Bioelectronic Energy Storage: A Pseudocapacitive Hydrogel

Sep 2, 2016 - Renewable-Biomolecule-Based Electrochemical Energy-Storage Materials. Hua Wang , Yun Yang , Lin Guo. Advanced Energy Materials 2017 7 (2...
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Bioelectronic Energy Storage: A Pseudocapacitive Hydrogel Composed of Endogenous Biomolecules Craig A. Milroy and Arumugam Manthiram* S Supporting Information *

ABSTRACT: Advances in bioelectronics have produced implantable devices for in vivo biosensing and therapeutics, but batteries for implantable devices currently require bulky metal cases to sequester toxic electrolytes and immunogenic active materials; therefore, development of new materials is paramount for safety and miniaturization. Implantable batteries could be fully biocompatible if they exclusively comprised endogenous materials. Accordingly, we present an energy-storage material fabricated entirely from endogenous biomolecules via one-step carbodiimide conjugation of dopamine (DA) to hyaluronic acid (HA). The DAHA composite can be electropolymerized to create a pseudocapacitive biopolymer, p(DAHA), that exhibits catechol−quinone interconversion, stability, long-term electroactivity for 400 cycles, and high pseudocapacitance (up to ∼900 F g−1) and discharge capacity (∼130 mAh g−1 at ∼10 A g−1). These characteristics predispose it for bioelectronic energy storage, i.e., as a supercapacitor or, when coupled with an implantable Ag/AgCl electrode, a biobattery with an operating voltage of ∼0.85 V. ter11,12 that forms the molecular basis for neuromelanin, which is chemically similar to other pigmentary melanins found in skin, hair, and eyes.13 Melanins display hydration-dependent mixed ionic-electronic conductivity,14,15 and their biochemical precursors (e.g., dopamine, 5,6-dihydroxyindole, and 5,6dihydroxyindole-2-carboxylic acid) exhibit catechol−quinone redox functionality;11,16 thus, these macromolecules are excellent candidates for implantable energy-storage materials. However, because of the hypothesized role of dopamine deficiency in schizophrenia and Parkinson’s disease,17 the vast majority of the electrochemical studies of dopamine have been devoted to in vivo sensing and detection, and very few studies have evaluated melanins for energy storage.18,19 Unfortunately, electronics and batteries for implantable medical devices are particularly challenging to fabricate because, in addition to the exigent requirements for reliability, biocompatibility, and/or biodegradability, implantable materials and devices must also resist nonspecific protein adsorption,4,5 as biofouling is the primary contributor to decreased sensitivity of implantable devices such as glucose sensors.20 In this context, biological hydrogels have proven useful for masking implantable devices because they are soft, elastic, and highly permeable to low molecular weight molecules; they also

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he United States National Academy of Engineering has presented the need to “advance health informatics” among its 14 grand challenges for engineering in the 21st century.1 Therefore, the development of implantable therapeutic and monitoring devices that seamlessly interface with biological systems would have enormous utility for “precision medicine”. Bioelectronics, in concert with the “Internet of Things”, which seeks to enable the facile integration of implantable devices with “big data”-driven health monitoring, promises to empower personalized healthcare.2 Accordingly, diverse groups have developed electronic devices fabricated with biocompatible materials for diagnostic and/or therapeutic use in living tissue.3−5 In contrast, the field of implantable energy-storage materials is relatively unexplored,6−9 and batteries for implantable devices currently require bulky casing because they contain toxic electrolytes and nonendogenous materials10 that elicit immune responses which negatively impact device performance and long-term functionality.4 Heller recognized that batteries for implantable biomedical devices could be effectively miniaturized “if the anode and the cathode, as well as their reaction products, were safe enough for implantation into the subcutaneous interstitial fluid, so that the fluid would serve as the electrolyte, i.e., the need for both the electrolytic solution and the case would be removed”.6 Ideally, implantable devices could achieve maximum biocompatibility if they exclusively comprised endogenous materials. In this context, dopamine is an electroactive, essential neurotransmit© XXXX American Chemical Society

Received: August 5, 2016 Accepted: September 2, 2016

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DOI: 10.1021/acsenergylett.6b00334 ACS Energy Lett. 2016, 1, 672−677

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http://pubs.acs.org/journal/aelccp

