Novel gas diffusion cloth bioanodes for high-performance methane

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Energy and the Environment

Novel gas diffusion cloth bioanodes for highperformance methane powered microbial fuel cells Linpeng Yu, Zujie Yang, Qiuxiang He, Raymond J Zeng, Yanan Bai, and Shungui Zhou Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b04311 • Publication Date (Web): 28 Nov 2018 Downloaded from http://pubs.acs.org on December 1, 2018

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Environmental Science & Technology

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Novel gas diffusion cloth bioanodes for high-performance methane powered microbial

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fuel cells

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Linpeng Yua, Zujie Yanga, Qiuxiang Hea, Raymond J. Zenga,b, Yanan Baia,b, Shungui Zhoua,*

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a

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Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou 350002, China

Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of

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b

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Science and Technology of China, Hefei 230026, PR China

CAS Key Laboratory for Urban Pollutant Conversion, Department of Chemistry, University of

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* Corresponding author: Shungui Zhou

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Email: [email protected]

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Tel: +86 591 86397843, Fax: +86 591 86397843

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TOC abstract

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ACS Paragon Plus Environment


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Abstract

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Microbial fuel cells (MFCs) are a promising technology that converts chemical energy into

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electricity. However, up to now only few MFCs have been powered by gas fuels such as methane and

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their limited performance is still challenged by the low solubility and bioavailability of gases. Here

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we developed a gas diffusion cloth (GDC) anode to significantly enhance the performance of

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methane-powered MFCs. The GDC anode was constructed by simply coating waterproof GORE-TEX

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cloth with conductive carbon cloth in one step. After biofilm enrichment, the GDC anodes obtained a

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methane-dependent current up to 1130.2 mA m-2, which was 165.2 times higher than conventional

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carbon cloth (CC) anodes. Moreover, MFCs equipped with GDC anodes generated a maximum power

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density of 419.5 mW m-2. Illumina high-throughput sequencing revealed that the GDC anode biofilm

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was dominated mainly by Geobacter, in contrast with the most abundant Methanobacterium in

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planktonic cells. It is hypothesized that Methanobacterium reversed the methanogenesis process by

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transferring electrons to the anodes and Geobacter generated electricity via the intermediates (e.g.

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acetate) of anaerobic methane oxidation. Overall, this work provides an effective route in preparing

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facile and cost-effective anodes for high-performance methane MFCs.

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1. Introduction

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Microbial fuel cells (MFCs) are energy-producing devices that directly convert organic

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compounds into electricity using microorganisms as the catalysts.1 Microorganisms in MFCs termed

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electroactive bacteria (EABs) perform the oxidation of organics and donate electrons to anodes via a

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pathway of extracellular electron transfer (EET).2,3 EET from EABs to the anodic surface generally

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follows two major pathways: i) direct EET via bacterial outer membrane cytochromes or conductive

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pili structures; 4,5 and ii) indirect EET via endogenous or exogenous redox-active electron shuttles.6 A

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wide variety of dissolved substrates ranging from macromolecular carbohydrates (starch, lignose, etc.)

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to simple compounds (e.g. acetate, formate), have been utilized for electricity generation in MFCs.7-10

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However, MFCs powered by gaseous substrates such as methane and hydrogen have emerged only in

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recent years and remained largely unexplored.

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Methane is the second most important greenhouse gas as well as a widespread renewable

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energy.11,12 It was estimated that 110–260 Tg of methane is released from natural wetlands to the

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atmosphere every year.13 Extracting electric energy from methane at source via the MFC technology

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will not only control its greenhouse effect, but also alleviate the global energy crisis. Besides, this

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technology is more environmentally-friendly and milder than methane incineration power generation.

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Another advantage is that in situ methane-powered MFCs would reduce the cost of methane storage

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and transportation as well as the leakage in these processes. In comparison with the liquid-powered

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(e.g. wastewater) MFCs, methane-powered MFCs have shown some noticeable advantages. For

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example, methane can be supplied to MFCs in a highly compressed state, leading to higher electricity

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productivity per unit volume fuel. The product of methane-powered MFCs is mainly CO2 and H2O,

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which decrease the spacial demand of outflows. These properties will benefit the structural scale-up of

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MFCs. 3



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As a high energy dense compound, methane has been suggested to be a potential MFC substrate

