ON/OFF states of a microbial fuel cell controlled by an optical switching system

Abstract

An optical signal was successfully used to reversibly switch the ON/OFF states of a microbial fuel cell via an optical switching system consisting of a functionalized electrode and a photoacid. Using this switching system as the controlling component achieved the effective, fast and reliable control of a microbial fuel cell.

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Microbial fuel cells (MFCs) are receiving much interest from researchers in different fields as a result of their potential applications in wastewater treatment, bioelectrochemical synthesis and for use as biosensors.^1–4 Achieving effective and reliable control of an MFC is an important issue.^5,6 The most suitable parameter for controlling an MFC is the electrical current, but little work has been reported about how to control the current production of an MFC. In recent years, enzymatic fuel cells based on stimuli-responsive electrodes have been developed and proposed for applications in signal processing, biofuel cell power switching, information storage and transduction.^7–11 However, the core parts of these enzymatic fuel cells are electrochemically active enzymes. Compared with enzymatic fuel cells, MFCs are more difficult to control by external signals. This is because the electrochemically active bacteria, the core part of MFCs, are more robust than enzymes. Thus it is harder for external signals to affect bacterial activity and, in turn, control the MFC. Also, the complexity of the bacteria's genetic regulation system and their metabolic processes make the response sluggish.¹² Therefore, to our knowledge, the best way to control an MFC is to control the electrodes rather than the bacteria. Stimuli-responsive functionalized interfaces provide us with this possibility.^13–16

Typical stimuli-responsive functionalized interfaces are fabricated by grafting a stimuli-responsive chemical matrix onto a conductive electrode material. Interfaces sensitive to changes in pH are the most mature stimuli-responsive interfaces and are usually made by modifying the bare electrode with a pH-sensitive polymer layer; the electrode conductivity can be controlled by the degree of swelling or shrinking of the polymer layer. Swelling or shrinking of the polymer layer is dependent on the environmental pH. Thus, to control the electric current production of an MFC equipped with an electrode modified with a pH-sensitive interface, the pH of the medium should be artificially tuned to a certain level.¹⁷ In most cases, the pH-sensitive interface is controlled by dosing with acids/alkalis, or with other chemicals that can be transformed to acids or alkalis by specific reactions, e.g. glucose oxidation and urea degradation.^18,19 To reset the MFC, the pH should be tuned back to the initial level.²⁰ Other chemicals are therefore needed to dose the system, which results in the accumulation of chemicals and by-products, decreasing the stability and reproducibility of the system. Instead of these invasive signals, using non-contact signals, e.g. light, temperature and magnetic fields, to trigger the shift in pH and then controlling the production of the current would have the following advantages: (1) fewer side-effects; (2) easier control; and (3) more compatibility with different types of control unit. Most environmental factors, e.g. light and temperature, are non-contact signals. Therefore developing an MFC controlled by non-contact signals provides the possibility of building “smart” MFCs that could be self-regulated according to variations in the environment.

In the work reported here, we demonstrated an optical switching system to control an MFC. To bridge the optical signal and the electric current production of an MFC, the optical switching system consists of two components: a photoacid and an ITO electrode with a poly(4-vinyl pyridine) (P4VP)-modified interface. The photoacid can reversibly undergo photo-isomerization on illumination with light, which releases protons and therefore decreases the solution pH.²¹ When the light illumination is removed, the photoacid recombines with the protons, increasing the pH to the initial level. Through the photo-isomerization processes of the photoacid, the photoacid can transduce an optical signal to a pH shift; the conductivity of the ITO electrode with the P4VP-modified interface is sensitive to the pH value. Therefore, combining these two components into a cathode chamber for an MFC can switch the production of current by the MFC with an optical signal.

To investigate the performance of the synthesized photoacid and the fabricated electrode, the properties of the photoacid and the polymer-modified electrode were first tested separately. The photoacid, a merocyanine with a propyl sulfonate group on the nitrogen of the indoline moiety, could reversibly change the solution pH by optical signals based on photo-isomerization reactions (Fig. 1a). In the absence of illumination, the photoacid (MEH) solution is predominantly in the form of protonated merocyanine (ME), which is a weak acid. Under illumination (λ_max = 419 nm), ME isomerizes rapidly, undergoing a 6π-electrocyclic ring-closing reaction and then complete dissociation of a proton.²² This process transforms the MEH from the ME state to the SP⁺ state, which is a strong acid and thus decreases the solution pH. These transformations caused by the optical signal are reversible.

