Performance Improvement of Microbial Fuel Cells by Lactic Acid Bacteria and Anode Modification

Abstract

Indium Tin Oxide (ITO) conductive glass was modified by layer-by-layer modification of chitosan (CS) and α-Fe₂O₃ nanoparticles. Lactic acid bacteria were the source of electrons in the studied microbial fuel cells (MFCs) system. When ITO/(CS/α-Fe₂O₃)₄/CS was the anode, external resistance was 626.6 Ω, while maximum current and maximum power density were 1.16 mA and 0.122 W/m², respectively. These values were far higher than already reported results. Atomic force microscope image proved that ITO/(CS/α-Fe₂O₃)₄/CS surface was rougher than blank ITO and ITO/(CS/α-Fe₂O₃)₈/CS surfaces, which enable it to have a higher specific surface area for the microbes to grow. For ITO/(CS/α-Fe₂O₃)₄/CS, physical properties played a leading role, while the chemical properties mainly determined the surface morphology of ITO/(CS/α-Fe₂O₃)₈/CS. Lactic acid bacteria in fermentation waste could improve the current of MFCs. Layer-by-layer assembly of CS/α-Fe₂O₃ could significantly improve the performance of MFCs.

Introduction

Microbial fuel cells (MFCs) could deal with organic and inorganic waste matters and transform chemical energy into electrical energy (Logan et al., 2006; Abrevaya et al., 2015a, 2015b). Due to their green nature and producing clean energy, MFCs have recently gained a lot of research attention. The process of energy production takes place in four major steps. In the first step, the substrate is digested by microbes to generate electrons and protons. In the second step, the electrons are transferred from microbes to the anode surface. In the third step, the electrons reach cathode through the external circuit and protons are transferred from the microbes to cathode through a proton exchange membrane. In the final step, the reduction reaction occurs on the cathode (Jia et al., 2014).

Various substrates, which have been researched for use in MFCs as feed, include natural and synthetic compounds or wastewaters (Pant et al., 2010). Food waste is usually added to the substrate, which acts as the carbon source for the microbes in bioelectrochemical systems (ElMekawy et al., 2015). It has been proven that the prefermentation of food waste could be a useful strategy to enhance the performance of MFCs (Kannaiah and Venkata Mohan, 2011).

Fermentation is a metabolic process that converts sugars to acids, gases, or alcohol. It takes place in the lack of oxygen and becomes the cell's primary means of ATP production (Nam et al., 2014; Alibardi and Cossu, 2016). The fermentation waste, produced by many food factories, includes chemical energy, carbon sources, and lactic acid bacteria. Such waste is ideal for anaerobic digestion, which mainly consists of four steps: hydrolysis of the substrate, acidogenesis, acetogenesis, and methanogenesis (Kastner et al., 2012; Zhang et al., 2015).

Organic acids, primarily propionic and lactic acids, are obtained from the hydrolysis process and acidogenesis processes. These compounds could be used by the electricity producing microbes to transform chemical energy to electrical energy (Lobo et al., 2015). For example, the fermentation of Chinese cabbage results in a large amount of lactic acid bacteria. The lactic acid bacteria had been proved to have good ability to produce electrons (Yang Jingna and Guan, 2014). The lactic acid bacteria in fermentation waste could inhibit the growth of some other bacteria by secreting lactic acid, acetic acid, hydrogen peroxide, and lactobacillin (Delavenne et al., 2012). These secretions would inhibit the transportation of electrons from lactic acid bacteria to the anode surface.

It has been proven that lactic acid bacteria belong to Fe(III) reducing bacteria, and the existence of Fe(III) oxides could induce lactic acid bacteria to assemble an electrically conductive network, which will accelerate the ability of lactic acid bacteria, through which they transfer the electrons (Mahadevan et al., 2006). The low electron transfer rate from microbes to the anode surface was one important factor that affects the efficiency of the MFCs (Santoro et al., 2015). This problem can be solved by the modification of anode material, which would change both the physical and chemical properties of the anode and facilitate the transfer of electrons from microbes to the anode surface (Choi, 2015).

Layer-by-layer assembly of polyelectrolytes has been proven to be an effective way for improving the transfer of electrons from microbes to the anode surface (Zhu et al., 2014). For example, the layer-by-layer assembly of chitosan (CS) and α-Fe₂O₃ nanorod could improve the transferring abilities of electrons. However, the resultant current density of the MFCs was found to be very low (Ji et al., 2011; Martin et al., 2011). The maximum current observed by using CS/α-Fe₂O₃-modified Indium Tin oxide (ITO) conductive glass and the Shewanella loihica PV-4 bacteria in MFCs is just around 2 × 10⁻⁶ A, and still is very low (Ji et al., 2011). To the best of our knowledge, there still is no study focusing on using CS/α-Fe₂O₃-modified ITO to improve the performance of MFCs by using high electron producing lactic acid bacteria.