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when catalyzed by methanogens or methanotrophs.14,15 For example, McAnulty et al. have engineered

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a methanogen Methanosarcina acetivorans to reverse methanogenesis for converting methane to

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acetate, which was then used by G. sulfurreducens and sludge microbes to give a maximum power of

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168 mW m-2.15 This was further enhanced to 5216 mW m-2 by changing the adding order of the

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consortium strains and by supplemented electron carriers (e.g. humic acids).16 Ding et al. used

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methane as the MFC substrate to decouple methanotrophic archaea from denitrifying,

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methane-oxidizing bacteria (Methylomirabilis genus).17 Unfortunately, the measurement of

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appreciable methane-electricity conversion in the aforementioned system was not practical since the

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maximum cell voltage (0.025 V) was close to the background. In addition, MFCs based on aerobic

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methane oxidation was also reported, with a maximum power density of 62 mW m-2.18 The syntrophic

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archaea-bacteria consortium was suggested to play a critical role in coupling methane oxidation to the

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anode reduction.18 Nevertheless, disputes still exist in the archaeal methane metabolisms and coupling

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pathways, and the underlying mechanisms remain not well understood. Some studies hypothesized

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that anaerobic oxidation of methane (AOM) occurred via reverse methanogenesis with intermediates

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(H2, formate, acetate, etc.) as electron carriers19,20, while others suggested that direct interspecies

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electron transfer (DIET) via cytochromes was the principal AOM mechanism21.

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However, the current methane-powered MFCs are still challenged by the low performance that is

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far from industrial or commercial applications. One main bottleneck is probably attributed to the low

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solubility and mass transfer coefficient of methane. Direct aeration of methane into the AOM

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bioreactors requires a large amount of energy and likely lead to the leakage of methane during

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operation. To resolve this problem, a few studies have employed hollow fiber membranes (HFMs) to

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supply methane to microorganisms, which can be directly utilized by the biofilms on the HFMs before

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its dissolution in water.22-25 Thus, HFMs offered a safe and efficient method to enhance the mass

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transfer rate of methane. Unfortunately, these HFMs are electrically nonconductive and can not be

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used as the anode materials.

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Therefore, this work aimed to enhance the performance of methane-powered mediator-less

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MFCs by developing a gas diffusion cloth (GDC) electrode. The GDC electrode was fabricated

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facilely by wrapping a waterproof GORE-TEX cloth together with carbon cloth (CC) on a tube. Such

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a structure created an ingenious consideration to both the methane bioavailability and microbial EET

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because methane can diffuse directly from the inner chamber of GDC electrodes to its outer surface.

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Electricity generation from MFCs equipped with the dual-function GDC anodes or conventional CC

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anodes were evaluated, and the EET mechanism was interpreted.

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2. Materials and methods

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2.1 MFC configuration and operation

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Dual-chamber glass MFCs were constructed identically with reactors described previously.26 To

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fabricate the GDC anode, a piece of GORE-TEX cloth (3.0 cm × 5.0 cm) with a waterproof layer of

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polytetrafluoroethylene (PTFE) was pasted to carbon cloth (3 cm × 4.5 cm) using nafion solution

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(10% wt). The cloth assembly was then wrapped to a cylindrical plastic tube (5.0 cm in height and 2.0

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cm in diameter) with the PTFE layer (40 µm in thickness), GORE-TEX cloth and carbon cloth

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positioned sequentially from the inside to the outside (Figure 1a). Carbon cloth served as a current

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collector and GORE-TEX cloth was used to distribute methane via the micropores of the PTFE layer.

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Both ends of the cylinder were sealed with rubber stoppers. A saturated calomel electrode (SCE) and

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graphite plate (2.0 cm × 3.0 cm × 1.5 mm) served as the cathode and reference electrode, respectively.

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The control MFCs were constructed using carbon cloth (3 cm× 4.5 cm) as the anode, which was

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wrapped similarly to a cylindrical tube. The anodic chamber was fed with a 110-mL inorganic

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medium that contained (per L): NH4Cl, 0.10 g; KHCO3, 0.50 g; NaH2PO4·2H2O, 5.92 g; Na2HPO4,

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8.80 g; MgSO4·7H2O, 0.20 g; CaCl2·2H2O, 0.10 g (pH = 7.0); acidic mineral element solution27, 1 mL;

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and alkaline mineral element solution27, 1 mL. The cathodic chamber was filled with a 110-mL

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potassium phosphate buffer (PBS, 100 mM, pH 7.0 with KCl or ferricyanide) (Table S1). All solutions

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were purged with N2/CO2 (80%/20%) for 1 h to remove oxygen.

