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Startup performance and anodic biofilm distribution in continuous-flow microbial fuel cells with serpentine flow fields: Effects of external resistance Liang Zhang, Jun Li, Xun Zhu, Dingding Ye, Qian Fu, and Qiang Liao Ind. Eng. Chem. Res., Just Accepted Manuscript • DOI: 10.1021/acs.iecr.6b04619 • Publication Date (Web): 22 Mar 2017 Downloaded from http://pubs.acs.org on March 27, 2017

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Industrial & Engineering Chemistry Research

Startup performance and anodic biofilm distribution in continuous-flow microbial fuel cells with serpentine flow fields: Effects of external resistance a,b

a,b

a,b

a,b

Liang Zhang , Jun Li *, Xun Zhu , Dingding Ye , Qian Fua,b, Qiang Liao a

a,b

Key Laboratory of Low-grade Energy Utilization Technologies and Systems (Chongqing University), Ministry of Education, Chongqing 40003, China, b

Institute of Engineering Thermophysics, Chongqing University, Chongqing 400030, China

*Corresponding

author.

Tel.:

+86-23-6510-2474;

fax:

+86-23-6510-2474;

[email protected] (Jun Li).

1 ACS Paragon Plus Environment

E-mail

address:


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Abstract: To better understand the startup process, the evolution of voltage output, energy gain and output, active biomass and electrochemical performance of microbial fuel cells (MFCs) started up under different external resistances (10, 50, 250 and 1000 Ω) were investigated. In addition, the influences of external resistance and mass transfer on the anodic biofilm distribution of MFCs were also investigated. The results showed that MFCs with a decreased external resistance during startup had an increased evolution rate of energy gain, energy output, active biomass and maximum power density but a reduced voltage evolution rate. A low external resistance for startup resulted in a thick and compact biofilm. As the flow field induced mass transfer, the biofilm was mainly distributed on the carbon cloth against the flow channel, and the biomass decreased along the flow direction. The compact biofilm on the surface resulted in a poor mass transfer and limited biofilm development inside the electrode.

Keywords: microbial fuel cell; startup; biofilm; external resistance; mass transfer


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1 Introduction Microbial fuel cells (MFCs) are a new type of renewable and sustainable technology for electricity generation. In a typical MFC, microorganisms are used to catalyze the oxidation of organic and inorganic matter, and electrons extracted by the bacteria from the substrates are transferred to the anode electrode and then flow through a circuit to the cathode.1 In the past decade, MFC research has been a rapidly evolving field, and a mass of work has been contributed to the development of MFC reactors, materials of construction, biofilms and key influencing factors.2-7 However, the startup performance and mass transfer are also two important considerations for MFC technology. It has been reported that bioreactor performance is highly influenced by the start-up process.8-9 With respect to MFCs, good startup performance would be necessary for electricity generation and wastewater treatment.10 On the one hand, a rapid startup of any bio-process for wastewater treatment is desirable so that the system can work efficiently as soon as possible.11 The startup time of MFCs varies depending on several key factors such as operational temperature,12 MFC reactor type,11,13-14 the type of wastewater and additional amendments,11 electrodes and separators,6,15-16 microorganism diversity14 and the anode potentials.17-19 Additionally, external resistance, as an easy and traditional strategy to run MFCs,20 would also significantly influence the startup time. On the other hand, the evolution of MFC process parameters during the startup period is also important. Faster evolution of MFC performance with a higher maximal power was found in a liter-scale MFC with a 3 ACS Paragon Plus Environment


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staggered electrode array compared to an MFC with an inline electrode array.15 An MFC applied at a positive anode potential had a faster and better MFC performance and more biomass of the anode biofilm during the evolution process.19 However, the influence of external resistance on the evolution of MFC process parameters, including energy gain, active biomass and maximal power, needs to be investigated to better understand the startup process. Mass transfer, as another important consideration for MFC, can significantly affect power generation especially, at a high working current.21-25 It has been reported that substrate transfer limitation would lead to voltage reversal in a microbial fuel cell stack operated in a batch mode for a long period, suggesting a continuous-flow operation may be desirable.26 Meanwhile, the continuous and stable current output by operating an MFC in continuous mode is one of the most important requirements of power sources for electronic devices in future application. Serpentine flow fields were widely used in fuel cells to enhance mass transfer and thereby obtain continuous energy output.27 A flat plate MFC using serpentine flow fields in the anode and cathode was constructed to produce continuous electricity generation28, demonstrating an attractive potential application as power sources for electronic devices. However, the transfer of substrate and product not only influenced electricity generation22-25 but also affected biofilm formation29. It is expected that the anodic biofilm distribution would be influenced by the uneven mass transfer resulting from the flow field effects. In addition, the utilization efficiency of the porous anode material such as carbon cloth for anodic biofilm development remains unclear. 4 ACS Paragon Plus Environment