In this study, a double-compartment MFC was built by using lactic acid bacteria as the electrons producing microbes and ITO as the anode. CS/α-Fe₂O₃ was assembled on the ITO surface. The surface properties of modified ITO were investigated by the atomic force microscope (AFM). The effects of assembled polyelectrolyte and number of layers on ITO anode on current and power density were investigated. The effect of fermentation substrate on the performance of MFC was also studied. The possible mechanism of fermentation waste for improving the performance of MFC was also discussed in the current work.

Materials and Methods

Materials

ITO anode was purchased from Conduc optics and electronics tech. (jintan) Co., Ltd. (China). The chitosan (deacetylation degree 85%, Mn = 250 kDa) was obtained from Qingdao Haidebei Bioengineering Co., Ltd. (China). Sodium bicarbonate (NaHCO₃), calcium chloride (CaCl₂), Ferric chloride hexahydrate (FeCl₃ · 6H₂O), urea (purity >95%), magnesium chloride hexahydrate (MgCl₂ · 6H₂O), sodium chloride (NaCl), sodium acetate (CH₃COONa), ammonium chloride (NH₄Cl), potassium ferricyanide (K₃Fe(CN)₆), disodium hydrogen phosphate (Na₂HPO₄), sodium dihydrogen phosphate (NaH₂PO₄), potassium dihydrogen phosphate (KH₂PO₄), potassium chloride (KCl), sodium hydroxide (NaOH), hydrochloric acid (HCl), and hydrogen peroxide (H₂O₂) were purchased from China National Pharmaceutical Group Corporation. All reagents were of analytical grade and used as received.

Synthesis of α-Fe₂O₃ nanorods

α-Fe₂O₃ nanorods were synthesized using the already reported method (Ocana et al., 1999). Ferric chloride hexahydrate, urea, and sodium dihydrogen phosphate were taken in 1:1.1:0.05 molar ratio, respectively, and were dissolved in ultrapure Millipore water with the iron content of 0.01 mol/L. The solution was sealed in a bottle and kept at 100°C for 3 days. Then, the solution was cooled to room temperature and centrifuged at 10,000 rpm for 20 min. The purification process was repeated for at least five times to obtain all the nanorods. The precipitates were dried by an oven and were redispersed in distilled water with ultrasound before further use.

Modification of ITO anode

ITO was cut into 4 × 5 cm. The activation of ITO surface was done by following the reported method (Ge et al., 2013). In short, the ITO was immersed in 4% potassium hydroxide (KOH) in acetic acid (CH₃COOH) solution and treated with ultrasound for 5 min. Then, it was treated with ultrasound in ethyl alcohol and ultrapure water for 5 min, respectively. After that, the obtained ITO anode was immersed alternatively in 1% chitosan (CS) solution and 0.1 g/L α-Fe₂O₃ nanorod solution. In each step, the adsorption time was 20 min. Then ITO was immersed in ultrapure water to wash off the unabsorbed ingredients for at least 5 min. The final step is to put layer-by-layer assembled polyelectrolyte-modified ITO anode in 1% chitosan solution for 20 min and then in ultrapure water for 10 min. The electrode was dried under soft ultrapure nitrogen gas.

Characterization of α-Fe₂O₃ nanorods

Morphology of the prepared α-Fe₂O₃ nanorods was investigated using a scanning electron microscope (JSM-6360LV; Japan). Particle size distribution analysis by intensity was done using Malvern Zetasizer Nano ZSP having a range of 0.3–10.0 μm (diameter).

Characterization of ITO anode and morphology of microbes

Surface morphology of ITO was taken with Dimension 3100 Atomic Force Microscope (AFM, Bruker, Germany). The morphology of the microbes on ITO anode was characterized by scanning electron microscope (JSM-6360LV, Japan). Electrical conductivity and total solids (SS) were measured using DDS-307A conductivity instrument (LeiCi Trade Shanghai Co., Ltd., China) at 25°C. COD of the system was measured by the potassium dichromate reflux method (Baumann et al., 1974).

