~0.6 V.
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Compared to bare CF electrode, a slightly higher anode potential of CA was
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observed. With the bacteria attached, the potential of Bio-CA was lower than Bio-CF
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by 39 mV. Additionally, the potential of Bio-CF firstly increased from +0.28 V to
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~+0.41V in the initial 5 hours after refilling nutrient solution, then declined slowly
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and reached the minimum value of -0.248 V in 2.9 h. There was no obvious potential
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increase with Bio-CA after replacing the nutrient solution. The potential of Bio-CA
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after 2.9 h. Notably, Bio-CA enabled the microbes to rapidly enter the electricity
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generating state and consequently lower the anode potential, suggesting that CA is
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an excellent culture substrate for the breeding and metabolism of microbes and has a
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better electricity generation compared with Bio-CF[44, 46].
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3.3 The mechanisms of the extracellular electron transfer on Bio-CA anode and
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the performance of MEC
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Both schematic diagrams of the Bio-CA and Bio-CF anode electrode were
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clearly presented (Figure 7a and 7b). The high-resolution SEM images of CA and
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CF electrodes were shown in Figure 2b and 2d. The bacterial directly attached on
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the surface and channel of CA (Figure 2b) enhanced the affinitive mechanical
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contact, thus improved the direct contact-based EET (Figure 7a)[39, 47]. On the
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contrary, the electrons produced by the bacterial were far away from the CF
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electrode (Figure 2d) and could not efficiently inject into electrode but only went
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along the adjacent nonconductive bacteria cells, leading to a poor EET efficiency
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(Figure 7b)[39, 47]. Therefore, CA electrode optimized the dispersion and
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attachment of bacteria, which was beneficial to the enhancement of the direct
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contact-based EET, and thus improved performance of Bio-CA anode electrode[43].
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Therefore, an enhanced MEC device is constructed with Bio-CA anode coupled
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to Pt cathode. Bio-CA anode could enhance EET and Pt cathode could improve H2
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shown in Table S2. The results showed that the MEC with Bio-CA anode coupled to
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Pt cathode showed H2 production (0.0083 µmol·cm-2·h-1) under the low voltage (190
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mV), and (0.37 µmol·cm-2·h-1) 5 times higher than that (0.07 µmol·cm-2·h-1) of CF
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anode under the voltage (300 mV). This enhanced H2 production on advanced MEC
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was mainly owing to Bio-CA anode. Moreover, the prepared CA anode didn’t
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change evidently after a long time test (as shown in Figure S2). First, the
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mesoporous structure of CA anode enables bacteria to stretch into the porous surface
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and channel of the electrode[48] and form a 3D network structure inside the CA,
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enhancing the direct based-contact EET and the stability of microbial attachment.
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Second, the existence of micropores in CA is conducive to the adsorption of
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nutrients for bacteria and enrichment of electronic mediators (such as lactochrome)[6,
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38], which could be applied as indirect electron transfer. Third, the excellent
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bioelectrocatalytic performance of Bio-CA is attributed to the highly matched and
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intensive interaction between microbial and the carbon aerogel electrode. These
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results fully prove that the self-supported microbial CA anode is a powerful strategy
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for improving the performance of MECs.
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4. Conclusion
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In conclusion, a novel strategy of 3D-CA anode electrode was successfully
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synthesized and applied in the MEC system for efficient hydrogen production. The
ACCEPTED MANUSCRIPT obtained CA anode can efficiently optimize the dispersion and attachment of bacteria
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and promote electron transfer due to its high specific surface area, 3D porous
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structure, perfect electrical conductivity, and biocompatibility porosity. Moreover,
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CA anode could achieve direct contact-based EET and bio-catalysis owing to its 3D
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hierarchical conductive framework. Meanwhile, CA anode coupled to the Pt cathode
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(0.0083 µmol·cm-2·h-1) showed greater hydrogen production performance than that
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of CF anode (0 µmol·cm-2·h-1) under the low voltage (190 mV). This study is of
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great theoretical significance and has estimable application prospect for electrolytic
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hydrogen evolution under low energy consumption with energy recycling.