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ACS Energy Letters Scheme 1. Dopamine−Hyaluronic Acid Synthesis

effectively resist the nonspecific protein adsorption that leads to cell adhesion and biofouling.21 Moreover, diverse groups have formulated hydrogels containing redox-active moieties (e.g., ferrocene, osmium-bipyridine, viologens, quinones, etc.) and used these electroactive “redox hydrogels” to electrically connect redox-active sites in enzymes directly to biosensor electrodes.21−24 This prior research inspired us to synthesize a redox hydrogel based entirely on endogenous biomolecules for use as an energy-storage material. To combine the electroactive properties of dopamine and the nonadhesive biocompatibility of hydrogels, we chemically conjugated hyaluronic acid (HA) and dopamine (DA) to form an electroactive biocomposite. Hyaluronic acid is an endogenous polysaccharide found throughout human endothelial and neural tissues and is a primary constituent of the extracellular matrix. It has well-characterized properties,25,26 is generally nonadhesive to cells, and inhibits glial cell response.27 The dopamine−hyaluronic acid (DAHA) composite can be electrodeposited onto electronically conducting substrates to form an electroactive polydopamine−hyaluronic acid (p(DAHA)) biopolymer for bioelectronic energy storage. Material Synthesis. Scheme 1 summarizes the carbodiimidebased synthesis of DAHA. NMR analyses indicated that 10− 30% of the carboxyl groups in HA could be functionalized with DA by varying the stoichiometric ratio of the reactants. Figure S1 (Supporting Information) depicts scanning electron microscopy (SEM) images of lyophilized DAHA and an NMR spectrum of a DAHA sample with approximately 30% of the HA carboxyl groups functionalized with dopamine. The assynthesized, lyophilized DAHA was nanofibrous, with individual fiber diameters ranging between ∼250 nm and 1 μm. Electrodeposition. Figure 1 depicts a typical electrodeposition characteristic of DAHA on indium tin oxide (ITO). Two faradaic features were visible in the forward (anodic) sweep at 0.41 and 0.68 V versus Ag/AgCl, attributed to dopamine grafting and preoxidation,28−30 followed by irreversible oxidative polymerization between 0.9 and 1.0 V. The peak electrodeposition current progressively declined after the initial sweep, suggesting that a p(DAHA) film progressively masked the ITO surface. However, the feature in the reverse sweep at 0.04 V, which was attributed to the reduction of dopaminequinone to dopamine,28−30 increased as the electrodeposition progressed, indicating that the deposited material became more electroactive as the deposition process proceeded. Electrochemical quartz crystal microbalance with dissipation (EQCM-D) was used to elucidate the electrodeposition process (Figure 2). A representative EQCM-D profile showed that the frequency ( f) decreased sharply and the dissipation (D) increased after the aqueous DAHA solution (0.5%, w/v) was

Figure 1. Representative profile for electropolmerization of dopamine−hyaluronic acid (DAHA) to form p(DAHA).

Figure 2. (a) Electrochemical quartz crystal microbalance with dissipation (EQCM-D) profile, (b) oscillation of EQCM-D third harmonic in phase with the applied potential during linear sweep voltammetry, (c) cycle-specific mass deposition and charge passed during 40-cycle (80-segment) electrodeposition, and (d) waterswollen gels on ITO substrates after electrodeposition.

added to the QCM, and that the frequency declined and the dissipation further increased during electrodeposition (Figure 2a). Small oscillations in the harmonics were observed in phase with potential changes during the linear voltage sweeps (Figure 2b): the frequency decreased in the anodic sweep, reached a minimum when the electrode potential was 1.0 V, then increased slightly during the reverse sweep back to 0 V. We attributed this to electrostatic attraction between the positively 673

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two smaller waves (−0.80 and −0.68 V) appeared in the anodic sweep and a single wave (−0.85 V) appeared in subsequent cathodic sweeps. The magnitude of the features between −0.6 and −1.0 V increased with the number of activation cycles, but the magnitude of the peak current at −1.2 V diminished with cycle number; however, the area within the feature between −1.0 and −1.2 V increased with cycle number. In contrast, bare ITO was not electroactive between −0.5 and −1.1 V (Figure 3a, dotted black line), and the area of the feature between −1.1 and −1.2 V did not increase with cycle number. Figure S3 illustrates the connection between the anodic and cathodic peaks that appeared during the activation process. The cyclic voltammetry (CV) plots of activated p(DAHA) displayed features corresponding to catechol−quinone interconversion (Figure 3b−d). The magnitude of the electroactive features between −0.5 and −1.0 V increased with the number of activation sweeps (Figure 3c; green, red, blue, and black traces), and activated p(DAHA) displayed stable, long-term electroactivity for 400 cyclic voltammetry cycles (Figure 3c), indicating that p(DAHA) was firmly attached to the electrode surface. Previous studies of dopa-melanin batteries have also noted an activation process.19 However, the need for activation at such low potential suggests H2 gas generation or proton removal was involved. Previous studies have found that p(DA) is impermeable to diverse redox probes;33,34 therefore, the electrode interface may have been blocked by a thin, dense layer of p(DA) prior to activation. We hypothesize that gas bubbles generated during electrochemical activation may have disrupted this blocking layer. This, in turn, could have increased the overall film−electrode interfacial area, enabled electron selfexchange among liberated catechol moieties (i.e., according to Laviron−Andrieux−Saveant theory),35,36 created channels for proton mobility, and facilitated Grotthus proton transport to catechol groups near the electrode via the nonfunctionalized carboxylic acid groups in HA. Catechol−quinone interconversion has been shown to occur via tunneling, even when spacer groups are present,16,30 so more than a single p(DAHA) monolayer may have contributed to the observed electrochemical pseudocapacitance. Figure 3d portrays the response of activated p(DAHA) to different scan rates between 10 and 200 mV s−1. As shown in Figure S3, a linear relationship between peak current (ip) and scan rate (ν) was observed for all levels of activation (20−80 segments), indicating that the electrochemical process was surface-controlled and that different levels of activation did not influence the underlying electrochemistry of the system. Although the electrochemical response correlated strongly with the number of activation cycles, Figure 3e reveals that the observed pseudocapacitance, quantified here as the slope of the ip versus ν relationship, was more influenced by the number of activation segments than by the number of deposition segments. For example, all samples that underwent 80 activation sweeps displayed the same slope for ip versus ν, regardless of whether they had been electrodeposited with 20, 40, or 80 deposition segments; the same phenomenon was observed for p(DAHA) activated with 20 sweeps, and for both 10% and 30% substitutions. This observation suggests that perhaps only a small fraction of the total material deposited on the electrode actually contributed to the observed pseudocapacitance. This observation also illustrates the importance of identifying or developing an appropriate high-surface area substrate for future investigation and application of this material. Table 1 (Supporting Information) displays the

