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Hemoproteins–nickel foam hybrids as effective supercapacitors† Mohamed Khairya and Sherif A. El-Safty*ab
Received 24th October 2013, Accepted 25th November 2013 DOI: 10.1039/c3cc48155g www.rsc.org/chemcomm
The immobilization of hemeproteins onto a nickel foam electrode was developed for the first time, and the electrode exhibits remarkable electrochemical performance with higher capacitance and stability compared to synthetic pseudocapacitors.
Electrochemical energy storage systems have a vital function in everyday life because of the limitations in renewable energy production from the sun and the wind, as well as in the development of electric or hybrid electric vehicles with low CO2 emissions.1 At the forefront of these energy storage devices are rechargeable batteries and electrochemical supercapacitors (ECs). Recently, ECs have drawn a great deal of interest compared to batteries because batteries suffer from a relatively slow power delivery or uptake.2,3 The ECs are the best candidates for energy storage because of their unique energy buffers, reliable life cycle (10 000 cycles), low internal resistance, fast charge and discharge rates, high power densities, and their applicability in biological environments.4 However, a number of problems prevent ECs from becoming commercially viable, in particular, their energy density is insufficient, and most fabrication processes are costly and inappropriate for large-scale manufacturing.2,5 Thus, constructing an EC with high power and high energy densities has become a challenge for the future of energy storage devices. The recent studies have focused on the synthesis of active porous nanomaterials with improved properties. The electroactive materials include metal oxides, hydroxides6–10 or sulfides11 and carbon-based materials.12,13 Among all of these materials, the conducting polymers store charge pseudocapacitively (200–3000 F g 1).13 These materials provide high capacitance but have several disadvantages, such as high cost, tedious fabrication steps, and difficult scaleup. To overcome this drawback, Malvankar et al.14 suggested the use of a conductive microbial biofilm on a gold electrode to enhance the
device capacitance. The electrochemical performance of a Geobacter sulfurreducens biofilm is related to the heme groups of the c-type cytochromes (CytC), which readily provide a large electron-storage capacity. Thus, CytC functions as an electron sink as well as a capacitor. Metalloproteins containing heme binding sites within various protein scaffolds have crucial functions in electron transfer, substrate oxidation, metal ion storage, ligand sensing, and transport.15 Thus, the breadth of electrochemical function of proteins of known structure has provided a wealth of information on the various factors that set and modulate heme redox activity. The demand for a more sustainable and economical energy storage has led to a renewed scientific and commercial interest in advanced supercapacitor electrode designs. Recently, a nanomagnet-selective captor of hemeproteins, CytC, myoglobin (Mb), and hemoglobin (Hb), based on NiO nanoparticles (NPs) was developed.16 The present study proposes a simple supercapacitor electrode design based on a commercially available 3D porous Ni foam (NF) electrode immobilized with hemeproteins (Scheme 1 and Fig. S1, ESI†). In fact, the specific capacitance (Cs) was enhanced about five times compared to the Ni foam. The proof of concept is provided with the study of the unusual binding efficiency of the porous nickel-based material and the hemeproteins (BEads = 211.45 kcal mol 1),16 as well as that of
a
National Institute for Materials Science, 1-2-1 Sengen, Tsukuba-shi, Ibaraki-ken 305-0047, Japan b Graduate School for Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan. E-mail: [email protected] † Electronic supplementary information (ESI) available: Experimental procedures, SEM, EDX, CV, discharge curves, and EIS of Ni–protein film. See DOI: 10.1039/c3cc48155g
This journal is © The Royal Society of Chemistry 2014
Scheme 1 Schematic representation of the charge–discharge redox mechanism of the NF protein film, where x is the thickness of the Ni(II) layer and y is the thickness of the protein film.
