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Hybrid Glucose/O2 Biobattery and Supercapacitor Utilizing a Pseudocapacitive Dimethylferrocene Redox Polymer at the Bioanode Krysti L. Knoche,† David P. Hickey,† Ross D. Milton,† Carol L. Curchoe,‡ and Shelley D. Minteer*,† †
Department of Chemistry and Department of Materials Science and Engineering, University of Utah, Salt Lake City, Utah 84112, United States ‡ 32ATPs, Salt Lake City, Utah 84103, United States S Supporting Information *
ABSTRACT: Small implantable electronic devices require biologically compatible energy sources that are capable of delivering quick high-energy pulses. Combining batteries and supercapacitors allows for high power and energy density while providing both small size and biocompatibility. Here, we report a hybrid supercapacitor/biobattery whereby an oxygen-reducing cathode of bilirubin oxidase immobilized with anthracene-modified carbon nanotubes and tetrabutylammonium bromide-modified Nafion is coupled with a glucose bioanode of flavin adenine dinucleotide-dependent glucose dehydrogenase. The redox polymer, dimethylferrocene-modified linear poly(ethylenimine), used at the bioanode simultaneously immobilizes enzyme, mediates electron transfer, and acts as a pseudocapacitor where capacitance of the anode scales with increased polymer loading. Both multiwalled carbon nanotubes and carbon felt incorporated into the anode construction improve polymer conductivity, subsequently resulting in further improved anodic capacitance. A supercapacitor/biobattery device of the above configuration results in a specific capacitance of 300 ± 100 F/g, which is over 4 times higher than that of other reported biologically derived supercapacitors.
T
method for entrapping one or more enzymes in a 3-D polymer network, resulting in a high loading of both enzyme and nondiffusive mediator near the electrode surface. Covalently bound redox species in these high-enzyme loading systems are traditionally thought to act as electron relays to enhance electrochemical communication throughout the cross-linked polymer network.19 Although EFCs have the high energy density required for implantable applications, they have relatively low power density (i.e., low energy delivery per time). As a possible alternative approach, capacitors are devices that are charged by an external power source, but they are capable of storing charge that can be rapidly discharged. By applying the principles of redox-mediated bioelectrocatalysis and EFCs in the context of pseudocapacitance, we suggest that a hybrid supercapacitor/EFC can combine the increased power density of a capacitor with the biocompatibility of an EFC.
here is a need for renewable, efficient power-generating devices for implantable applications. In particular, small, implantable electronic devices such as pacemakers, neurostimulators, or defibrillators need to deliver pulsed energy in quick bursts.1−3 Enzymatic energy sources are effective biocompatible alternatives to traditional energy storage systems like fuel cells and secondary batteries. Enzymatic fuel cells (EFCs) and biobatteries have been developed that operate at near-neutral pH and ambient temperatures, making them good candidates for small, implantable devices.2,4−9 Glucose/ O2 EFCs are the most studied candidates for powering small implantable devices,2,3,10 and various glucose/O2 EFCs have been implanted and successfully operated in a variety of organisms including insects, lobsters, and rats.3,10−18 There is a large body of research investigating various EFC design strategies, especially for improving electron transfer from the enzymes to the electrodes and immobilizing enzymes at electrode surfaces.7,19−21 Redox polymers contain covalently bound electron mediators and are an effective class of materials for both electron transfer and enzyme immobilization.4,8,19,20 Redox polymers are cross-linked onto electrode surfaces as a © 2016 American Chemical Society
Received: June 22, 2016 Accepted: July 14, 2016 Published: July 19, 2016 380
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ACS Energy Letters