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Acknowledgements
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This work was supported by the National Natural Science Foundations of China
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(NSFC, no. 21477085 and 21537003), the China Postdoctoral Science Foundation
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(2017M620169), and Science & Technology Commission of Shanghai Municipality
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(14DZ2261100).
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Figure 1. Schematic of the microbial carbon aerogel electrode preparation
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Figure 3. N2 adsorption-desorption isotherms curves of CA, insert is the pore size
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Figure 2. SEM images of CA and CF electrodes: (a, c) blank CA and CF electrodes;
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(b, d) biofilms attached on the CA and CF electrodes, respectively
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Figure 4. (a) The Raman spectrum of the CA and CF samples, and XPS spectra of
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the CA and CF samples: (b) Survey spectra; (c, d) High-resolution XPS spectra of
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C1s.
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Figure 5. Water contact angle on the CA (a-e) and CF (f-j) at different time,
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respectively
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Figure 6. (a) Polarization and power-density curves of MECs with different
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electrodes; (b) CV curves of Bio-CA and Bio-CF electrodes; (c) The Nyquist curves
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of CA and CF electrodes with and without bacterial; (d) Microbial anode
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potential-time curves of CA and CF electrodes
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Figure 7. (a, b) Schematic depicting the direct contact-based EET mechanism of
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Bio-CA anode and Bio-CF electrodes, respectively.
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ACCEPTED MANUSCRIPT Research Highlights CA electrode maintains the perfect electrical conductivity and biocompatibility porosity CA can enhance direct contact-based EET and bio-catalysis.
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Mechanism of direct contact-based EET was elucidated.
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Hydrogen can be rapidly produced under applied voltage of 0.19 V in such MEC.
S0013-4686(19)30356-1
DOI:
https://doi.org/10.1016/j.electacta.2019.02.099
Reference:
EA 33690
To appear in:
Electrochimica Acta
Received Date: 2 April 2018 Revised Date:
22 February 2019
Accepted Date: 25 February 2019
Please cite this article as: W.-K. Wang, B. Tang, J. Liu, H. Shi, Q. Xu, G. Zhao, Self-supported microbial carbon aerogel bioelectrocatalytic anode promoting extracellular electron transfer for efficient hydrogen evolution, Electrochimica Acta (2019), doi: https://doi.org/10.1016/j.electacta.2019.02.099. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. 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.
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Graphical Abstract
ACCEPTED MANUSCRIPT Self-supported Microbial Carbon Aerogel Bioelectrocatalytic Anode Promoting Extracellular Electron Transfer for Efficient Hydrogen Evolution Wei-Kang Wang†,§, Bo Tang†,§, Jian Liu†,§, Huijie Shi†, Qunjie Xu*,‡, , Guohua
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Zhao*,†,
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Shanghai Key Lab of Chemical Assessment and Sustainability, Department of Chemistry, Tongji University, Shanghai 200092, People’s Republic of China. Shanghai Key Laboratory of Materials Protection and Advanced Materials in
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Electric Power, Shanghai University of Electric Power, Shanghai 200090, China. Shanghai Institute of Pollution Control and Ecological Security,
W.K. Wang, B.Tang and J. Liu: These authors contributed equally.
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Shanghai200092, P.R. China.
Corresponding author:
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*E-mail: [email protected], [email protected]
ACCEPTED MANUSCRIPT ABSTRACT: Hydrogen production by microbial electrolysis cells (MECs) is an
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attractive and promising technology for sustainable energy. The bioelectrocatalytic
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activity of bioanode plays an essential role in improving the supply of electrons to
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cathode. Herein, a self-supported three-dimensional (3D) porous carbon aerogel (CA)
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bioanode was successfully applied in a MEC system for efficient hydrogen
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production. The 3D porous structure of CA greatly increased the bacterial incubation,
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then favored the extracellular electron transfer (EET) owing to its high specific
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surface area, excellent electrical conductivity and enhanced interaction with
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microbial. As a result, the hydrogen production of Bio-CA||Pt (0.37 µmol·cm-2·h-1)
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was 5 times higher than that of bio-carbon fiber (Bio-CF)||Pt (0.007µmol·cm-2·h-1) at
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the bias voltage of 0.3 V. Such a MEC with self-supported 3D porous microbial CA
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bioanode as a promising biotechnology will be further investigated for pollutant
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degradation and hydrogen production.