MFC reactor construction

The experimental instrument was a double-compartment MFC reactor. The chamber size of each compartment was 8 × 8 × 8 cm. The cultivation buffer consisting of 2.5 g/L NaHCO₃, 0.08 g/L CaCl₂, 1 g/L NH₄Cl, 0.2 g/L MgCl₂ · 6H₂O, 10 g/L NaCl, and 0.82 g/L CH₃COONa was used for bacteria growth. The working solution gradient consisted of 165 mL cultivation buffer and 135 mL fermentation waste, which was cultivated in a biochemical incubator at 37.5°C for 3 days before use. The cathode compartment was filled with 300 mL 50 mmol potassium ferricyanide solution. A proton exchange membrane (N117, Dupont, Inc., USA) was placed between the two chambers to separate them.

Both electrodes were connected to an external resistance (0–9999 Ω). The MFCs were operated in the intermittent flow mode, whereby each batch mode test continued for at least 7 days. Every MFC reactor chamber was stirred using a magnetic stirrer.

Electrochemical measurements

All the current-time curves, cyclic voltammetry (CV), open circuit potential, and polarization curves were measured by the electrochemical workstation (chi660d CH Instruments, Inc., China). The voltage and current across an external resistor (100, 300, 500, 800, 1000, 3000, 5000, 7000, and 9000 Ω) were monitored using a virtual instrument (UT803,UNI-T™) connected through a data monitor card (MPS010601; Mofei Co., Ltd., China). The current response at the electrode surface to a specific range of potentials was measured at a fixed scan rate, shifting from −1.0 to 0.5 V versus with Ag/AgCl at 5 mV/s while monitoring the current. All of the mentioned measurements were performed for the anode system.

Results and Discussion

Structure and morphology of ITO anode

Size of nanorods and zeta potential distribution of α-Fe₂O₃ nanorods are shown in Fig. 1. The average size of α-Fe₂O₃ nanorods is around 40–100 nm. It also can be seen that most of the nanorods are negatively charged. To investigate the influence of assembled layers of CS and α-Fe₂O₃ on the morphology of ITO anode, the ITO was subjected to AFM characterization before and after the layer-by-layer modification. As shown in Fig. 2, the blank ITO anode, four layers CS/α-Fe₂O₃ and one layer chitosan-modified ITO (ITO/(CS/α-Fe₂O₃)₄/CS), six layers CS/α-Fe₂O₃ and one layer chitosan-modified ITO (ITO/(CS/α-Fe₂O₃)₆/CS), and eight layers CS/α-Fe₂O₃ and one layer chitosan-modified ITO (ITO/(CS/α-Fe₂O₃)₈/CS) had different surface morphology and roughness.

FIG. 1.

(a) Mean size of α-Fe₂O₃ nanorods; (b) zeta potential of α-Fe₂O₃ nanorods. ITO, Indium Tin Oxide.

FIG. 2.

Morphology of (a) ITO blank, (b) ITO/(CS/α-Fe₂O₃)₄/CS, (c) ITO/(CS/α-Fe₂O₃)₆/CS, and (d) ITO/(CS/α-Fe₂O₃)₈/CS characterized by AFM. AFM, atomic force microscope.

The mathematical average roughness (Ra) of ITO blank was 0.791 nm, while the RMS average roughness (Rq) is 1.81 nm. Ra and Rq of ITO/(CS/α-Fe₂O₃)₄/CS had a value of 0.844 nm and 1.13 nm, respectively. The Ra and Rq values of ITO/(CS/α-Fe₂O₃)₆/CS were 0.872 and 1.27 nm, respectively. The Ra and Rq values of ITO/(CS/α-Fe₂O₃)₈/CS were 0.436 and 1.46 nm, respectively. ITO/(CS/α-Fe₂O₃)₆/CS had the maximum surface roughness, while the ITO/(CS/α-Fe₂O₃)₈/CS anode had the minimum surface roughness. The lowest surface roughness of ITO/(CS/α-Fe₂O₃)₈/CS would be due to the properties of the assembled charged polymers. With more polyelectrolyte molecules assembled on the ITO surface, the charged polymer chain became more regular, which made it smoother than the other three kinds of ITO surfaces.

The analysis of physical properties of layer-by-layer assembled polyelectrolyte had shown similar results (Han et al., 2012). Large surface roughness means large specific surface area. The thickness of the charged polymer layers increases with the assembly layer number. ITO/(CS/α-Fe₂O₃)₄/CS and ITO/(CS/α-Fe₂O₃)₈/CS were chosen for the following experiments. Figure 3 shows the SEM image of microbes on ITO blank and ITO/(CS/α-Fe₂O₃)₄/CS. The results show that there are many kinds of microbes in this substrate system. The types of the microbes have not been identified in the current work and should be done in future work. It is observed that the amount of microbes on ITO/(CS/α-Fe₂O₃)₄/CS is higher than that on the blank, which had also been proven by the microbes' activity experiment.