surface area for a bioanode of FAD-GDH immobilized on Toray carbon paper with ethylene glycol diglycidyl ether (EGDGE) cross-linked FcMe2-LPEI. Figure 1 shows an overlay
Electrochemical supercapacitors are viewed as a bridge between batteries and classical supercapacitors because they can store high energy density while being capable of rapid charge and discharge.22−24 Electrochemical double layer (EDL) capacitance results from charge separation in the Helmholtz layer at the electrode interface, whereas pseudocapacitors derive capacitance from faradaic redox processes.25−28 Common EDL devices consist of carbon materials and have specific capacitance of ∼20−200 F g−1.29 Pseudocapacitors are commonly based on conducting polymers or electrolyte/ metal oxide electrode interactions with specific capacitances reported in the range of 200−800 F g −1 . 1,26−28,30,31 Pseudocapacitance from redox polymers is not as well studied, although specific capacitances of 130−475 F g−1 have been reported for some quinone-based redox polymer supercapacitors.32 No hybrid devices utilizing redox polymers have previously been reported. Most supercapacitors are charged by separate external devices/sources, but there are examples of hybrid systems combining supercapacitors with batteries or fuel cells in nonbiological systems,28 biobased systems,33,34 and hybrid combinations therein.35,36 Hybrid systems are especially advantageous for implantation over individual battery and supercapacitor devices due to size limitations. Given the advantages of both devices, combining enzymatic catalysis with a charge-storing matrix to achieve a small, efficient power system is appealing because the enzymes provide the means of recharging the system, removing the need for an external charging source. A redox polymer provides further advantages of both an effective EFC immobilization and mediation strategy and faradaic charge storage. Because the mediator is immobilized as a polymer, there is no need for a proton exchange membrane to prevent crossover, further decreasing device size requirements. Previously, an EDL system was reported in which enzymes and multiwalled carbon nanotubes (MWCNTs) were pressed into pellets and soaked in fuel,34 and a conducting polymer hybrid has been reported where a polypyrrole-modified cellulose bioanode is used in a flow EFC/ supercapacitor,31,33 although capacitance is relatively low for both systems. Here, a glucose/O2 EFC with a redox polymer bioanode was converted to a hybrid supercapacitor/biobattery to enhance capacitive performance to be competitive with other reported hybrids. The anode consists of flavin adenine dinucleotide-dependent glucose dehydrogenase (FAD-GDH) and MWCNTs immobilized within a dimethylferrocenemodified linear poly(ethylenimine) (FcMe2-LPEI) redox polymer on carbon felt,37,38 where high loading of FcMe2LPEI provides capacitance. The cathode consists of bilirubin oxidase (BOx) immobilized with MWCNTs covalently functionalized with anthracene and tetrabutylammonium bromide (TBAB)-modified Nafion on carbon felt.39,40 Anthracene functionalities facilitate direct electron transfer of BOx and permit the enzyme to undergo a 4e− reduction of O2 to H2O at near-neutral pH. The pseudocapacitance of the FcMe2-LPEI was initially studied as a bioanode in a three-electrode setup, and a supercapacitor/biobattery device was created and subsequently analyzed for supercapacitive behavior. Constant current charge/discharge (CCD) cycles are a standard method for determining capacitance.25 The capacitance (F) can be calculated as C = i(∂E/∂t)−1, where i (A) is the current and ∂E/∂t (V/s) is the change in potential divided by the time required for discharge. The FcMe2-LPEI loading was varied between 0.7 and 6 mg cm−2 of the geometric electrode
Figure 1. (a) Overlay of 10 μA CCD curves for FAD-GDH anodes on Toray paper with various loadings of FcMe2-LPEI in 200 mM phosphate/citrate buffer, pH 6.5. Loadings are 0.7 (black line), 1 (blue line), 3 (green line), and 6 mg cm−2 (red line). (b) Capacitance calculated from these curves is plotted versus the polymer loading, and (c) specific capacitance is plotted versus the polymer loading.