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Keywords: self-supported; carbon aerogel; bioelectrocatalytic; extracellular electron
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transfer; hydrogen evolution;
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ACCEPTED MANUSCRIPT 1. Introductin
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Hydrogen is a typical sustainable energy carrier for developing low carbon emission
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economy. Microbial electrolysis cells (MECs) are considered as a sort of
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environmental biotechnologies simultaneously for wastewater treatment and
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hydrogen production[1-3] for its high efficiency, cost effectiveness, and utilization of
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bio-electrons[4]. However, MECs for hydrogen production has suffered the low
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power density of bio-anode so far. Numerous efforts have been made to improve the
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performance of MECs via exploring the limiting factors[5], such as anode
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materials[6, 7], proton exchange membrane[8], efficiency of cathode[9] and so
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on[10-14]. And, the electron transfer efficiency of bio-anode has been recognized to
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be the key factor to enhancing the performance of MECs.
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Thus, developing of bio-anode materials with an excellent conductivity, high
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surface area, three-dimensional (3D) structure, and good bio-compatibility is
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promising solution to the problem. On conventional bio-anode materials in MECs
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such as carbon cloth (CC) and carbon fiber (CF)[15-18], the oxidation of organic
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species occurs with sluggish kinetics, leading to relatively low current densities and
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poor electron transfer to the cathode[3]. Aimed at improving the electron transfer on
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bio-anodes, carbon nanotube and graphene have been applied to modify bio-anodes
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owing to their good electrical conductivity[19]. Furthermore, 3D porous materials,
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such as carbon nanotube−textile and graphene sponges, have also been proved to
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improve current densities via increasing the quantity of incubated bacteria[20-25].
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However, besides of the high cost and instability in anaerobic conditions, more
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ACCEPTED MANUSCRIPT importantly, the usage of adhesives that immobilize electron conductor materials
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onto the anode greatly increased interface contact resistance, resulting in the limited
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electron transfer[26, 27]. Thus, some researches have been done for preparation of
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bio-anode by using biomass instead of commercial carbon-based materials[28, 29].
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Therefore, self-supported porous carbon bio-anode with high surface area, the
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abundance, 3D structure, environmental compatibility, chemical inertness, and high
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conductivity are desired for application of MECs.
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To date, carbon aerogels (CAs) are widely used as electrode materials[30-32].
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The morphologies and properties of CAs can be controled by the sol-gel reaction
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chemistry[32]. Thus, CAs exhibit not only have anaerobic stability and little
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interfacial contact resistance, but also the perfect electrical conductivity and
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biocompatible porosity derived from the tunable 3D hierarchical morphology with
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ultrafine sizes and conductive framework[31, 33]. For instance, electrical
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conductivity in CAs occurs through the movement of charge carriers via individual
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carbon particles and ‘‘hopping’’ of these carriers between adjacent carbon
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particles[31]. Meanwhile, CAs possess abundant micro and mesoporous structure
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with large BET surface area up to 500~600 m2/g, which benefits microbial
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attachment and the adsorption of organic species[34, 35].
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In this work, a self-supported 3D CA bio-anode electrode was successfully
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synthesized and applied in a MEC system. Also, the mechanism of enhanced direct
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contact-based EET and bio-catalysis on self-supported 3D CA bioanode was
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explored. Moreover, the current density and bio-anode potential of MEC with HER
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self-supported 3D CA bio-anode to achieve the efficient hydrogen evolution from
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MEC system. Meanwhile, these resluts may provide novel ideas of designing new
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systems for hydrogen production from bio-electro-catalysis.