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In this study, four flat plate microbial fuel cells with serpentine flow fields were started up under different external resistances of 10, 50, 250 and 1000 Ω, respectively. The objective of the present study was to investigate the effects of external resistance on the startup process. Meanwhile, the influences of external resistance and mass transfer on the anodic biofilm distribution of MFCs were also discussed. 2 Materials and methods 2.1 MFC configuration Figure S1 showed a schematic of the serpentine flow field (a) and the MFC system (b). The serpentine flow field was composed of 9 flow channels and 8 ribs all with the same height of 2 mm and same width of 2 mm, as shown in Figure S1(a). With the flow direction, four flow channels in the front and the back part were defined as the upstream and downstream part of the flow rate, respectively. The experiments were conducted using four two-chamber MFCs with serpentine flow fields in the anode and cathode. Each MFC consisted of a proton exchange membrane (PEM) (Nafion 117, DuPont), two carbon cloth electrodes (E-TEK, B-1A, USA) and two plexiglass plates with a flow channel holding a volume of 2.7 mL. The PEM, with a surface area of 25 cm2, had a slightly larger surface area than electrodes. Two Ag/AgCl reference electrodes were placed in the 50 mL glass bottles connected to the outlet of the anode and cathode flow field plate. 2.2 MFC operation The anode compartments of the four MFCs were individually inoculated with the effluent from a continuous-flow running MFC fed with an artificial wastewater (500 5 ACS Paragon Plus Environment


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mg COD L-1; solution conductivity=15.12 mS cm-1) containing 0.64 g L-1 sodium acetate, 4.58 g L-1 Na2HPO4, 2.45 g L-1 NaH2PO4·H2O, 0.31 g L-1 NH4Cl, 0.13 g L-1 KCl, trace minerals and vitamins30. During startup, all the anode flow rates were 1 mL min-1 and the anode chambers were directly fed with fresh wastewater at the same flow rate on day 7. The external resistances for the four MFCs during startup were 10, 50, 250, and 1000 Ω (denoted as MFC-10, MFC-50, MFC-250 and MFC-1000, respectively). The cathodes were continuously supplied with 50 mM fresh potassium ferricyanide solution at a rate of 1 mL min-1 during the start-up stage and steady-state operation. All MFC tests were conducted in a temperature-controlled room at 25 °C. 2.3 Measurements and calculations The cell voltages (U) and anode and cathode potentials of each MFC were collected every 15 s via an Agilent 34970A data acquisition unit connected to a PC (Figure S1(b)). For measurement, the external resistance was varied in a range of 5-1.0×105 Ω to control the discharging condition and record the voltage-current curves. For each external resistance step, the voltage was measured at a steady state with a voltage drift of less than 5 mV h-1. The current and power density of the MFC were calculated according to Eq. (1) and (2), respectively: I=U/R

(1)

P=U×I/A

(2)

where R and A are the external resistance and the surface area of the electrode, respectively. The metabolic energy gain (MEG) for the electrochemically active bacteria and 6 ACS Paragon Plus Environment

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energy output (EO) as heat dissipation on the external resistance (R) were calculated with the following Eq. (3) described by Wei et al.18 and Eq. (4) based on Ohm’s Law, respectively. t

MEG = ∫ (E andoe(t ) − E 0`)I(t )dt

(3)