of 10 μA (6 mA g−1) CCD cycles for bioanodes with different FcMe2-LPEI loadings. Control CVs of unmodified Toray paper and Toray paper modified only with FcMe2-LPEI (no enzyme present) are included in Figure S1 in the Supporting Information, and an overlay of CVs corresponding to the CCDs in Figure 1 can be found in Figure S2. The anode capacitance increased with increased polymer loading. Even when capacitance was normalized by the mass of the polymer (i.e., specific capacitance), the capacitance increased with higher polymer loading. The 6 mg cm−2 polymer loading resulted in 80 ± 10 F g−1, which is on the same order of magnitude as the specific capacitance of high-surface-area carbon materials like MWCNTs (∼20−200 F g−1). In optimizing the supercapacitor/biobattery device, MWCNTs were added to the 381
DOI: 10.1021/acsenergylett.6b00225 ACS Energy Lett. 2016, 1, 380−385
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ACS Energy Letters bioanode, and the electrode material was changed from Toray paper to carbon felt to improve polymer conductivity. The MWCNT loading was optimized by testing anodes with a range of 0−16 mg MWCNTs per cm−2 electrode area. Optimal loading was found to be 4 mg cm−2, which further increased the bioanode specific capacitance to 105 ± 10 F g−1. A plot of specific capacitance versus MWCNT loading is provided in Figure S3 in the Supporting Information. The above data demonstrate that redox polymers can greatly enhance the specific capacitance of a bioelectrode. In order to combine this capacitive bioelectrode with an EFC to produce a hybrid device, we first evaluated the performances of the EFC biocathode and bioanode individually. Figure 2a shows overlaid cyclic voltammograms (CVs) for a biocathode in N2-sparged, air-equilibrated, and O2-sparged solutions of 200 mM glucose in pH 6.5 200 mM phosphate/citrate buffer. Currents are higher when there is more O2 present, confirming oxygen bioelectrocatalysis. Figure 2b shows overlaid CVs for anodes with 0.7 and 6 mg cm−2 polymer in buffer and in 200 mM glucose in buffer. While currents from the ferrocene redox reaction are higher when polymer loading is higher (due to a higher concentration of ferrocene on the electrode), the bioelectrocatalytic currents upon glucose addition are much more similar. This is to be expected given that both electrodes have the same enzyme loading. In all anode CVs, there appear to be two overlapping reductive ferrocene peaks. This is likely an effect of the MWCNTs, which seem to create a second redox environment for the ferrocene pendent. An adsorption effect occurs where the reduced ferrocene moiety is not particularly water-soluble and thus is partially adsorbed onto the MWCNT surface. Figure S4 in the Supporting Information demonstrates CVs of anodes without any MWCNT present, in which only a single reductive ferrocene peak is observed. Figure 2c shows polarization and power curves for BOx/FAD-GDH EFC devices with either 0.7 or 6 mg cm−2 polymer loading. EFCs with higher polymer loading have higher maximum current densities and higher maximum power densities. The open-circuit potential (OCP) for devices with both polymer loadings was 0.6 ± 0.2 V. The average maximum current density Jmax and average maximum power density Pmax for 0.7 mg FcMe2-LPEI cm−2 devices were 8.4 ± 1 mA cm−2 and 1.7 ± 0.2 mW cm−2, respectively. Devices containing 6 mg FcMe2LPEI cm−2 had Jmax and Pmax of 12 ± 2 mA cm−2 (38 ± 7 mA cm−3) and 3.0 ± 0.5 mW cm−2 (10 ± 2 mW cm−3), respectively. These values are competitive with reported values for the hybrid flow EFC (Jmax = 6 mA cm−2, Pmax = 0.6 mW cm−231,33) and hybrid CNT pellet EFC (Jmax = 37.7 mA cm−3, Pmax = 20.1 mW cm−334) mentioned above. The electrochemical stability of FcMe2-LPEI by itself and in EFCs has been studied previously. Films of FcMe2-LPEI operated continuously at 0.3 V vs SCE for 48 h still retained 60% of the original current density,38,41 and an EFC consisting of a FcMe2-LPEI/ glucose oxidase anode and poly[(vinylpyridine)Os(bipyridyl)2Cl2+/3+/laccase cathode still retained 55% of the original power density after 48 h of continuous operation at maximum power.38 After evaluating the fuel cell performance of the hybrid supercapacitor/EFC, we evaluated the capacitance properties of the hybrid supercapacitor/EFC. Figure 3a shows an overlay of 100 μA (6 mA g−1) CCD curves for FAD-GDH/BOx devices with 0.7 and 6 mg cm−2 FcMe2-LPEI anode loadings. The morphology of the curves is typical of hybrid devices where there is an initial iR drop as would be observed for a battery,
Figure 2. (a) Overlay of 5 mV s−1 CVs for a BOx cathode in a N2sparged (solid line), air-equilibrated (long dashed line), and O2sparged (dashed line) solution of 200 mM glucose in 200 mM phosphate/citrate buffer, pH 6.5. (b) Overlay of 10 mV s−1 CVs for FAD-GDH anodes with 0.7 (black lines) and 6 mg cm−2 FcMe2LPEI loading (red lines) in buffer (solid lines) and in a solution of 200 mM glucose in buffer (dashed lines). (c) Polarization (black lines) and power (blue lines) curves for FAD-GDH/BOx devices with 0.7 (dashed lines) and 6 mg cm−2 FcMe2-LPEI (solid lines) anode loading in an O2-sparged solution of 200 mM glucose in buffer.