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2. Materials and Methods
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2.1 Fabrication of microbial carbon aerogel anode
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The fabrication procedures of microbial carbon aerogel electrode are schematically
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shown in Figure 1a. 1, 3-dihydroxy benzene, formaldehyde, deionized water, and
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sodium carbonate were homogeneously mingled at a molar ratio of 1:2:17.5: 0.0008
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till colorless and transparent solution was obtained. Later the mixture was transferred
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into a cubical glass with the interlayer distance about of 5 mm, followed by aged at
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30 °C for 24 h, 50 °C for 24 h, and 90 °C for 72 h consecutively. The consequent
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organic wet gel was immerged into acetone for 72 h to remove water. Then, the wet
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aerogel was transformed to carbon aerogel (CA) in a tubular oven via pyrolysis, kept
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at 950 oC for 4 h under N2 atmosphere with the flow rate of 100 mL min-1 and the
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heating rate of 1 oC min-1.
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The as-prepared CA was polished with abrasive paper (320#) into the size of 13
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mm × 28 mm × 3 mm, then it was attached with a titanium wire (d=0.5 mm) as the
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conductor. A dual chambered MEC was constructed with two glass bottles connected
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anode was inoculated with the anaerobic sludge from a local pond. The anode
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chamber was filled with nutrient solution (per 1 L of deionized water: 1.64 g
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CH3COONa, 18.30 g K2HPO4·3H2O, 2.70 g KH2PO4, 0.5 g NaCl, 0.1 g NH4Cl, 0.1
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g MgSO4·7H2O, and 1 mL trace elements). The phosphate buffer solution in the
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cathode contained 16.46 g L-1 K3[Fe(CN)6]; 18.30 g L-1 K2HPO4·3H2O and 2.70 g
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L-1 KH2PO4). The solutions of both chambers were replaced per 48 h and then
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purged with N2 gas to remove the dissolved oxygen, to keep anaerobic condition.
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Commercial carbon fiber felt was calcined under 450 °C for 30 min, tailored into the
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same size as carbon aerogel, and then cultured into Bio-CF with the same method
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mentioned above.
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2.2 MEC set-up and inoculums
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Continuous bulk 3D structured carbon aerogel (CA) material was synthesized by
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polymerization method with 1, 3-dihydroxy benzene and formaldehyde, and dried at
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ambient temperature and pressure. The as-prepared CA bio-anode was then
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inoculated with the anaerobic sludge and operated in electricity generation mode as
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sequencing batch. The microbial CA electrode was accomplished till the stable
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anode potential was obtained for three consecutive times. A MEC with two chambers
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connected of 28 mL liquid was connected by a cation exchange membrane. The
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anode chamber was filled with phosphate buffer solution containing 20 mM of
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solution containing 50 mM of K3[Fe(CN)6. Two electrodes were connected with a
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resistance of 1 kΩ for determining the cell voltage. The solutions of both chambers
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were replaced per 48 h and then purged with nitrogen gas to remove the dissolved
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oxygen, thus keeping anaerobic condition. Commercial carbon fiber felt was
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calcined under 450 °C for 30 min, tailored into the same size as carbon aerogel and
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cultured into Bio-CF in the same method aforementioned.
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2.3 Characterization
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The morphologies of the samples were characterized by a field emission scanning
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electron microscope (FE-SEM, Hitachi S-4800, Hitachi Co., Japan). The chemical
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composition was characterized by X-ray photoelectron spectroscopy (XPS, PHI
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5600 XPS spectroscopy, Ulvac-Phi Co., Japan). The water contact angle on the
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surface of CA and CF electrodes was measured by a contact angle meter (JC2000A,
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Zhongchen, China). All electrochemical measurements were executed in a
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three-electrode cell system of the CHI 660c (Chenhua Co., China) electrochemical
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workstation at the ambient temperature. A Pt foil and a saturated calomel electrode
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(SCE) were applied as the counter electrode and the reference electrode, respectively.