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Fig. 1 SEM-EDX mapping of Hb-film onto the Ni foam electrode, the distribution of nickel, carbon, iron, nitrogen, oxygen, and sulphur.
the binding affinity of the latter with oxygen molecules that enhance the redox process through the heme group (Fig. S2, ESI†). Moreover, the 3D nanostructure protein network and the porous architecture of the Ni electrode are the key factors that determine the application of our electrode in energy storage devices. Nickel foam is commercially available and possesses distinct features, such as exceptional uniformity, light weight, high porosity, intrinsic strength, corrosion resistance, and high magnetic, electrical, and thermal conductivities. The SEM micrographs reveal a 3D crosslinked grid structure that contains small and large open pores ranging from 50 mm to 500 mm (Fig. S3, ESI†). The chemical composition and distribution mapping of the Ni–protein film are shown in Fig. 1 and Fig. S4 in ESI.† The EDX mapping showed a 3D porous network consisting of Ni, C, Pt, O, N, S, and Fe. The Ni atoms are uniformly distributed over the entire surface area of NF. The C, O, N, S, and Fe atoms are components of Hb (Fig. S2, ESI†). This elemental ratio of the NF hybrid indicates that the Ni foam is in metallic form. The electrochemical performance of the Ni–protein film electrode as an electrochemical supercapacitor was investigated. Fig. 2 and Fig. S5 (ESI†) show the typical CV curves of the NF and protein films in 6 M NaOH as recorded at different voltage scan rates. The curves are mainly characteristic of Faradaic pseudocapacitive material. Initially, the electrode was stabilized for 50 cycles in alkaline media prior to the final measurement. These CV cycles indicated the
Fig. 2 (A) Typical CV curves of 0.68 mg of Hb immobilized onto the NF electrode. (B) Correlation between Ip vs. n1/2 of Hb. Calculated specific capacitance (C) and derived energy and power densities as a function of the scan rate (D). [Note that the Cs, E and P values were calculated based on total mass of the electrodes (100.68 mg).]
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formation of active sublayers from Ni(OH)2 and Ni(OH)3 according to the Pourbaix diagram.17 The CV patterns show a pair of redox current peaks related to the oxidation of the Ni(II)/Ni(III) species in the form of g-NiOOH.17 The anodic peak potential of the NF–protein film shifted toward a more positive potential with increasing scan rate. In addition, the DEp (Epa Epc) increased, and the ratios of the current peaks (Ipa/Ipc) approached unity. The unsymmetrical nature of the redox peaks indicated the quasi-reversible redox process of the NF–protein film. The peak current is linearly correlated with n1/2, which indicated that the electrochemical process was controlled by the diffusion of [OH ] into the porous network (Fig. 2B). Significantly, the peak current of Hb-film is enhanced about three times more than the Ni-foam electrode. These findings indicated that the Hb film not only enhances the electron transfer but also increases the active sites of NF. Moreover, the slight shift in the peak potentials of the NF–protein film may be due to the dehydration of Ni(OH)2 and Ni(OH)3 or to the formation of a NiO sublayer, depending on the protein type (Scheme 1).17,18 Hemeproteins exhibit a nanostructured network with porous architecture.14 In particular, Hb is an intelligent molecule because it varies its activity in response to environmental stimuli.19 In alkaline media, the immobilized Hb shows a higher surface activation for the 3D porous network of NF than those of Mb and CytC (see ESI†). Therefore, the nanostructured metalloproteins on the 3D porous network with the active film are the major factors that affect the electrochemical performance. The Cs values were calculated from the CV measurements according to eqn (S1) (see ESI†). The high specific capacitance of the Hb film was due to the rapid electron transfer arising from the strong binding affinity between the heme group and the Ni surface.17 This binding affinity may increase the usage of the surface materials and enhance the electron transfer and diffusion of ions through the 3D-porous network. The outstanding electrochemical performance of the Hb film supercapacitor is expected to provide remarkable specific energy in rapid charging–discharging processes. This finding indicated that the immobilization of biomolecules onto Ni foam might open new avenues for the fabrication of a new generation of supercapacitors (Fig. 2D and Fig. S6 in ESI†). Rate capability is one of the important factors used for evaluating the power application of supercapacitors. The constant current galvanostatic discharge curves of the Ni-film electrode at different discharge currents were measured (Fig. 3 and Fig. S7 in ESI†). The Hb film exhibited a longer discharge time than Mb and CytC. This result
Fig. 3 (A) Galvanostatic discharge curve at different discharge currents (0.4 mA to 10 mA) for Hb films. (B) Calculated Cs as a function of the discharging current for different electrodes. The Cs was calculated based on the total mass of the electrode (100.68 mg).