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Anaerobic activated sludge was obtained from the Fuzhou municipal wastewater treatment plant,

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China. The reactors were initially inoculated with 5 mL of the sludge filtrate (filtered through a piece

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of gauze) and started up after a 6-day lag. 50 mL of methane in a syringe was supplied to the inside of

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cylindrical GDC anodes and CC anodes, respectively. The methane pressure in the syringe was

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maintained at approximately 25 kPa as detailed in the Supporting Information. The entire experiment

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included four stages (Table S1). For stage I (start-up) and stage III, the GDC electrode was poised at

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+0.3 V vs. SHE using a multi-potentiostat (CHI1040, Chenhua Co., Ltd., Shanghai, China). The

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anode was connected electrically to the cathode via an external resistor of 1000 Ω during stage II and

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IV. There was no addition of the sludge filtrate during stage II to IV. All tests were run in a fed-batch

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mode at 37±1°C. To enrich methanotrophs, 90% of the anodic biomass suspension in stage I was

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periodically replaced with fresh deoxygenated medium unless otherwise stated. Such a process was

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repeated for six times to shift gradually the electron donors in the sludge filtrate (e.g. dissolved

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organics) to methane. The residual methane in the syringe was supplemented to 50 mL after each

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medium replacement.

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2.2 Electrochemical measurements

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To evaluate the electrocatalytic activities of anodic biofilms, the intact GDC and CC reactors

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were scanned by cyclic voltammetry (CV) and electrochemical impedance spectroscopy (EIS) on day

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198. The CV scan range was from -0.8 to +0.6 V vs. SHE at a scan rate of 5 mV s-1. EIS of the

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bioanodes were analyzed at a constant potential of +0.3 V vs. SHE over a frequency range of 1 × 105

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to 0.01 Hz with a sinusoidal perturbation amplitude of 5 mV. The power density was measured by

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varying the external resistance from 50 to 20000 Ω when voltage outputs achieved a stable state in

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stage IV. The power was normalized to the projected surface area of the anode.

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2.3 Isotope tracer experiments

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To verify the methane oxidation, the anolyte was changed with fresh medium and purged with N2

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gas (99.99%) for 1 h to remove 12CH4. 50 mL of 13CH4 was supplied to the GDC electrode in the same

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way as mentioned above.

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carbon in the medium were analyzed using a gas chromatography-mass spectrometry (GC-MS)

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(7890-5975c, Agilent, USA). The detailed GC-MS protocol was provided in the Supporting

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Information. To identify the production of

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extracted twice with 10 mL of acetic ether. The resulted acetic ether extract was concentrated to 1 mL

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on a rotatory evaporator and determined using liquid chromatography together with mass

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spectrometry (LC-MS, Thermo LTQ XL, USA). The specific conditions for LC-MS were described in

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the Supporting Information.

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2.4 Analytical techniques

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CO2 in the headspace of anodic chambers and

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C-labelled inorganic

CH3COOH, 10 mL of the anolyte was sampled and

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The micropore diameter of GORE-TEX cloth was measured with a PMI capillary flow

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porometer (CFP-1500AE, USA). The gas permeability of GDC electrodes was evaluated using a

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micro gas flowmeter (RTK-SGMC, China). Scanning electron microscopy (SEM) and fluorescence in

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situ hybridization (FISH) were conducted with published methods (see details in the Supporting

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Information).28,29 The probe MB1174 was labeled with CY3 (red fluorescence) to target the 16S rRNA

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of Methanobacteriaceae family. The probe mixtures (equimolar amounts of Geo3a, Geo3b and Geo

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3c) were labeled with 6-FAM (green fluorescence) to target the 16S rRNA of Geobacter genus. The

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sequences of these oligonucleotide probes were identical with those documented in the literature.29

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The quantification of dissolved methane and methane in the headspace, Illumina high throughout

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sequencing and calculation of coulombic efficiency (CE) of methane to electricity were provided in

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the Supporting Information.