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The structural features of the CA sample were explored by nitrogen
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adsorption-desorption isotherms using a BET analyzer (TRISTAR 3000,
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Micromeritics
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Co.,
U.S.).
Electrochemical
impedance
spectroscopy
(EIS)
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range from 105 to 10-2 Hz. The hydrogen production from MEC was detected by an
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online gas chromatography (GC, GC7900, Tianmei Co., China) with a thermal
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conductivity detector.
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3. Results and Discussion
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3.1 Surface morphology and composition characteristics of the Bio-CA anode
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The procedure for constructing the microbial CA anode electrode is illustrated
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in Figure 1, by a modified method[36]. The wet aerogel was transformed to carbon
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aerogel (CA) in a tubular oven via pyrolysis and activation. As shown in Figure
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2a-d, as-prepared anode materials are clearly observed from the SEM images.
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Compared to the CF electrode (Figure 2c), Figure 2a shows that the surface of CA
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was relatively rough and possessed porous structure so that it can provide a great
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quantity of attachment points for bacteria. Moreover, such porous structure is
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conducive to the absorption of the organic species[37]. As shown in Figure 3, CA
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achieved the specific surface area up to 566 m2/g and exhibited a wide pore size
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distribution (<5 nm and 50 nm), in agreement with the results of SEM images. In
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order to further demonstrate the porous structure for bacteria attachment, the Bio-CA
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and Bio-CF electrodes samples were subjected to SEM imaging. Figure 2b shows
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that the bacteria attached to the surface and channel of CA substrate were uniformly
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adsorption of organic species for the utilization of the bacteria[37, 38]. In contrast,
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the bacteria were aggregated on certain locations of the CF surface which showed
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the smooth surface and non-porous structure (Figure 2d). Moreover, the amount of
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incubated bacteria attached on the CA electrode was more than that of CF electrode
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at same area (Figure 2c and 2d). This result indicates that the roughness and porous
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structure of CA were suitable for the attachment and growth of bacteria.
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The graphitization degree of CA and CF electrodes are analyzed using Raman
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spectrum shown in Figure 4a. The peaks around wavenumber of 1355 and 1592
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cm-1 belong to the characteristic D (defect) and G (graphitic) bands of carbon,
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respectively. The D band ( 1355 cm-1, the breathing mode of κ-point phonons of A1g
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symmetry) and the G band (the E2g phonon of sp2 carbon atoms) reflect the disorder
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degree of the carbon materials and the graphitization degree of the carbon materials,
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respectively. The results indicate that the CA had a greater graphitization degree
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from the relative peak width compared with the CF. Meanwhile, the chemical states
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of C and O are analyzed by XPS. The obtained CA mainly contained C and O
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elements from the XPS survey spectrum (Figure 4b). For the CA and CF, both C 1s
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spectrum (Figure 4c and 4d) could be deconvoluted into four carbon species, i.e.,
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C-C (284.5 eV), C-O (285.0 eV), C=O (287.2 eV), and O-C=O (288.6 eV),
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respectively. Moreover, the high C/O atom ratio of the CA implies its good electron
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conductivity, which was proven in Table S1. These results also confirm that the CA
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had a greater graphitization degree than that of CF, which is in agreement with the
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Raman results. The wettability of CA and CF electrodes was investigated by measuring water
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contact angles. Figure 5a-e show that the water contact angle on the CA electrode
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decreases with different contact time. On the contrary, the water contact angle on the
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CF electrode did not change in a long-term measurement (Figure 5f-j). These results
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indicate that CA is more hydrophilic than CF[36]. Thus, CA is considered as better
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electrode than CF due to its greater graphitization degree and hydrophilic interaction,
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according to the analytical results of Raman and XPS spectrum.