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indicates that the Hb film has enhanced electrochemical reactivity with lower polarization. This finding was confirmed previously by CV measurements (Fig. 2). The Cs of the supercapacitor can be determined from a charge–discharge experiment using eqn (S2) (see ESI†). The results are presented in Fig. 3B. At 0.4 mA, the Hb film had a specific capacitance of 13.8 F g 1, whereas those of Mb and CytC were 8.9 and 8.2 F g 1, respectively. The specific capacitance was calculated based on the total weight of the NF electrode (100 mg) and protein film. However, the calculated Cs related only to the weight of the protein film was 2052, 1460, and 1213 F g 1 for Hb, Mb, and CytC respectively, which is comparable to a synthetic supercapacitor.6–13 Noticeably, the Cs for the Hb, Mb, and CytC films remained as high as 11.9, 8.2, and 6.9 F g 1, respectively, even when the discharge current was increased to 10 mA. These findings reveal that the capacitance was enhanced five times more than that resulting from the NF electrode by using proteins. The reliability of the capacitance measurements was investigated through the immobilization of increasing quantities of Hb on the NF electrode surface (Fig. S8A in ESI†). A direct correlation between the immobilized Hb mass and Cs was observed, which indicates the high stability, high capability rate, and applicability of the Hb film for highperformance supercapacitor applications.17 Moreover, the EIS profile indicates accumulation of electrolyte ions at the electrode surface, which reveals the ideal capacitive behavior (Fig. S8 and S9, ESI†). A continuous galvanostatic charge–discharge cycling at a constant current of 0.4 mA over 1000 cycles was performed (Fig. S10, ESI†). The porous Hb film shows a markedly superior cycling behavior. At 1000 cycles, the capacitance retention drops only by 2.5% of its initial value. However, the specific capacitance of Mb decreased by 28.4%, respectively. Such superior pseudocapacitive performance is rarely observed and may be attributed to a fast electron transfer, a 3D porous network, an impressive binding between Hb and the Ni electrode and formation of superoxide and/or peroxide that enhanced the surface active sites of the NF electrode. To understand the mechanism behind the high capacitance of the Ni–Hb platform, Banks et al. suggested the evaluation of oxygen molecules in alkaline media at a relatively high voltage (+0.65 V vs. SCE) of the NiO-screen-printed electrode as follows:17,18 4OH $ O2 + 2H2O + 4e This electrochemical reaction is also catalyzed by the redox coupling of the nickel species (Ni2+/Ni3+). Regarding the function of hemeprotein functionality, the heme group has crucial physiological functions, which are referred to as the gasotransmitters in biological systems. Hb consists of four polypeptides and four heme groups that can bind four O2 molecules (versus one for Mb) and exhibits a sigmoidal shape that closely resembles allosteric enzymes.20 Theoretically, the immobilization of 0.136 mg of Hb at the Ni electrode surface can accumulate and store around 4.82 1015 molecules of oxygen. Moreover, these oxygenated heme groups of proteins (Hb and Mb) lead to the formation of superoxides in the heme pocket.21 These superoxide radicals can accumulate at the electrode surfaces where the metal atoms are under-coordinated and they can react further to form surface adsorbed HO or O2 . In terms of its bonding with the surface metal atoms, the adsorbed HO forms an open shell structure. Interestingly, Mb functions as an oxygen-storage protein rather than an oxygen-transport protein (Hb) because it has a very strong binding
This journal is © The Royal Society of Chemistry 2014
affinity for oxygen molecules. Moreover, its structure helps prevent superoxides (O2 ) from leaving the heme group.20 These findings indicate that Hb is responsible for the high surface activation rather than Mb and CytC because of the transport of superoxides into the 3D porous network of NF. In addition, the superoxides may be catalyzed by iron in the heme pocket to form peroxide radicals in situ according to Fenton’s reaction (Scheme 1).17,18 Fe3+ + H2O2 $ Fe2+ + OOH + H+ These findings indicate that the immobilization of Hb on the surface of the NF working electrode in alkaline medium leads to the formation of superoxide and/or peroxide radicals, which enhance the surface active sites of the NF. Such protein film subsequently increases the active material usage because of rapid electron transfer in addition to the storage reservoir for ions and radicals. In turn, powerful, highly stable Faradaic reactions occur in energy storage devices even at high current densities. In conclusion, we developed a simple and low-cost supercapacitor design based on commercial 3D porous Ni foam and hemeproteins (Hb, Mb, and CytC). The controlled immobilization of biomolecules onto the electrode while maintaining their full biological activity, as well as the effective electronic connection between the redox-active sites of biomolecules and the electrode surface, shows evidence of the design of an advanced electrode. The Hb–Ni hybrid electrode showed remarkable specific capacitance in terms of the reliability, and retention at various current densities, making this electrode design one of the promising supercapacitors.