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3. Results and discussion

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3.1 Electrochemical features of GDC bioanodes

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GORE-TEX cloth was chosen as an assembly material because of its excellent waterproof ability

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and gas permeability. The morphological features of GORE-TEX cloth showed that small PTFE

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particles were evenly distributed on the waterproof side of the cloth (Figure S1). The micropore size

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of GORE-TEX cloth ranged from 0.05 to 1.35 µm and centered at approximately 0.45 µm (Figure

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S2a). Such a structure was analogous to hollow fiber membrane, guaranteeing a gradual release of

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methane from the inside of the GDC electrode to the biofilms. To evaluate the gas permeability of the

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GDC electrode, dissolved methane in the sealed reactors was determined at a constant methane

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pressure of 25 kPa without microorganisms. The concentration of dissolved methane reached

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saturation within 20 min and fluctuated around 1.0 mM (Figure S3).18 By contrast, methane provided

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in the headspace of the control MFCs with CC anodes permeated slowly into the mediums and

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reached only 0.04 mM after 20 min. When methane was allowed to flow out of the anodic chamber

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toward a flowmeter, the flow rate of methane through the GDC electrode was 0.47 mL min-1 at a

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pressure of 25 kPa (Figure S2b). This demonstrated the GDC electrode harbored a high methane

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permeability.

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With an anodic potential set at +0.3 V vs. SHE, pronounced biocurrents were observed in the

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143-d enrichment phase (stage I) (Figure S4). The electron donors in the initial 30 days were likely

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dissolved organic matter in the sludge filtrate (DOC-SF) and methane to a less extent. Electron donors

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shifted gradually from DOC-SF to methane and there was no residual DOC-SF after five batch cycles.

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A maximum biocurrent of 724.9 mA m-2 was produced during day 96 to 143 when methane was the

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sole electron donor. By contrast, negligible currents were produced in the absence of methane for the

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well-running reactor (Figure S5a), which was probably resulted from the degradation of intracellular

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organics (e.g. polyhydroxyalkanoates (PHA))30 or microbial extracellular polymeric substances

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(EPS)31. These results indicated that no other electron donors except methane could account for the

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electricity generation. To further verify this statement, the reactor was supplied alternately with

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methane and N2 (25 kPa, each for 30 min). The current increased noticeably once methane was

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supplied, whereas it decreased significantly when methane was gradually diluted by N2 (Figure 1b).

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Such current responses were absent in an abiotic reactor (Figure S5b). Therefore, the strong methane

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dependence of the bio-currents suggested that AOM was a main mechanism of electricity

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generation.32 To validate methane oxidation,

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headspace CO2 increased from 1.75±0.06% to 4.21±0.70% (Figure S6), which confirmed the 13CH4

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oxidation. The well-acclimated microbes were inoculated into the reactors equipped with new GDC

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anodes to evaluate the long-term electrogenic performance. Comparable maximum currents (1130.2 ±

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67.7 mA m-2) were achieved in five successive cycles of experiments (stage III, 130 days), indicating

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CH4 was shifted to

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CH4 on day 123 of stage I and

CO2 was analyzed by GC-MS. After an 18-d operation, the proportion of

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13

CO2 in the total


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the long-term operation stability of GDC anodes (Figure 1c). The current decrease in each cycle was

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likely caused by the depletion of nutrients in the anodic medium because there was 18.4 ± 4.7% of

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methane residual in the gas-tight system (Table S2). This resulted in an average methane utilization

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efficiency of 81.6 ± 5.3% and a CE of 70.4 ± 7.9% for these cycles. In comparison, the maximum

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current density for the CC anode was only 6.8 mA m-2 (Figure S7), which was close to those values

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reported by Gao et al.29 Therefore, the electrogenic activity of GDC anodes was enhanced by two

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orders of magnitude compared with CC anodes, suggesting the advantage of the GDC anodes.

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CVs were conducted to confirm the anodic electrochemical activities when the electrogenic

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currents fell to the background. As shown in Figure 1d, the GDC anode showed a higher catalytic

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current (740.2 mA m-2) than the CC anode (261.2 mA m-2), which was consistent with their

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electrogenic activities. Meanwhile, a pair of redox peaks (inflexion points at -0.39 and +0.23 V vs.