0

EO =

t

∫ RI(t )I(t )dt 0

(4)

where E anode (t ) and I (t ) are the anode potential and current at time t during start-up period, respectively. E 0` is the standard potential of CO2/acetate (-0.29 V). The unavailable part of the energy gain for the electrochemically active bacteria was neglected because this portion makes up less than 20% of the energy gain when the MFC was started up by applying an external resistance to the electrical circuit Wei et al.19 The morphology of the biofilm formed in each segment of the anode electrode was analyzed by a scanning electron microscopy (SEM, 3400N, HITACHI Instrument Inc). To prepare the SEM samples, the graphite rods at the center of each anode segment were carefully removed from the anode compartment at the end of the experiment and then immediately fixed in phosphate buffered saline (PBS) with 2.5% glutaraldehyde (pH 7.2-7.4) for 1 h. After washing three times with the same buffer, the samples were dehydrated stepwise with a graded series of ethanol solutions (30, 50, 70, 80, 90 and 100%) and then critical-point dried with a tert-butyl ethanol solutions. After that, the samples were sputter coated with a thin gold layer and observed in a high vacuum using SEM in the secondary electron imaging mode. To measure the active biomass, the upstream and downstream pieces of anode 7 ACS Paragon Plus Environment


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electrode with biofilms were taken from the MFCs and analyzed according to methods described previously.31 The phosphate concentration released from phospholipids was determined using a Leng Guang 756mc spectrophotometer at 610 nm. The phosphate concentration was then correlated to total active biomass using the conversion factor of 191.7 µg of biomass-C per 100 mmol of phospholipid.31 3 Results and discussion 3.1 Effect of external resistance on MFC start-up process 3.1.1 Evolution of MFC voltage

Figure 1. Voltage evolution of MFCs started up at different external resistances

The evolution of MFC voltages was shown in Figure 1. It was found that external resistances had a significant effect on the startup of MFCs. With increasing external resistance from 10 to 1000 Ω, the lag period of MFCs decreased from approximately 3.0 to 0.6 days. After a lag period, rapid increases were observed in the cell voltages of all MFCs operated at different external resistances. MFC-1000 reached a voltage peak of 0.74 V on day 2.5. The voltage peaks for MFC-250, MFC-50 and MFC-10 were observed on day 3.2, 4.0 and 5.0, respectively. No obvious change was observed 8 ACS Paragon Plus Environment

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in cell voltages and electrode potentials of the four MFCs after being directly fed with fresh medium on day-7. The stable currents of the MFCs (with 1000 to 10 Ω external resistance) were approximately 0.74, 2.64, 10.8 and 15.0 mA, respectively. The above results indicated that MFCs with higher external resistance would have a faster startup process. Moreover, it was much harder to successfully startup an MFC using a very low external resistance (10 Ω), which is probably due to unstable anodic potential during startup (data not shown). Thus, for MFC startup, it is feasible to operate at a high external resistance and then gradually switch to lower external resistances to produce high current.32 3.1.2 Evolution of energy gain for bacterial and energy output

Figure 2. Evolution of energy gain for microorganism growth (a) and energy output (b) during startup process

It has been reported that the energy gain for microorganism is essential for the maintenance of bacterial vitality.33 During the startup process, energy gain directly influences microorganism growth. From the respective of energy, the evolution of energy gain and energy output was shown in Figure 2 (a) and (b), respectively. It can be clearly seen that the increasing rate of energy gain for bacteria growth sharply 9 ACS Paragon Plus Environment


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decreased with increasing external resistance during MFC startup. This indicated that MFCs operated at a lower external resistance would have higher energy gain per unit time for microorganism growth during startup process. It was also found that different evolution rates of heat dissipation of external resistance were observed as energy output from MFCs started up under different external resistances. The heat dissipation between MFCs had relatively small differences on day 2 and the differences obviously increased with time. After day 5, the rapidest increase rate on the energy output was observed in MFC-50 followed by MFC-10, MFC-250 and then MFC-1000. This indicated that, the energy output increased when the external resistance decreased from 1000 to 250 and then 50 Ω during startup process. However, after a further decease in the external resistance, a decrease in the energy output was observed. 3.1.3 Evolution of active biomass

Figure 3. Evolution of active biomass in the upstream (a) and downstream (b) area of MFC biofilms during the startup process

Considering the direct relationship with current generation, the average active biomass in the upstream and downstream area of MFC biofilms that developed at 10 ACS Paragon Plus Environment