Notes and references 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
P. Simon and Y. GoGotSi, Nat. Mater., 2008, 7, 845–854. Q. Lu, J. G. Chen and J. Q. Xiao, Angew. Chem., Int. Ed., 2013, 52, 1882. S. Chen, J. Duan, Y. Tang and S. Z. Qiao, Chem.–Eur. J., 2013, 19, 7118. J. Hur, K. Im, S. Hwang, B. Choi, S. Kim, S. Hwang, N. Park and K. Kim, Sci. Rep., 2013, 3, 1282. Z. Yang, J. Zhang, M. C. W. K. Meyer, X. Lu, D. Choi, J. P. Lemmon and J. Liu, Chem. Rev., 2011, 111, 3577–3613. R. B. Ambade, S. B. Ambade, N. K. Shrestha, Y.-C. Nah, S.-H. Han, W. Lee and S.-H. Lee, Chem. Commun., 2013, 49, 2308–2310. Q. Lu, M. W. Lattanzi, Y. Chen, X. Kou, W. Li, X. Fan, K. M. Unruh, J. G. Chen and J. Q. Xiao, Angew. Chem., Int. Ed., 2011, 50, 6847–6850. J. Kang, A. Hirata, L. Kang, X. Zhang, Y. Hou, L. Chen, C. Li, T. Fujita, K. Akagi and M. Chen, Angew. Chem., Int. Ed., 2013, 52, 1664. C. Guan, X. Li, Z. Wang, X. Cao, C. Soci, H. Zhang and H. J. Fan, Adv. Mater., 2012, 24, 4186–4190. H. Jiang, J. Ma and C. Li, Adv. Mater., 2012, 24, 4197–4202. J.-Y. Lin and S.-W. Chou, RSC Adv., 2013, 3, 2043–2048. C. M. Yang, Y. J. Kim, M. Endo, H. Kanoh, M. Yudasaka, S. Iijima and K. Kaneko, J. Am. Chem. Soc., 2007, 129, 20–21. H. Jiang, P. S. Lee and C. Li, Energy Environ. Sci., 2013, 6, 41–53; C. Peng, D. Hu and G. Z. Chen, Chem. Commun., 2011, 47, 4105–4107. N. S. Malvankar, T. Mester, M. T. Tuominen and D. R. Lovley, ChemPhysChem, 2012, 13, 463–468. C. J. Reedy and B. R. Gibney, Chem. Rev., 2004, 104, 617–649. M. Khairy, S. A. El-Safty and M. Ismael, Chem. Commun., 2012, 48, 10832–10834. P. M. Hallam, D. K. Kampouris, R. O. Kadara, N. Jenkinson and C. E. Banks, Anal. Methods, 2010, 2, 1152–1155. A. Seghiouer, J. Chevalet, A. Barhoun and F. Lantelme, J. Electroanal. Chem., 1998, 442, 113. M. Perrella and R. Russo, News Physiol. Sci., 2003, 18, 232–236. R. H. Garrett and C. M. Grisham, Biochemistry, Brooks/Cole Cengage learning, 4th edn, 2010, vol. 15, pp. 467–474, ISBN-13: 9780495109358. C. Balagopalakrishna, P. T. Manoharan, O. O. Abugo and J. M. Rifkind, Biochemistry, 1996, 35, 6393–6398.
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Cite this: DOI: 10.1039/c3cc48155g
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Hemoproteins–nickel foam hybrids as effective supercapacitors† Mohamed Khairya and Sherif A. El-Safty*ab
Received 24th October 2013, Accepted 25th November 2013 DOI: 10.1039/c3cc48155g www.rsc.org/chemcomm
The immobilization of hemeproteins onto a nickel foam electrode was developed for the first time, and the electrode exhibits remarkable electrochemical performance with higher capacitance and stability compared to synthetic pseudocapacitors.