but then, the voltage decreases linearly over time as would be observed for a capacitor. The specific capacitance calculated for 6 mg cm−2 FcMe2-LPEI devices is 300 ± 100 F g−1, which is competitive with reported values for activated carbon EDLs mentioned above.29,34 Other methods for evaluating capacitance include current pulse chronopotentiometry (CPCP) and CV.1,25 CCD curves are the capacitor industry standard, but CPCP allows evaluation of device performance for very fast bursts of power delivery, and CV allows elucidation of the capacitance mechanism (i.e., EDL or pseudocapacitance) by scan rate variation. Here, all three techniques were used for a thorough evaluation of the device and as a means of comparing results to other reported hybrid EFC devices. Figure 3b,c shows 382
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Figure 3. (a) Overlay of CCD curves for a FAD-GDH/BOx device with 0.7 (black line) and 6 mg cm−2 FcMe2-LPEI (red line) anode loading in O2-sparged 200 mM glucose and 200 mM phosphate/citrate buffer, pH 6.5. (b) Overlay of 1 mA CPCPs for a FAD-GDH/BOx device with 0.7 (black line) and 6 mg cm−2 FcMe2-LPEI (red line) anode loading. (c) 1 mA CPCP for a FAD-GDH/BOx device with 6 mg cm−2 FcMe2LPEI anode loading. (d,e) Overlays of various scan rate CVs for a FAD-GDH/BOx device with 0.7 (d) and 6 mg/cm2 FcMe2-LPEI loading (e). Scan rates are 3 (green lines), 5 (red lines), 10 (blue lines), and 20 mV s−1 (black lines).
CPCPs for FAD-GDH/BOx devices with 0.7 and 6 mg cm−2 FcMe2-LPEI anode loadings. In Figure 3b, 1 mA pulses of current were demanded for 1 s to discharge the device; then the device was left to recharge back to OCP. While 1 mA pulses used up all of the 0.7 mg cm−2 FcMe2-LPEI device’s potential, the 6 mg cm−2 FcMe2-LPEI device was able to withstand 2 mA (130 mA g−1) pulses, as shown in Figure 3c. The capacitance calculated from the 2 mA pulse is 16 ± 2 F g−1, where each pulse delivered approximately 1 mW (13 mW cm−3) in 1 s. This value is more than 2000 times higher than the 6 mF g−1 calculated from reported CPCPs (10 ms pulses of 3 mA) for the CNT pellet EFC.34 Lower capacitances are generally calculated from CPCPs due to the brevity of the pulses. Figure 3d,e shows overlays of various scan rate CVs for FAD-GDH/ BOx devices with 0.7 and 6 mg cm−2 FcMe2-LPEI loadings. Plots of the current versus scan rate for both devices are linear, indicating capacitive behavior. The 0.7 mg cm−2 FcMe2-LPEI device exhibits linearity of R2 = 0.98, and the 6 mg cm−2 FcMe2LPEI device exhibits R2 = 0.99. After normalizing currents by scan rate, they do not superimpose and the lowest scan rate
gives the highest value, confirming that the majority of observed capacitance is due to pseudocapacitance from the ferrocene rather than an EDL effect. Specific capacitance for the 6 mg cm−2 device calculated from 1 mV s−1 CVs was 230 ± 60 F g−1, which is not statistically different from that obtained from the CCD cycles. This value is more than 400% higher than the 67 F g−1 reported for the flow EFC from a 1 mV s−1 CV.33 The EFC and capacitance experiments showed that the utilization of redox polymer mediated bioelectrocatalysis in an EFC can be used to make a hybrid supercapacitor/EFC device with high power densities and high specific capacitance. Table 1 compares the results for this device with the other hybrid enzyme-based systems mentioned above. Cosnier and coworkers reported a system of compressed pellets of MWCNTs and enzymes (glucose oxidase, GOx, and catalase anode and laccase cathode), which they measured by CPCP.34 Their results here are considered relative to the geometric electrode volume for comparison; in addition, their device did not employ electron mediators. In addition, Bilewicz and co383