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different external resistances was measured on day 2, 5 and 15 as shown in Figure 3 (a) and (b), respectively. Minor differences were observed in the small active biomass of four MFC biofilms developed at different external resistances on day 2. It should be noted that the active biomass of MFCs increased at different rates after day 5 even through the MFCs had stable current generation and a stable increase rate in energy gain for bacteria growth. This indicated that it was unreasonable to judge the success of the startup process only based on whether it reached the stable current generation. A similar phenomenon was also observed in the previous MFCs started up under different poised anode potentials.31 The largest amount of active biomass in the upstream biofilm during the startup period was found in MFC-50 followed by MFC-10, MFC-250 and then MFC-1000. This order was inconsistent with the evolution rate of energy gain for bacteria growth. Compared with MFC-50, MFC-10 had a higher energy gain for bacteria but had lower biomass content. It is generally accepted that bacteria also produce extracellular polymeric substances (EPS) by consuming energy gain during the startup process to contribute up to 50-90% of the total organic carbon of the biofilms.34 Thus, a possible explanation was that MFC-10 had a higher proportion of energy gain for producing EPS instead of biomass than MFC-50. In addition, MFC-50 and MFC-10 had similar active biomass contents in the downstream biofilm. The above results showed that MFC startup at a low external resistance lead to a high evolution rate of active biomass. It was clearly seen that the active biomass in the upstream biofilm was higher than that in the downstream biofilm, possibly due to decreasing COD 11 ACS Paragon Plus Environment


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concentration and pH along the flow direction. The average biomass of MFCs at different startup periods as a function of energy gain for bacteria growth was shown in Figure S2. It was found that a linear correlation (R2>0.991) between biomass production and energy gain for microorganism growth was observed in MFCs started up under different external resistances. This trend is consistent with a previous study that used anode potential to regulate the energy for growth and output.19 The linear function for MFC-1000 had the steepest slope (0.3500), followed by MFC-250 (0.1550), MFC-50 (0.0318) and MFC-10 (0.0147). This indicated that MFCs started up under a high external resistance had a high biomass density production rate per unit energy gain for bacteria. 3.1.4 Evolution of MFC performance To investigate the evolution of MFC performance, polarization tests were conducted on day 3, 4, 5, 7, 9 and 15. Polarization curves were shown in Figure S3, and performance details were summarized and shown in Figure 4. It can be clearly seen that different anode potentials could be attributed to the differences in power density of MFCs started up under different external resistances, whereas minor differences in cathode potentials were observed (Figure S3). During startup, the evolution of MFC performance was recognized as the anode potential varied from positive to negative values (Figure S3), indicating increased levels of bacteria forming biofilm (Figure 3).


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Figure 4. Evolution of maximum power density (a), current density (b) and external resistance (c) at maximum power production

As shown in Figure 4a, the highest maximum power density (661.6 mW m-2) was observed at an optimal external resistance of 250 Ω in MFC-250 on day 3 followed by MFC-1000 (446.3 mW m-2 at 400 Ω), MFC-50 (275.5 mW m-2 at 400 Ω) and MFC-10 (226.1 mW m-2 at 400 Ω). Two days later, a maximum power density of 2591.0 mW m-2 was obtained at an optimal external reisitance of 50 Ω in MFC-50. The maximal power density and the optimal resistance were 1641.7 mW m-2 and 100 Ω for MFC-250, 1082.8 mW m-2 and 50 Ω for MFC-10, and 713.5 mW m-2 and 250 Ω 13 ACS Paragon Plus Environment


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for MFC-1000, respectively. MFC-10 and MFC-250 basically reached peaks of the maximum power density on day 5 while MFC-50 and MFC-1000 required two more days for reaching the power peaks (day 7). After day 7, no noticeable change in the maximum power was observed in the four MFCs. It could be concluded from Figure 4 that an MFC with a low external resistance would have a fast evolution rate of MFC performance although having a slow startup process. The highest maximal performance (approximately 2600.4 mW m-2) was found in MFC-50 followed by MFC-250 (approximately 1536.8 mW m-2), MFC-10 (approximately 1206.2 mW m-2) and MFC-1000 (approximately 961.6 mW m-2). The current density (approximately 4500 mA m-2) at the maximal power density of MFC-50 was also the highest in the four MFCs. This indicated that 50 Ω was the optimal external resistance for MFCs startup to obtain high performance. In addition, for each MFC, the optimal external resistance at maximal power density decreased with the startup resistance (Figure 4c). After day 5, MFC-50 and MFC-10 had the same and lowest optimal external resistance (50 Ω). The optimal external resistance was 100 Ω for MFC-250 and 150 Ω for MFC-1000.