Electrochemical energy storage systems have a vital function in everyday life because of the limitations in renewable energy production from the sun and the wind, as well as in the development of electric or hybrid electric vehicles with low CO2 emissions.1 At the forefront of these energy storage devices are rechargeable batteries and electrochemical supercapacitors (ECs). Recently, ECs have drawn a great deal of interest compared to batteries because batteries suffer from a relatively slow power delivery or uptake.2,3 The ECs are the best candidates for energy storage because of their unique energy buffers, reliable life cycle (10 000 cycles), low internal resistance, fast charge and discharge rates, high power densities, and their applicability in biological environments.4 However, a number of problems prevent ECs from becoming commercially viable, in particular, their energy density is insufficient, and most fabrication processes are costly and inappropriate for large-scale manufacturing.2,5 Thus, constructing an EC with high power and high energy densities has become a challenge for the future of energy storage devices. The recent studies have focused on the synthesis of active porous nanomaterials with improved properties. The electroactive materials include metal oxides, hydroxides6–10 or sulfides11 and carbon-based materials.12,13 Among all of these materials, the conducting polymers store charge pseudocapacitively (200–3000 F g 1).13 These materials provide high capacitance but have several disadvantages, such as high cost, tedious fabrication steps, and difficult scaleup. To overcome this drawback, Malvankar et al.14 suggested the use of a conductive microbial biofilm on a gold electrode to enhance the
device capacitance. The electrochemical performance of a Geobacter sulfurreducens biofilm is related to the heme groups of the c-type cytochromes (CytC), which readily provide a large electron-storage capacity. Thus, CytC functions as an electron sink as well as a capacitor. Metalloproteins containing heme binding sites within various protein scaffolds have crucial functions in electron transfer, substrate oxidation, metal ion storage, ligand sensing, and transport.15 Thus, the breadth of electrochemical function of proteins of known structure has provided a wealth of information on the various factors that set and modulate heme redox activity. The demand for a more sustainable and economical energy storage has led to a renewed scientific and commercial interest in advanced supercapacitor electrode designs. Recently, a nanomagnet-selective captor of hemeproteins, CytC, myoglobin (Mb), and hemoglobin (Hb), based on NiO nanoparticles (NPs) was developed.16 The present study proposes a simple supercapacitor electrode design based on a commercially available 3D porous Ni foam (NF) electrode immobilized with hemeproteins (Scheme 1 and Fig. S1, ESI†). In fact, the specific capacitance (Cs) was enhanced about five times compared to the Ni foam. The proof of concept is provided with the study of the unusual binding efficiency of the porous nickel-based material and the hemeproteins (BEads = 211.45 kcal mol 1),16 as well as that of
a
National Institute for Materials Science, 1-2-1 Sengen, Tsukuba-shi, Ibaraki-ken 305-0047, Japan b Graduate School for Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-8555, Japan. E-mail: [email protected] † Electronic supplementary information (ESI) available: Experimental procedures, SEM, EDX, CV, discharge curves, and EIS of Ni–protein film. See DOI: 10.1039/c3cc48155g
This journal is © The Royal Society of Chemistry 2014
Scheme 1 Schematic representation of the charge–discharge redox mechanism of the NF protein film, where x is the thickness of the Ni(II) layer and y is the thickness of the protein film.
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Fig. 1 SEM-EDX mapping of Hb-film onto the Ni foam electrode, the distribution of nickel, carbon, iron, nitrogen, oxygen, and sulphur.