Fig. 1 (a) Transformation of the photoacid among the MEH, ME and SP⁺ states. (b) Variation in pH of the photoacid solution (600 μM) with and without illumination (λ = 405 nm).

In our illumination test, the initial pH of the photoacid solution was adjusted to 6.1 to obtain the largest ON/OFF current ratio. When the photoacid solution (600 μM) was illuminated (laser transmitter, λ = 405 nm, 100 mW), the pH dropped dramatically from 6.1 to 4.5 and then became stable at pH 4.5. When the illumination was removed, the pH value recovered to the initial level (pH 6.1) (Fig. 1b). In addition to the range of pH variation to control the pH-sensitive interface, our photoacid has another two merits. The first of these merits is fast photo-isomerization: a 600 μM solution of photoacid can release enough protons to decrease the solution pH from 6.1 to 4.5 in 2 minutes and the pH can recover within 6 minutes, which is enough time to switch the pH-sensitive interface. The second merit is the long-lived photo-isomerized state of the photoacid (at least 5 minutes), which leaves enough time to activate the pH-sensitive interface. Even after the pH variation experiments had been repeated 15 times, the pH variation was still stable (data not shown). Based on the results obtained, the photoacid is suitable to trigger the activation of the pH-sensitive interface.

As another important component of the optical switching system, the electrode with the pH-sensitive interface was fabricated by grafting the pH-sensitive polymer P4VP onto the single-side conducting glass of the ITO electrode. The functionalized ITO electrode was evaluated in a standard potentiostatically controlled three-electrode system using cyclic voltammetry (CV). The pH of the electrolyte (without the photoacid) was artificially adjusted by an HCl or NaOH solution. When the electrolyte was at pH 6.0, a small reduction peak (I_max = −65 μA) was seen in the cyclic voltammogram (Fig. 2). When the electrolyte was at pH 4.4, the height of the reduction peak dramatically increased (I_max = −196 μA). These changes were attributed to the morphological change of the polymer interface caused by the variation in the pH of the electrolyte solution. Specifically, when the pH of the electrolyte was about 6.1, the tethered P4VP chains collapsed on the ITO glass and the shrunken hydrophobic polymer prevented the permeation of the potassium ferricyanide ions into the ITO conducting base.¹⁷ When the pH of the electrolyte was about 4.4, the pyridine functional groups on the polymer chains were ionized into the positively charged hydrophilic state. This resulted in swelling of the polymer layer and, as a consequence, the ITO conductive surface became accessible. Therefore the [Fe(CN)₆]³⁻ ions were attracted to the ITO surface and were reduced on the surface. Theoretically, no reduction peak is observed in the cyclic voltammograms at pH 6.1. However, there was still a minor [Fe(CN)₆]³⁻ reduction peak in the cyclic voltammograms (at about −65 μA), which might be due to grafting defects on the electrode surface. Although the electrode was not perfect, the low level current in the OFF state was still acceptable compared with the current signal in the ON state (the ratio of the ON/OFF current, i.e. the ratio of the reduction peak height at the ON state to that at the OFF state, was around 3). The current in the OFF state was about −65 μA, which indicated that the functionalized interface was not completely shrunken. This allowed the bacteria to respire with the anode in the MFC mode when the cathode of the MFC was in the OFF state.

Fig. 2 Cyclic voltammograms of the functionalized electrode at different electrolyte pH values.

Reproducibility is another important factor in the evaluation of the reliability of the functionalized electrode. The electrode was therefore switched between the ON and OFF states repeatedly for five cycles. The peak heights at pH 4.4 and 6.1 were both recorded. The ratio of the ON/OFF current was stable (around 3), which indicated that the functionalized electrode was reliable for multiple switches.

After being tested separately, the photoacid and the functionalized electrode were integrated into an optical switching system. The most important three indices representing the overall performance of the optical switching system are the ratio of the ON/OFF current, the response time and the reproducibility. The larger the ratio of the ON/OFF current, the better the ON and OFF states are defined. We repeatedly switched the system for 15 cycles and the ratio obtained from CV measurements was stabilized around 1.7 (Fig. 3), whereas the ratio obtained from chronoamperometry (CA) measurements was 1.34 ± 0.03 (averaged from three cycles). This difference was because the results obtained from CV were instantaneous values and the ratios deduced from CA were 5 minute averaged values. Katz et al.²³ built a similar optical switching system based on Au electrodes modified with a photo-isomerizable nitrospiropyran/nitromerocyanine monolayer. The ratios of the electrical responses at the ON and OFF states varied from 1.90 to 2.20, which are higher than our results. However, our system is more versatile.