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SHE, respectively) appeared in the CVs of both GDC and CC anodes. However, no redox peaks were

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detected for the spent medium when the GDC bioanode was replaced by a bare GDC electrode. This

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indicated that the redox components were present on the anode surface rather than in the culture

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medium. The mid-point potential (E1/2, -0.08 V vs. SHE) of the peaks was close to the redox potential

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of menaquinone (E0′, -0.07 V vs. SHE),33 which was generally present in the plasma membrane of

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microbes. Additionally, a reduction peak at -0.08 V vs. SHE was observed for the GDC anode,

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whereas it was absent for the CC anode. To further understand the electrogenic process, EIS was used

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to evaluate the anodic charge transfer resistances (Rct), which was crucial to the overall anodic

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performance. Figure 1e shows a typical Nyquist impedance spectrum of the anodes. As indicated by

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the diameter of the first semicircle in the spectra, the GDC anode had a lower Rct than the CC anode,

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which would benefit the electrogenesis of the former. The lower Rct for the GDC anode was likely

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attributable to an increased interaction between the biofilms and anodes. Therefore, both the CV and

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EIS results implied an improved electrochemical activity of GDC anodes.

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3.2 Enhanced MFC performance by GDC anodes

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The performance of MFCs with GDC anodes is presented in Figure 2a and 2b. At a fixed

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resistance of 1000 Ω, the voltage outputs for MFCs with GDC anodes (stage II) increased

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significantly to a maximum value of 0.55/0.52 V. The voltages were still higher than 0.40 V after 100

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h and the slow voltage decreases were mainly due to the consumption of ferricyanide and anodic

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medium as well as methane. Successful startup was also observed in a new GDC anode MFC (stage

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IV) after an operation time of 6 days (Figure 2b). The new MFC obtained a maximum cell voltage

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output of 0.41 V in the first cycle. Such performance was well reproduced in subsequent four cycles

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after replacing the anodic and cathodic electrolytes with the fresh medium and ferricyanide,

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respectively. This indicated an excellent stability of the GDC anode during the 30-d operation. The

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average residual methane in the gas-tight MFCs was 85.2 ± 3.0% for these cycles, resulting in a

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methane utilization efficiency of 14.8 ± 3.3% and a CE of 61.3 ± 16.7%. The voltage decrease in each

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cycle and the low methane utilization efficiency were caused by the depletion of ferricyanide (20

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mM), which faded into colorless solutions. The stoichiometric ratio of ferricyanide to methane was

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7.4 ± 1.6 (Table S3), which is in agreement with the theoretical value of 8. This indicated that most of

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the AOM electrons were removed from cells for cathodic ferricyanide reduction. By contrast, the

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values (ca. 0.02 V) were negligible during the 10-day operation although MFCs with CC anodes

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(stage IV) also produced small peak voltages (Figure 2c). These results demonstrated that the

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performance of MFCs with GDC anodes was superior to that of CC anodes. This superiority may be

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attributed to two main reasons: i) the GDC electrode accelerated the dissolution and distribution of

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methane in the medium (Figure S3); and ii) the GDC electrode could promote in situ utilization of

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gaseous methane by the biofilms. Such novel functions of the GDC electrode made it more efficient to

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couple AOM with electrogenesis, and thus enhancing the MFC performance.

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Figure 2d shows the power density versus current density curve as well as the polarization curve.

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The maximum power density obtained from MFCs with GDC anodes was 419.5 ± 15.9 mW m-2

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(normalized to the anode surface area) (Table 1), which was 2.5 times of these reported by McAnulty

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et al.15 In comparison with conventional electrodes used in previous studies, the GDC electrode

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accelerated the dissolution of methane and promoted in situ methane utilization by the biofilms. These

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novel functions may explain its excellent performance. The polarization behaviors of GDC anode and

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cathode were determined to assess the limiting reaction of power (Figure 2d). The decrease of external

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resistances significantly increased the GDC anode polarization potential from -458 to -138 mV.

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However, the cathodic polarization potential decreased slowly from +186 to +14 mV in this process.

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As suggested previously, the limiting electrode reaction could lead to a steep slope versus current in

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the polarization curve.34 Therefore, the steeper slope observed in the GDC anode polarization revealed

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that the electrogenic performance was mainly limited by anodic reactions rather than cathodic

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reactions. Linear regression analysis of the polarization curve for the entire cell gave a slope of -0.22

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Ω•m2 (i.e. -163.0 Ω) in the ohmic loss region. The absolute value of the slope reflected the internal

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resistance (Rin) of MFCs, which was consisted of the activation resistance, ohmic resistance and

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concentration resistance.35 Thus, the power output of the GDC anode-based MFC could be optimized

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at an external resistance of 163.0 Ω.