the binding affinity of the latter with oxygen molecules that enhance the redox process through the heme group (Fig. S2, ESI†). Moreover, the 3D nanostructure protein network and the porous architecture of the Ni electrode are the key factors that determine the application of our electrode in energy storage devices. Nickel foam is commercially available and possesses distinct features, such as exceptional uniformity, light weight, high porosity, intrinsic strength, corrosion resistance, and high magnetic, electrical, and thermal conductivities. The SEM micrographs reveal a 3D crosslinked grid structure that contains small and large open pores ranging from 50 mm to 500 mm (Fig. S3, ESI†). The chemical composition and distribution mapping of the Ni–protein film are shown in Fig. 1 and Fig. S4 in ESI.† The EDX mapping showed a 3D porous network consisting of Ni, C, Pt, O, N, S, and Fe. The Ni atoms are uniformly distributed over the entire surface area of NF. The C, O, N, S, and Fe atoms are components of Hb (Fig. S2, ESI†). This elemental ratio of the NF hybrid indicates that the Ni foam is in metallic form. The electrochemical performance of the Ni–protein film electrode as an electrochemical supercapacitor was investigated. Fig. 2 and Fig. S5 (ESI†) show the typical CV curves of the NF and protein films in 6 M NaOH as recorded at different voltage scan rates. The curves are mainly characteristic of Faradaic pseudocapacitive material. Initially, the electrode was stabilized for 50 cycles in alkaline media prior to the final measurement. These CV cycles indicated the
Fig. 2 (A) Typical CV curves of 0.68 mg of Hb immobilized onto the NF electrode. (B) Correlation between Ip vs. n1/2 of Hb. Calculated specific capacitance (C) and derived energy and power densities as a function of the scan rate (D). [Note that the Cs, E and P values were calculated based on total mass of the electrodes (100.68 mg).]
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formation of active sublayers from Ni(OH)2 and Ni(OH)3 according to the Pourbaix diagram.17 The CV patterns show a pair of redox current peaks related to the oxidation of the Ni(II)/Ni(III) species in the form of g-NiOOH.17 The anodic peak potential of the NF–protein film shifted toward a more positive potential with increasing scan rate. In addition, the DEp (Epa Epc) increased, and the ratios of the current peaks (Ipa/Ipc) approached unity. The unsymmetrical nature of the redox peaks indicated the quasi-reversible redox process of the NF–protein film. The peak current is linearly correlated with n1/2, which indicated that the electrochemical process was controlled by the diffusion of [OH ] into the porous network (Fig. 2B). Significantly, the peak current of Hb-film is enhanced about three times more than the Ni-foam electrode. These findings indicated that the Hb film not only enhances the electron transfer but also increases the active sites of NF. Moreover, the slight shift in the peak potentials of the NF–protein film may be due to the dehydration of Ni(OH)2 and Ni(OH)3 or to the formation of a NiO sublayer, depending on the protein type (Scheme 1).17,18 Hemeproteins exhibit a nanostructured network with porous architecture.14 In particular, Hb is an intelligent molecule because it varies its activity in response to environmental stimuli.19 In alkaline media, the immobilized Hb shows a higher surface activation for the 3D porous network of NF than those of Mb and CytC (see ESI†). Therefore, the nanostructured metalloproteins on the 3D porous network with the active film are the major factors that affect the electrochemical performance. The Cs values were calculated from the CV measurements according to eqn (S1) (see ESI†). The high specific capacitance of the Hb film was due to the rapid electron transfer arising from the strong binding affinity between the heme group and the Ni surface.17 This binding affinity may increase the usage of the surface materials and enhance the electron transfer and diffusion of ions through the 3D-porous network. The outstanding electrochemical performance of the Hb film supercapacitor is expected to provide remarkable specific energy in rapid charging–discharging processes. This finding indicated that the immobilization of biomolecules onto Ni foam might open new avenues for the fabrication of a new generation of supercapacitors (Fig. 2D and Fig. S6 in ESI†). Rate capability is one of the important factors used for evaluating the power application of supercapacitors. The constant current galvanostatic discharge curves of the Ni-film electrode at different discharge currents were measured (Fig. 3 and Fig. S7 in ESI†). The Hb film exhibited a longer discharge time than Mb and CytC. This result
Fig. 3 (A) Galvanostatic discharge curve at different discharge currents (0.4 mA to 10 mA) for Hb films. (B) Calculated Cs as a function of the discharging current for different electrodes. The Cs was calculated based on the total mass of the electrode (100.68 mg).