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3.1 Electrochemical activities of the the Bio-CA anode
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Therefore, the electrochemical performances of as-prepared electrodes for
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MECs were also evaluated. By varying the external load, the polarization curves and
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power density curves were recorded for further evaluation of MECs performance[39].
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As shown in Figure 6a, a smaller polarization curve slope of Bio-CA was obtained,
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which indicated a less electric resistance. Besides, the power density of MEC with
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Bio-CA anode reached up to 4890 mW/m2, which was 4.67 times higher than that of
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Bio-CF (1047 mW/m2) anode, indicating that Bio-CA displayed a stronger electric
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production capacity[39, 40]. In addition, the direct contact-based EET was examined
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by cyclic voltammetry (CV) analysis. CV test for microbial anode (Figure 6b)
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further showed that redox peaks occurred after microorganism attachment, indicating
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ACCEPTED MANUSCRIPT that the microorganism possessed electrochemical activity[39]. OmcZ is an outer
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membrane protein (cytochrome c) with 8 hemes for direct electron transfer of
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microbes and possesses a wide redox potential ranging from -0.66 to -0.30 V (vs
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SCE)[41]. Potential peaks of the MEC with Bio-CF were at -0.39 V, -0.33 V, and
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-0.24 V (vs SCE), respectively. Among them, peak at -0.39 V was corresponded to
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the cytoplasmic cytochrome c (PpcA) extracted by G. Sulfurreducens[42]. Moreover,
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the electrochemical impedance spectroscopy (EIS) measurement (Figure 6c) showed
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that after bacteria attachment, the charge transfer resistance (Rct) of CA reduced from
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12 Ω to 1 Ω, and 300 Ω to 43 Ω for CF electrode. And, the impedance data was fitted
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with an electrical model as shown in Figure S1. This result manifests that the
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attachment of microorganisms can distinctly reduce Rct and that CA is more
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conducive and exhibit more rapid charge transfer than CF[29, 43-45]. The potential
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change of anodes after refilling nutrient solution (0.41 g/L acetate sodium) for
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microbes is shown in Figure 6d. The average potential of CA, CF, Bio-CA and
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Bio-CF reached +0.408 V, +0.393 V, -0.266 V and -0.227 V (vs SHE), respectively,
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which indicated that the attachment of bacteria reduced the anode potential by ~0.6 V.
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Compared to bare CF electrode, a slightly higher anode potential of CA was
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observed. With the bacteria attached, the potential of Bio-CA was lower than Bio-CF
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by 39 mV. Additionally, the potential of Bio-CF firstly increased from +0.28 V to
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~+0.41V in the initial 5 hours after refilling nutrient solution, then declined slowly
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and reached the minimum value of -0.248 V in 2.9 h. There was no obvious potential
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increase with Bio-CA after replacing the nutrient solution. The potential of Bio-CA
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after 2.9 h. Notably, Bio-CA enabled the microbes to rapidly enter the electricity
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generating state and consequently lower the anode potential, suggesting that CA is
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an excellent culture substrate for the breeding and metabolism of microbes and has a
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better electricity generation compared with Bio-CF[44, 46].
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3.3 The mechanisms of the extracellular electron transfer on Bio-CA anode and
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the performance of MEC
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Both schematic diagrams of the Bio-CA and Bio-CF anode electrode were
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clearly presented (Figure 7a and 7b). The high-resolution SEM images of CA and
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CF electrodes were shown in Figure 2b and 2d. The bacterial directly attached on
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the surface and channel of CA (Figure 2b) enhanced the affinitive mechanical
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contact, thus improved the direct contact-based EET (Figure 7a)[39, 47]. On the
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contrary, the electrons produced by the bacterial were far away from the CF
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electrode (Figure 2d) and could not efficiently inject into electrode but only went
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along the adjacent nonconductive bacteria cells, leading to a poor EET efficiency
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(Figure 7b)[39, 47]. Therefore, CA electrode optimized the dispersion and
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attachment of bacteria, which was beneficial to the enhancement of the direct
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contact-based EET, and thus improved performance of Bio-CA anode electrode[43].