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3.3 Proposed electrogenic mechanisms

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The morphology and distribution of biofilms on the GDC anodes (Figure 3a) and CC anodes

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(Figure 3b) were visualized by SEM images. More short and rod-shaped microorganisms colonized

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on GDC anodes than those on CC anodes, providing the possibility of direct electron transfer to

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electrodes. FISH images demonstrated the presence of both Methanobacterium (red fluorescence)

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and Geobacter (green fluorescence) on the GDC anodes (Figure 3c) and CC anodes (Figure 3d). This

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observation was consistent with that reported by Gao et al., who suggested Methanobacterium might

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grow synergistically with Geobacter in the bioelectrochemical system.29 For the GDC anode,

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Geobacter seemed to be the dominant species of the biofilms compared with Methanobacterium.

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Besides, the density of Geobacter on GDC anodes was much higher than those on CC anodes. This

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may account for the enhanced electrogenic performance of GDC anodes.

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The contribution of the GDC biofilms and planktonic microorganisms to the electrogenesis was

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compared by removing or recycling planktonic cells during medium replacement (Figure S8). When

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all planktonic cells were removed from the anodic medium, the maximum current density in the

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second cycle was only 24.5% of that for the first cycle (Figure S8a). By contrast, the maximum

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current density recovered to that of the first cycle when the planktonic cells were harvested and

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recycled in the fresh anodic medium (Figure S8b). This phenomenon indicated that the planktonic

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cells and the biofilms accounted for 75.5% and 24.5% of electricity generation, respectively. It is

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therefore suggested that methanotrophs in both planktonic cells and GDC biofilms played an

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important role in the electrogenesis. CV experiments showed that the redox activities of the GDC

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anodic system were mostly derived from the Geobacter-dominating biofilms (Table S4). Based on

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the CV and FISH results as well as the observations above, it was speculated that the electrogenesis

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had proceeded in two steps via the cooperation of planktonic cells and biofilms as well as the

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cooperation of microbes on the biofilms. The first step was the intermediates-mediated electron

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transfer from methanotrophs to Geobacter (see later discussion), and the second step involved the

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direct electron transfer from Geobacter to anodes due to its contact with electrode surfaces.

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Microbial community structures of the initial inoculum, the GDC anode biofilms, and the

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planktonic microorganisms were analyzed to reveal the electrogenic mechanisms. The most

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abundant microorganisms in the inoculum were Lactobacillus (5.34%), Christensenellaceae R-7

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(1.81%) and Gelria (1.29%) (Table S5). In comparison, the GDC anode biofilm was dominated by

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Geobacter (47.35%), Actinotalea (6.57%), Pseudobacteroides (4.28%), Desulfovibrio (1.59%).

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Meanwhile, Methanobacterium (4.60%) and Methanobrevibacter (0.59%) were detected on the

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GDC anode. Three other archaeal genera Methanocella, Methanolobus and Methanomassiliicoccus

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were also detected on the GDC anode, yet their abundances were less than 0.05%. Contrary to the

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biofilms, the relative abundance of Methanobacterium in the medium increased remarkably to

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37.41%, whereas Geobacter decreased to 6.25%. Other planktonic microorganisms included

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Pseudobacteroides (18.98%), Desulfovibrio (4.03%), Actinotalea (2.69%), Ignavibacterium (2.10%)

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and Methanobrevibacter (0.06%), etc.

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Methanobacterium bryantii (3.82%) was the dominant archaeon in the biofilm, followed by M.

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formicicum (0.75%) and Methanobrevibacter arboriphilus (0.59%) (Table S6). Geobacter species in

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the biofilm included G. soli (44.89%), G. metallireducens GS-15 (1.83%), and two unclassified

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Geobacter strains (0.63%). M. bryantii was a nonmotile and strict hydrogenotrophic methanogen.36,37

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Its representative strain M. bryantii M.o.H. and five other Methanobacterium strains were previously

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shown to work as methanotrophs for AOM.38,39 Since the ANME clades (ANME-1, ANME-2 and

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ANME-3) were not detected in our reactors, we ruled out the possibility of AOM by ANME.

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Therefore, M. bryantii could have played a predominant role in coupling AOM with electrogenesis.