Fig. 3 (a) Reduction peak current in cyclic voltammograms in the ON and OFF states and pH variations over 15 cycles. (b) Variation in chronoamperometric current and pH controlled by an optical signal.

The integration of the photoacid and the functionalized electrode provides a method of producing a quick ON/OFF switch. The response time for switching from the OFF state to the ON state was 4.33 ± 1.73 minutes and the response time for switching from the ON state to the OFF state was 5.67 ± 0.57 minutes (averaged from three cycles). Compared with a pH switching system based on enzymatic reactions, our optical switching system based on a photo-isomerizable reaction has a shorter response time. For example, Tam et al.¹¹ developed a dual-enzyme controlled interface to enable and reset a glucose biosensor; the enable time was around 5 minutes and the reset time was about 20 minutes, which is four times longer than our optical signal switching system. Another advantage of our system compared with switching systems based on enzymatic reactions is the input to the system: our optical signal is non-contact. A non-contact input signal can minimize the impact on the MFCs compared with a contact signal (e.g. dosing chemicals). Our optical switching system offers the possibility of utilizing visible light or sunlight as an input signal to control MFCs. With the help of the long-distance transmission properties of lasers, this system could possibly be controlled remotely by a laser. For practical applications, our optical switching system could be used to achieve in situ and real-time control of marine sediment MFCs with a laser beam.

To evaluate the reproducibility of the system, we repeatedly switched the system with an optical signal. Even after being switched 15 times, the ratios of the ON/OFF current were still relatively stable (Fig. 3a). This indicated that our optical switching system is reliable. However, compared with the performance of the photoacid and the functionalized electrode when tested separately, both the variation in pH range and the ratio of the ON/OFF current decreased. This may be due to the equilibrium among the MEH, ME and SP + states of the photoacid being disturbed by the ionization of the modified polymer on the ITO base. To improve this performance, future work should focus on developing some alternatives for the photoacid or the polymer layer to eliminate this interference.

Finally, we integrated the optical switching system into the cathode chamber of a dual-chambered MFC to achieve the goal of controlling an MFC between the ON and OFF states with light. The two chambers were separated by proton exchange membrane and an external resistance of 1000 Ω was connected between the anode and the cathode. The anode chamber was inoculated with electrochemically active bacteria and the bacteria could not make contact with the photoacid solution. The voltage produced by the MFC was chosen as the output signal and a laser was used as the input signal. As shown in Fig. 4, the voltage of the MFC increased dramatically once the cathode chamber was exposed to illumination. When the illumination was removed, the voltage dropped immediately to the initial level (1.55 ± 0.27 minutes to turn it on and 3.09 ± 0.16 minutes to reset). The ratio of the ON/OFF current was around 1.68 ± 0.02 (averaged over four cycles). Therefore the optical switching system could be used to achieve the fast and reliable switching of an MFC. MFC-based biosensors are becoming a promising technology in a number of different fields. Our system can provide two potential applications in this area: (1) reversible switching of the biosensor between the ON and OFF states with an optical signal; and (2) our optical switching system can adjust the measuring range of a biosensor using a laser beam.

Fig. 4 Voltage production of the MFC controlled by an optical signal.

Conclusions

An optical switching system for MFCs has been developed. The two components of the system are a photoacid and a P4VP-modified electrode. We first successfully synthesized the photoacid and fabricated the functionalized electrode. The switching system was then tested in a potentiostatically controlled three-electrode system. The ratio of the ON/OFF current was stabilized at around 1.7 and the response time for switching from the OFF state to the ON state was 4.33 ± 1.73 minutes and the reverse process took 5.67 ± 0.57 minutes. We repeated the optical switching for 15 cycles and the ratio of the ON/OFF current and the response time were both stable. This indicated that the optical switching system was reliable and had a fast response time. Finally, we successfully used our system to control an MFC. The voltage of the MFC was reversibly switched between high and low levels over multiple cycles. Based on this result, this optical switching system could provide a new solution to controlling MFCs.

Acknowledgements

We gratefully acknowledge the financial support by National Natural Science Foundation of China (Grant no. 21206145) and China Postdoctoral Science Foundation (Grant no. 2012M510147).

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