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indicates that the Hb film has enhanced electrochemical reactivity with lower polarization. This finding was confirmed previously by CV measurements (Fig. 2). The Cs of the supercapacitor can be determined from a charge–discharge experiment using eqn (S2) (see ESI†). The results are presented in Fig. 3B. At 0.4 mA, the Hb film had a specific capacitance of 13.8 F g 1, whereas those of Mb and CytC were 8.9 and 8.2 F g 1, respectively. The specific capacitance was calculated based on the total weight of the NF electrode (100 mg) and protein film. However, the calculated Cs related only to the weight of the protein film was 2052, 1460, and 1213 F g 1 for Hb, Mb, and CytC respectively, which is comparable to a synthetic supercapacitor.6–13 Noticeably, the Cs for the Hb, Mb, and CytC films remained as high as 11.9, 8.2, and 6.9 F g 1, respectively, even when the discharge current was increased to 10 mA. These findings reveal that the capacitance was enhanced five times more than that resulting from the NF electrode by using proteins. The reliability of the capacitance measurements was investigated through the immobilization of increasing quantities of Hb on the NF electrode surface (Fig. S8A in ESI†). A direct correlation between the immobilized Hb mass and Cs was observed, which indicates the high stability, high capability rate, and applicability of the Hb film for highperformance supercapacitor applications.17 Moreover, the EIS profile indicates accumulation of electrolyte ions at the electrode surface, which reveals the ideal capacitive behavior (Fig. S8 and S9, ESI†). A continuous galvanostatic charge–discharge cycling at a constant current of 0.4 mA over 1000 cycles was performed (Fig. S10, ESI†). The porous Hb film shows a markedly superior cycling behavior. At 1000 cycles, the capacitance retention drops only by 2.5% of its initial value. However, the specific capacitance of Mb decreased by 28.4%, respectively. Such superior pseudocapacitive performance is rarely observed and may be attributed to a fast electron transfer, a 3D porous network, an impressive binding between Hb and the Ni electrode and formation of superoxide and/or peroxide that enhanced the surface active sites of the NF electrode. To understand the mechanism behind the high capacitance of the Ni–Hb platform, Banks et al. suggested the evaluation of oxygen molecules in alkaline media at a relatively high voltage (+0.65 V vs. SCE) of the NiO-screen-printed electrode as follows:17,18 4OH $ O2 + 2H2O + 4e This electrochemical reaction is also catalyzed by the redox coupling of the nickel species (Ni2+/Ni3+). Regarding the function of hemeprotein functionality, the heme group has crucial physiological functions, which are referred to as the gasotransmitters in biological systems. Hb consists of four polypeptides and four heme groups that can bind four O2 molecules (versus one for Mb) and exhibits a sigmoidal shape that closely resembles allosteric enzymes.20 Theoretically, the immobilization of 0.136 mg of Hb at the Ni electrode surface can accumulate and store around 4.82 1015 molecules of oxygen. Moreover, these oxygenated heme groups of proteins (Hb and Mb) lead to the formation of superoxides in the heme pocket.21 These superoxide radicals can accumulate at the electrode surfaces where the metal atoms are under-coordinated and they can react further to form surface adsorbed HO or O2 . In terms of its bonding with the surface metal atoms, the adsorbed HO forms an open shell structure. Interestingly, Mb functions as an oxygen-storage protein rather than an oxygen-transport protein (Hb) because it has a very strong binding
This journal is © The Royal Society of Chemistry 2014
affinity for oxygen molecules. Moreover, its structure helps prevent superoxides (O2 ) from leaving the heme group.20 These findings indicate that Hb is responsible for the high surface activation rather than Mb and CytC because of the transport of superoxides into the 3D porous network of NF. In addition, the superoxides may be catalyzed by iron in the heme pocket to form peroxide radicals in situ according to Fenton’s reaction (Scheme 1).17,18 Fe3+ + H2O2 $ Fe2+ + OOH + H+ These findings indicate that the immobilization of Hb on the surface of the NF working electrode in alkaline medium leads to the formation of superoxide and/or peroxide radicals, which enhance the surface active sites of the NF. Such protein film subsequently increases the active material usage because of rapid electron transfer in addition to the storage reservoir for ions and radicals. In turn, powerful, highly stable Faradaic reactions occur in energy storage devices even at high current densities. In conclusion, we developed a simple and low-cost supercapacitor design based on commercial 3D porous Ni foam and hemeproteins (Hb, Mb, and CytC). The controlled immobilization of biomolecules onto the electrode while maintaining their full biological activity, as well as the effective electronic connection between the redox-active sites of biomolecules and the electrode surface, shows evidence of the design of an advanced electrode. The Hb–Ni hybrid electrode showed remarkable specific capacitance in terms of the reliability, and retention at various current densities, making this electrode design one of the promising supercapacitors.
Notes and references 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
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