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Previous studies showed that Methanobacterium could take in electrons from solid electrodes for

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eletromethanogenesis.40,41 This indicates that Methanobacterium is electroactive and capable of EET.

321

Moreover, the methanogen Methanosarcina was suggested to catalyze reversed methanogenesis by

322

transferring electrons to extracellular Fe(III) via EET.42 Therefore, it is likely that Methanobacterium

323

reversed the electromethanogenesis process and donated electrons to GDC anodes (Figure 1a).

324

Nevertheless, Methanobacterium does not contain c-type cytochromes and it EET ability may be

325

weak.29,43,44 G. soli is a dissimilatory Fe(III)-reducing and electroactive bacterium and can utilize

326

various substrates including glucose, phenol, propionate and acetate,45 with an electrogenic ability

327

slightly higher than that of the model exoelectrogen G. sulfurreducens.46 However, Geobacter seems

328

not to metabolize methane directly, and thus it could not oxidize methane for electrogenesis alone.

329

Methanobacterium occupied 99.84% and 87.09% of total archaea in the medium and biofilm,

330

respectively. Meanwhile, Geobacter accounted for 9.99% of planktonic bacteria and 49.99% of the

331

biofilm bacteria (Figure 4). The high abundances of both Methanobacterium and Geobacter strongly

332

suggested a methanotroph-exoelectrogen interaction. Previous studies have shown that direct

333

interspecies electron transfer (DIET) can occur between ANME-1 and sulfate-reducing bacteria, or

334

between Geobacter and methanogens.47-49 Outer membrane c-type cytochromes were suggested to

335

play an important role in the DIET process. However, Methanobacterium seemed not to be capable of

336

DIET due to the lack of c-type cytochromes.29,43 As a result, the methanotroph-exoelectrogen

337

cooperation was speculated to be an intermediate-mediated process rather than DIET. In other words,

338

the methanotrophs transferred electrons from methane to CO2 and secreted the intermediates,38 which

339

were then utilized by exoelectrogens for electrogenesis. To support this hypothesis, the AOM products

340

in the medium were tracked using 13CH4 and identified by LC-MS. 13CH3COO- (up to 0.11 mM) was

15



Page 16 of 29

341

observed as an intermediate (Figure S9), whereas no formate or H2 was detected. Such low

342

13

343

The presence of

344

methanotrophs to exoelectrogens. Previously, Zehnder et al. (1979) showed that pure methanogens (M.

345

bryantii M.o.H. etc.) oxidized methane into acid-soluble organics such as amino acids.38 Nevertheless,

346

M. bryantii was a strict H2-oxidizing archaeon that did not produce acetate.36,37 Thus,

347

might have evolved from bacterial decomposition of acid-soluble organics excreted by methanotrophs

348

(e.g. M. bryantii) and was used for electrogenesis. Alternatively, the acid-soluble organics was utilized

349

directly by exoelectrogens for electrogenesis. Despite of trace AOM generated by pure methanogen

350

cultures,38,39 methane consumption by mixed cultures could reach 19% or 90% of methane produced

351

in methanogenic sludges.50,51 These results matched well with the appreciable electricity generation

352

from methane in our MFCs. Carbon balance analysis of the 13CH4 products showed that the headspace

353

13

354

0.2% of the consumed 13CH4, respectively (Table S9). Therefore, 23.8% of the consumed 13CH4 could

355

have been assimilated by microorganisms for biomass synthesis.

356

3.4 Implications

CH3COO- concentrations were probably resulted from the ongoing consumption by exoelectrogens. 13

CH3COO- demonstrated the occurrence of mediated electron transfer from

13

CH3COO-

CO2, 13C-labelled inorganic carbon in the medium and 13CH3COO- accounted for 68.6%, 7.4% and

357

This study has demonstrated for the first time that the dual-function GDC electrode can be used

358

as a high-performance anode for microbial electricity generation from AOM. Besides, the

359

electrogenesis mechanism is speculated to be the reversed methanogenesis with electrons deposited

360

on the anodes by methanotrophs in combination with electron production by exoelectrogens (e.g.