FIG. 3.

SEM images of microbes grow on (a, b) ITO blank and (c, d) ITO/(CS/α-Fe₂O₃)₄/CS anodes. SEM, scanning electronic microscopy.

The phosphatide method was used for checking the microbes' activity (Aelterman et al., 2008). The results showed that the amount of microbes on the ITO/(CS/α-Fe₂O₃)₄/CS was around 80 mg biomass-C, while that on ITO blank was 56 mg biomass-C. This might be attributed to the morphology and change in chemical composition of the ITO surface.

Current-time curves

Figure 4 shows the current-time curves of MFCs with the blank and modified ITO anode. As can be seen, the current produced by ITO/(CS/α-Fe₂O₃)₄/CS was far higher than that produced by ITO/(CS/α-Fe₂O₃)₈/CS, which were both far higher than the blank ITO anode. When the external resistance is 1000 Ω, the maximum current of ITO/(CS/α-Fe₂O₃)₄/CS anode reaches 0.63 mA. After functioning for 4800 min, its electronic current begins to decrease slowly and reaches the final value of 0.41 mA.

FIG. 4.

Current-time curves of the MFCs with ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS anodes. MFC, microbial fuel cell.

The maximum current of ITO/(CS/α-Fe₂O₃)₈/CS could reach 0.43 mA and also begins to decrease slowly after running for 3000 min. Its current was relatively stable and remained constant at 0.32 mA until the end of the operation. The maximum current of ITO blank is 0.25 mA after 3000 min. It decreases to 0.10 mA after operating for 9000 min. The current-time result was related to the surface morphology and chemical component of ITO anode. After CS/α-Fe₂O₃ modification, the performance of MFCs was dramatically increased. The current of this substrate system is far higher than the current (2 × 10⁻⁶ A), which was obtained for the reported system (Ji et al., 2011).

Cyclic voltammetry

To evaluate the effect of modification of ITO with CS/α-Fe₂O₃ and CS on electrochemical performance of anode, CV measurements were performed after the anodes had operated in MFCs for 24 h (Fig. 5). ITO/(CS/α-Fe₂O₃)₄/CS and ITO/(CS/α-Fe₂O₃)₈/CS anode had one oxidation current and one reduction current. ITO blank anode had one oxidation current and two reduction currents. The results of CVs, as shown in Fig. 5, were in accordance with the results of the current-time curves in Fig. 4.

FIG. 5.

CV curves of ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS anodes. CV, cyclic voltammetry.

Obviously, the ITO/(CS/α-Fe₂O₃)₄/CS anode had a higher oxidation peak than ITO/(CS/α-Fe₂O₃)₈/CS anode, both of which are far higher than the corresponding value of ITO blank. It meant microbes on ITO/(CS/α-Fe₂O₃)₄/CS anode had higher activities than ITO/(CS/α-Fe₂O₃)₈/CS and ITO blank anode. This also explains the reason why ITO/(CS/α-Fe₂O₃)₄/CS and ITO/(CS/α-Fe₂O₃)₈/CS anode had higher current than the blank ITO anode in the studied MFCs system. There are two reduction peaks in the ITO blank anode, which might be attributed to the Fe³⁺ in K₃Fe(CN)₆ that was deoxidized to Fe²⁺ and then to Fe in catholyte compartment.

In fact, the increases in redox peak and current are probably due to several factors. One of them is the change in microenvironment of the ITO surface, which altered the activities of the microbes and the interaction between microbes and anode. The outer layer of modified ITO surface is polyelectrolyte CS, which had a very good biocompatibility and could attract more microbes to adhere and grow. Large surface roughness means large specific surface area, which also was good for more microbes to grow. The existence of negative α-Fe₂O₃ could induce some microbes to assemble into the electrically conductive network, which was built by microbes (Mahadevan et al., 2006).

The α-Fe₂O₃ nanorods also improved the electron transferring efficiency in the extracellular network of microbes. Both chemical and physical properties influenced the results in the ITO/(CS/α-Fe₂O₃)₄/CS and ITO/(CS/α-Fe₂O₃)₈/CS anode systems. The higher roughness of ITO/(CS/α-Fe₂O₃)₄/CS resulted in higher specific surface area of the system and, due to the anchoring of more microbes with higher activities, resulted in high performance of MFCs.