3.2 Anodic biofilm distribution After a month of stable operation followed by successful startup, four anode electrodes were removed from the MFC reactors to investigate the anodic biofilms. Photos of MFC anodic biofilms developed at different external resistances were shown in Figure S4. It was observed that the anode electrodes against the flow 14 ACS Paragon Plus Environment

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channel showed different colors with that against the rib in each biofilm sample, which might be due to the flow field inducing mass transfer, thereby influencing biofilm development. In addition, biofilms developed under external resistances presented different colors as well. To explain this phenomenon, SEM micrographs of biofilms were used to analyze the mass transfer and external resistance effects on the anodic biofilm distribution. 3.2.1 Effect of mass transfer

Figure 5. SEM micrographs of MFC-10 bioﬁlm on the carbon cloth against flow channel ((a)×1000, (b)×8000), rib ((c)×1000, (d)×8000) and cross-sectional images (e, f)

As an important consideration for MFCs, substrate and product transfer can affect not only electricity generation at high current21-25 but also influence biofilm 15 ACS Paragon Plus Environment


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formation.29 In MFCs using a serpentine flow field, substrate and product are mainly transported along the flow channel, which might influence biofilm development. The color difference between the anode electrode against the flow channel and the one against the rib was probably related to the fact that the biofilm was mainly distributed on the carbon cloth against the flow channel, and only minor biofilm was observed on the carbon cloth against the rib due to lack of substrate in these areas. To confirm this point, the morphology of biofilm on the carbon cloth against flow channel and rib in MFC-10 was shown by using scanning electron microscopy (SEM). The results showed that the carbon fiber against flow channel was totally covered by thick biofilm whereas only a few bacteria were found on the surface of carbon fiber against the rib (Figure 5 (a)~(d)). This was because minor amounts of substrate were transported to the carbon cloth against the rib. Moreover, Figure 5(e) and (f) showed SEM cross-sectional images of the carbon cloth against the flow channel. It was observed that the thick and dense biofilms were mainly distributed on the surface of the carbon cloth. However, minor amounts of bacteria were observed inside the carbon fiber because the thick and compact biofilm on the surface of carbon cloth limited mass transfer from the outside to the inside. This resulted in a low utilization of carbon fiber for bacteria attachment in MFCs with thick anode material. Further study is necessary to understand the effects of the physical characteristics of porous anode materials such as porosity, thickness and conductivity. In addition, the active biomass content in the upstream biofilm was higher than that in the downstream biofilm due to the decreasing COD concentration and pH along the flow direction 16 ACS Paragon Plus Environment

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(Figure 3). This indicated that the upstream biofilm might be more compact than the downstream biofilm. The above results showed the significant effects of mass transfer on biofilm formation in MFCs and more attention needs to be paid to the mass transfer in MFCs. There is noted that, many previous studies reported the flow channel geometry effects on mass transfer and the performance of other chemical fuel cells using flow fields. Further research would be focused on this effects in MFCs using flow fields. 3.2.2 Effect of external resistance

Figure 6. SEM surface micrographs of anode biofilm developed at different external resistance (10 Ω, 50 Ω, 250 Ω and 1000 Ω) in MFCs with serpentine flow fields

In addition to mass transfer, external resistance would also influence biofilm development. The above results indicated that biofilm was mainly distributed on the anode electrode that was against the flow channel. To investigate the external resistance effects on biofilm development, the surface and cross-sectional SEM microphotographs of the biofilms on the anode electrode against the flow channel of 17 ACS Paragon Plus Environment