361

Geobacter, Desulfovibrio52) that degrade the AOM intermediates. This is analogous to the bacterial

362

syntrophic electrogenic behaviors observed previously among pure co-cultures.8,53 Therefore, the

16


Page 17 of 29


363

syntrophic interaction between certain archaea and bacteria can be designed as an alternative

364

electrogenic strategy in future MFCs. Such synergistic biocatalysts will expand the biodegradable

365

substrate types of MFCs. The supply of methane to MFCs via GDC electrodes is very similar to

366

membrane biofilm reactors (MBRs). In principle, GDC electrodes may also be suitable to supply

367

other gas fuels such as hydrogen to MFCs. Therefore, GDC electrodes will have promising

368

application potentials to integrate membrane biofilm reactors with MFCs. This integration

369

undoubtedly promotes the technological development of powering MFCs with gases.

370

Notes

371

The authors declare no competing financial interest.

372

Acknowledgments

373

This study was supported by the Natural Science Foundation of China (No. 41701270, 91751109 and

374

41671264).

375

Supporting Information Available

376

SEM images of GORE-TEX cloth, dissolved methane concentrations, the electrogenic performance in

377

stage I, effects of planktonic microorganisms on electrogenesis, GCMS and LCMS data, and

378

microbial community of the sludge filtrate. This material is available free of charge via the Internet at

379

http://pubs.acs.org.

380 381

References

382

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510

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511

Microbiol. 2017, 83 (6), e03033–16.

512 513

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514

Figure captions

515

Figure 1 Schematic of the preparation of GDC electrode and proposed electricity generation model (a).

516

Current responses of the GDC electrode to alternate purge of CH4 and N2 gases (each for 30 mins) at

517

the end of stage I (b). Electricity generation by the GDC electrode at a poised anode potential of +0.3

518

V vs. SHE and 37±1°C in stage III (c); black arrows indicate the time of medium replacement and

519

methane addition; all planktonic biomasses of stage III were recycled by centrifugation and reused in

520

each cycle during medium replacement. Characterizations of the GDC bioanode and CC bioanode by

521

cyclic voltammogram (d) and electrochemical impedance spectroscopy on day 198 of stage III (e).

522

Inset of Figure 1e shows an enlarged image in the range of 0–14 Ω.

523

Figure 2 Voltage differences across a fixed 1000 Ω resistance for the GDC anode MFCs in stage II (a),

524

GDC anode (b) and CC-anode (c) MFCs in stage IV at 37±1°C. The different colored lines represent

525

the results from two or three replicates. The power density and polarization curves obtained from the

526

GDC anode MFCs (b); the bars indicate the standard deviation of three replicates (n=3).

527

Figure 3 Scanning electron microscopy and fluorescence in situ hybridization images showing the

528

biofilms on GDC anodes (a, c) and CC anodes (b, d). Red fluorescence indicates the

529

Methanobacteriaceae family and green fluorescence indicates the Geobacter genus. The biofilm

530

samples were collected after a 40-d operation in the beginning of stage III.

531

Figure 4 Compositions of main bacteria and archaea in the medium and biofilm at the genus level.

532

Genomic DNA samples were extracted on day 296 of stage III. The abundance of each bacterium was

533

relative to the total amount of bacteria and the same case for archaea.

534 535 536 24


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537


Figure 1

538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558

25



559

Figure 2

560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580

26


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Page 27 of 29

581


Figure 3

582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602

27



603

Figure 4

604 605 606 607 608 609 610 611 612 613 614 615 28


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616

Table 1 Comparison of the electrogenic performance for different bioelectrochemical reactors.

617

Anode material

Carbon fiber felt Carbon fiber brush Carbon cloth Carbon fiber Carbon fiber brush GDC cloth

Cathode surface area (cm2) 26.8 22.7 22.7, 0.5 60 13.5

Maximum cell voltagea (V) 0.028 0.60 0.75 ± 0.06 0.61 0.62±0.03

Maximum current density (mA m-2) 10.4 273 ± 7 6000 ± 1000 13.6 101.7 1130.2± 67.7b

Maximum power density (mW m-2) 0.65 168 ± 9 4700 ± 800 62.0 419.5 ± 5.9b

618

a

Maximum voltage outputs across an external resistance of 1000 Ω.

619

b

Expressed as mean ± SD that were obtained from five cycles of experiments.

620

29


CE (%)

Reference

90 ± 10 82.3 0.9-17.7 65.9±13.2b

17 15 16 29 18 This study

Novel gas diffusion cloth bioanodes for high-performance methane

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