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Therefore, an enhanced MEC device is constructed with Bio-CA anode coupled
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to Pt cathode. Bio-CA anode could enhance EET and Pt cathode could improve H2
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shown in Table S2. The results showed that the MEC with Bio-CA anode coupled to
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Pt cathode showed H2 production (0.0083 µmol·cm-2·h-1) under the low voltage (190
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mV), and (0.37 µmol·cm-2·h-1) 5 times higher than that (0.07 µmol·cm-2·h-1) of CF
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anode under the voltage (300 mV). This enhanced H2 production on advanced MEC
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was mainly owing to Bio-CA anode. Moreover, the prepared CA anode didn’t
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change evidently after a long time test (as shown in Figure S2). First, the
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mesoporous structure of CA anode enables bacteria to stretch into the porous surface
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and channel of the electrode[48] and form a 3D network structure inside the CA,
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enhancing the direct based-contact EET and the stability of microbial attachment.
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Second, the existence of micropores in CA is conducive to the adsorption of
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nutrients for bacteria and enrichment of electronic mediators (such as lactochrome)[6,
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38], which could be applied as indirect electron transfer. Third, the excellent
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bioelectrocatalytic performance of Bio-CA is attributed to the highly matched and
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intensive interaction between microbial and the carbon aerogel electrode. These
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results fully prove that the self-supported microbial CA anode is a powerful strategy
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for improving the performance of MECs.
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4. Conclusion
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In conclusion, a novel strategy of 3D-CA anode electrode was successfully
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synthesized and applied in the MEC system for efficient hydrogen production. The
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and promote electron transfer due to its high specific surface area, 3D porous
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structure, perfect electrical conductivity, and biocompatibility porosity. Moreover,
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CA anode could achieve direct contact-based EET and bio-catalysis owing to its 3D
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hierarchical conductive framework. Meanwhile, CA anode coupled to the Pt cathode
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(0.0083 µmol·cm-2·h-1) showed greater hydrogen production performance than that
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of CF anode (0 µmol·cm-2·h-1) under the low voltage (190 mV). This study is of
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great theoretical significance and has estimable application prospect for electrolytic
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hydrogen evolution under low energy consumption with energy recycling.
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Acknowledgements
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This work was supported by the National Natural Science Foundations of China
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(NSFC, no. 21477085 and 21537003), the China Postdoctoral Science Foundation
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(2017M620169), and Science & Technology Commission of Shanghai Municipality
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(14DZ2261100).
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Figure 1. Schematic of the microbial carbon aerogel electrode preparation
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Figure 3. N2 adsorption-desorption isotherms curves of CA, insert is the pore size
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distribution
Figure 2. SEM images of CA and CF electrodes: (a, c) blank CA and CF electrodes;
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(b, d) biofilms attached on the CA and CF electrodes, respectively
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Figure 4. (a) The Raman spectrum of the CA and CF samples, and XPS spectra of
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the CA and CF samples: (b) Survey spectra; (c, d) High-resolution XPS spectra of
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C1s.
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Figure 5. Water contact angle on the CA (a-e) and CF (f-j) at different time,
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respectively
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Figure 6. (a) Polarization and power-density curves of MECs with different
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electrodes; (b) CV curves of Bio-CA and Bio-CF electrodes; (c) The Nyquist curves
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of CA and CF electrodes with and without bacterial; (d) Microbial anode
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potential-time curves of CA and CF electrodes
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Figure 7. (a, b) Schematic depicting the direct contact-based EET mechanism of
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Bio-CA anode and Bio-CF electrodes, respectively.
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ACCEPTED MANUSCRIPT Research Highlights CA electrode maintains the perfect electrical conductivity and biocompatibility porosity CA can enhance direct contact-based EET and bio-catalysis.
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Mechanism of direct contact-based EET was elucidated.
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Hydrogen can be rapidly produced under applied voltage of 0.19 V in such MEC.