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the four MFCs were presented in Figure 6 and Figure S5, respectively. From the surface microphotograph at different magnifications (Figure 6), it was obvious that the anodic biofilms against the channel almost totally covered the electrode in MFC-10 and MFC-50, whereas the electrodes of MFC-250 and MFC-1000 were not totally covered by the biofilms. As shown in Figure 3, the active biomass density of MFC-10 and MFC-50 was several times higher than that of MFC-250 and MFC-1000. Considering the four biofilm samples with similar contents and component proportion, it could be assumed that MFC-10 and MFC-50 had much thicker biofilms than MFC-250 and MFC-1000. This was proved by scanning the cross-section of biofilms on the anode electrodes against the flow channel (Figure S5). In addition, it was obvious that MFC-10 and MFC-50 had a thick orange-brown biofilm, whereas a thin gray biofilm was observed on the black carbon cloth in MFC-250 and MFC-1000 (Figure S4). This was probably related to the fact that MFCs with a low external resistance resulted in a high energy gain for bacteria growth and then high biomass (Figure 2 and 3). A similar phenomenon was also observed in previous study of MFC biofilms developed at different anode potentials and current densities.35 It has been reported that a thick orange-brown biofilm could contribute to the high current density of MFCs. 35 In the present study, the relatively stable current densities of MFC-10 (14.5 mA) and MFC-50 (11.0 mA) were much higher than that of MFC-250 (2.8 mA) and MFC-1000 (0.7 mA) after day 5, supporting that conclusion. There was noted that external resistance effects on the anodic biofilm development 18 ACS Paragon Plus Environment

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is directly related with the current effects. This study indicated that a low external resistance resulted in a high current and then large coverage of biofilm on the surface of the anode, which would be beneficial for MFC biofilm distribution. Thus, the current effects is another important factor for the anodic biofilm development. Our previous study investigated the effects of discharging current on the anodic biofilm and the results showed that the coverage of the biofilm on the anode surface increased as the discharging current densities increased from 0.3 to 3.6 A/m2.

36

This indicated

that an increased current can also promote biofilm distribution.

4 Conclusions In the present study, the effects of external resistance on the startup process and the effects of mass transfer on anodic biofilm distribution were investigated in MFCs with serpentine flow fields. The experimental results showed that MFCs with a low external resistance had a slow voltage evolution but a fast energy gain for bacterial growth during startup. This led to a fast evolution of active biomass and maximal power density. However, a decreased evolution rate of active biomass and MFC performance was observed when an extra low external resistance was used for startup. With respect to anodic biofilm distribution, a low external resistance for startup led to a thick and compact biofilm. In addition, the biofilm was mainly distributed on the carbon cloth against the flow channel instead of the rib in MFCs with serpentine flow fields due to the effects of flow fields on mass transfer. The thick and compact biofilm on the surface of the carbon cloth would limit mass transfer inside porous electrode 19 ACS Paragon Plus Environment


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and then hinder biofilm development, leading to a low utilization of the porous electrode for bacterial attachment.

Supporting Information Schematic of serpentine flow field and MFC system, Biomass production as a function of energy gain for bacteria growth, Evolution of MFC performance during startup, Photos of biofilms developed at different external resistance and SEM cross-sectional micrographs of anode biofilms are given in Supporting Information.

Acknowledgements This work was supported by the National Science Foundation for Young Scientists of China (No. 51606022), the National Natural Science Funds for Distinguished Young Scholar (No. 51325602), the National Natural Science Funds for Outstanding Young Scholar (No. 51622602), and the Fundamental Research Funds for the Central Universities (106112016CDJXY145504).


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Figure Captions Figure 1. Voltage evolution of MFCs started up at different external resistances Figure 2. Evolution of energy gain for microorganism growth (a) and energy output (b) during startup process Figure 3. Evolution of active biomass in the upstream (a) and downstream (b) area of MFC biofilms during the startup process Figure 4. Evolution of maximum power density (a), current density (b) and external resistance (c) at maximum power production Figure 5. SEM micrographs of MFC-10 bioﬁlm on the carbon cloth against flow channel ((a)×1000, (b)×8000), rib ((c)×1000, (d)×8000) and cross-sectional images (e, f) Figure 6. SEM surface micrographs of anode biofilm developed at different external resistance (10 Ω, 50 Ω, 250 Ω and 1000 Ω) in MFCs with serpentine flow fields


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