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ACS Energy Letters Table 1. Comparison of Enzyme-Based Hybrid Supercapacitor Systems literature report device description: enzymes electrode materials fuel solutions electrode dimensions: geometric area geometric volume fuel cell measurements: OCP Pmax Jmax capacitance measurements: current pulse constant current discharge cyclic voltammetry a
Cosnier34
Bilewicz31,33
this work
BFC in beaker
flow BFC
biobattery
GOx, catalase/ laccase compressed pellets of MWCNT + enzyme 200 mM glucose, 0.2 M buffer, pH 7 13 mm diameter, 6 mm thick MWCNT pellet
FDH/laccase
FAD-GDH/BOx
anode: acetylene black + polypyrrole/cellulose + FDH on carbon paper cathode: naphthylated CNT + Nafion + laccase on carbon paper 100 mM fructose, 0.2 M buffer, pH 5.3
anode: ferrocene-LPEI + FAD-GDH + MWCNT on carbon felt cathode: anthracene-MWCNT + TBAB-Nafion + BOx on carbon paper 200 mM glucose, 0.2 M buffer, pH 6.5
carbon paper
5 × 5 × 3.18 mm carbon felt
3.14 cm2
0.25 cm2 0.0795 cm3
0.7 V 2 mW flow, 1.5 mW stationary
0.6 ± 0.2 V 0.8 mW (3 mW cm−2, 10 mW cm−3)
6 mA cm−2a
3 mA (12 mA cm−2, 38 mA cm−3)
pseudocapacitance
pseudocapacitance
0.796 cm3
0.67 ± 0.1 V 16 mW (20.1 mW cm−3) 30 mA (37.7 mA cm−3) electrostatic double layer 6 mF g−1
67 F g
16 ± 2 F g−1 300 ± 100 F g−1
65 F g−1
230 ± 60 F g−1
−1
Reference 33.
workers reported on the capacitance of fructose dehydrogenase (FDH) anodes with polypyrrole-modified cellulose31 and a flow EFC using their FDH anode and a laccase cathode.33 This device utilized conducting polymers rather than redox polymers. Table 1 demonstrates the advantages of utilizing redox polymers for making hybrid devices that produce both high energy density and high power density due to the pseudocapacitance of the redox polymer. In conclusion, a hybrid supercapacitor/biobattery device has been created with a specific capacitance of 300 ± 100 F g−1. The device had an OCP of 0.6 ± 0.2 V, Jmax of 12 ± 2 mA cm−2 (38 ± 7 mA cm−3), and Pmax of 3.0 ± 0.5 mW cm−2 (10 ± 2 mW cm−3). Enzymes catalyze the oxidation of glucose and reduction of O2 to provide energy, which is stored by the pseudocapacitive redox polymer FcMe2-LPEI. Capacitance of the system scales with increased loading of redox polymer. The capacitance, OCP, maximum current density, and maximum power density are competitive with those of other reported systems and show the clear advantage of mediated bioelectrocatalysis via redox polymers in improving performance. This has great implications for powering small, implantable devices. Combining enzyme catalysis with a charge-storing matrix allows for a small, efficient system with high power output while maintaining the recharge capability and high energy density of a battery.
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Experimental methods, cyclic voltammetry of control anodes, cyclic voltammetry of bioanodes with various polymer loadings, carbon felt bioanode CVs without MWCNTs present, and MWCNT loading optimization plot (PDF)
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors acknowledge the National Science Foundation, USDA-NIFA, and USTAR for funding. REFERENCES
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsenergylett.6b00225. 384
DOI: 10.1021/acsenergylett.6b00225 ACS Energy Lett. 2016, 1, 380−385
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