Electrochemical impedance spectroscopy and polarization curves

Figure 6 shows the polarization curves of MFCs with ITO blank and modified anodes. It can be seen that the voltage of ITO blank remained unchanged with the increase of current density. After calculations, its internal resistance was 1524 Ω. ITO/(CS/α-Fe₂O₃)₈/CS anode system showed a similar trend with the ITO blank anode. Its internal resistance was found to be 1018.6 Ω. The voltage curve of ITO/(CS/α-Fe₂O₃)₄/CS anode system became smooth with the increase of current density, whereas its internal resistance was 626.6 Ω.

FIG. 6.

Polarization curves of MFCs with ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS anodes.

Power densities of MFCs with ITO blank and modified anodes are shown in Fig. 7. The power density of ITO/(CS/α-Fe₂O₃)₄/CS is higher than those of ITO/(CS/α-Fe₂O₃)₈/CS and ITO blank anode. The maximum power densities of ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS were found to be 0.035, 0.124, and 0.084 W/m², respectively. This is in accordance with the current, CV, and polarization curves. It was attributed to the surface roughness of ITO/(CS/α-Fe₂O₃)₄/CS, which was far higher than the blank ITO and ITO/(CS/α-Fe₂O₃)₈/CS. Physical factor strongly influenced the higher power density of ITO/(CS/α-Fe₂O₃)₄/CS anode system, while the chemical factors strongly affected the results of ITO/(CS/α-Fe₂O₃)₈/CS anode system.

FIG. 7.

Power density curves of MFCs with ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS anodes.

Variations in other factors in MFC system

COD removal efficiency of ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS anode system was 69.8%, 76%, and 74%, respectively. The original pH value of anode substrate was 6.96, and after dealing with the ITO/(CS/α-Fe₂O₃)₄/CS and ITO/(CS/α-Fe₂O₃)₈/CS, the pH value changed to 7.28 and 7.72, respectively. The anode system changed from week acidic state to week basic state, which proved that a good proton transfer ability was maintained in the MFC system (Rozendal et al., 2006). The values of electrical conductivity of cathode compartment were found to be 1097 μs/cm (for ITO blank anode system), 2010 μs/cm (for ITO/(CS/α-Fe₂O₃)₄/CS anode system), and 1936 μs/cm (for ITO/(CS/α-Fe₂O₃)₈/CS anode system).

Conclusions

Lactic acid bacteria in fermentation waste could improve the current of MFCs. The roughness of ITO/(CS/α-Fe₂O₃)₄/CS is higher than the corresponding value of ITO blank and ITO/(CS/α-Fe₂O₃)₈/CS. The current and activities of microbes in ITO/(CS/α-Fe₂O₃)₄/CS anode system are higher than those found in ITO/(CS/α-Fe₂O₃)₈/CS and ITO blank systems. The values for internal resistance of ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS were 1524, 1018.6, and 626.6 Ω in the MFCs wastewater treatment system, respectively.

The values for maximum power density of ITO blank, ITO/(CS/α-Fe₂O₃)₄/CS, and ITO/(CS/α-Fe₂O₃)₈/CS were 0.035, 0.124, and 0.084 W/m², respectively. The higher roughness of ITO/(CS/α-Fe₂O₃)₄/CS resulted in higher specific surface area available for growth of more microbes. The physical properties had a stronger effect on ITO/(CS/α-Fe₂O₃)₄/CS anode. The layer-by-layer assembly of CS/α-Fe₂O₃ could significantly improve the performance of MFCs. The exact type of bacteria and metabolic pathway of the microbes are still uncertain and need to be identified in future research work.

Footnotes

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 41373127), the Program for Liaoning Excellent Talents in University of China (No. LR2015052), Liaoning Provincial Natural Science Foundation of China (No. 2013020082), Science and Technology special fund of Shenyang City under Grant (No. F14-207-6-00), General project of the Education Department of Liaoning Province (No. L2015428), and the Zhejiang Open Foundation of the Most Important Subjects.

Author Disclosure Statement

No competing financial interests exist.

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Performance Improvement of Microbial Fuel Cells by Lactic Acid Bacteria and Anode Modification

Abstract

Abstract

Introduction

Materials and Methods

Materials

Synthesis of α-Fe2O3 nanorods

Modification of ITO anode

Characterization of α-Fe2O3 nanorods

Characterization of ITO anode and morphology of microbes

MFC reactor construction

Electrochemical measurements

Results and Discussion

Structure and morphology of ITO anode

Current-time curves

Cyclic voltammetry

Electrochemical impedance spectroscopy and polarization curves

Variations in other factors in MFC system

Conclusions

Footnotes

Acknowledgments

Author Disclosure Statement

References

Synthesis of α-Fe₂O₃ nanorods

Characterization of α-Fe₂O₃ nanorods