polarized electrode and the unfunctionalized carboxyl groups in HA, which were negatively charged in the pH ∼7.4 physiological PBS buffer (i.e., because the HA carboxylic acid has pKa ∼2.9)25 and could electrostatically physisorb to the electrode during the anodic sweep and subsequently detach in the reverse sweep. However, the observed increase in dissipation during electrosynthesis suggested that the composite film exhibited visoelastic properties, possibly due to the presence of soft (gel) material trapped within the rigid, electrodeposited polydopamine. The mass deposited in the first cycle was approximately an order of magnitude greater that than in subsequent cycles (Figure 2c), but mass deposition declined gently in cycles 2−40 (i.e., sweep segments 3−80). Figure 2d shows water-swollen gels after electrodeposition. The H2O-contact angle of p(DAHA)-coated ITO (28°) was significantly less than that of bare ITO (88°) because of increased surface hydrophilicity from the presence of HA. This result corroborates prior studies of surface-immobilized HA.31,32 Optical profilometry indicated that the dried, electrodeposited material was ∼300 nm thick (Figure S2). Electrochemical Characterization. Figure 3 summarizes the electrochemical properties of electropolymerized DAHA. No

Figure 3. (a) i−V profile for the activation process; (b) number of activation segments and resulting electroactivity; (c) long-term stability of activated p(DAHA); (d) response of activated p(DAHA) to different scan rates; (e) peak current (ip) as a function of scan rate (ν) for p(DAHA) samples electrodeposited with 20, 40, or 80 sweeps and subsequently activated with either 20 (diamonds) or 80 (circles) sweeps; and (f) galvanostatic discharge profiles of electrodeposited p(DAHA).

electroactivity was observed unless the electrodeposited gel was first “activated” by repeatedly sweeping the potential below −1.1 V vs Ag/AgCl. Figure 3a displays a representative i−V characteristic for the activation process. A solvent-like peak was observed below −1.1 V; however, after sweeping below −1.1 V, 674

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The general shape of the X-ray photoelectron spectroscopy (XPS) C 1s envelope for lyophilized DAHA (Figure S5) was similar to that of prior XPS evaluations of HA.40,41 Although previous XPS evaluations of HA identified a single N 1s peak,40 two distinct peaks were identified for lyophilized DAHA. These peaks were attributed to N atoms in DA (402.1 eV, 32%) and glucosamine groups in HA (400.1 eV, 68%), and their observed areas corroborated the level of DA functionalization determined by NMR. The XPS and Raman spectra of the electrodeposited and cycled p(DAHA) bore general similarity to previous XPS studies of solution-deposited polydopamine33,34 and Raman spectroscopic investigations of natural and synthetic melanins.18,19,42 In conclusion, we synthesized an electroactive composite material for bioelectronic energy storage by chemically conjugating two endogenous biomolecules, hyaluronic acid and dopamine. By adopting this approach, we were able to explore the energy-storage properties of polydopamine and incorporate HA as a shield against oxidative stress and nonspecific protein adsorption. Different groups have reported electroconductive hydrogels,21−24,43,44 but we believe this is the first report of an energy-storage material synthesized exclusively with endogenous biomolecules. Although the catechol group of DA is redox-active,16−19 DA autopolymerizes rapidly in physiological solutions to form a highly disordered and electrochemically inactive28,29,33 polydopamine material that is not suitable for energy storage. However, chemical conjugation of DA to HA effectively immobilized DA and prevented autopolymerization. Furthermore, our p(DAHA) was electrochemically active and displayed stable pseudocapacitance for 400 CV cycles under in vitro conditions in physiological (pH 7.4) phosphate-buffered saline solution. EQCM-D analysis indicated that HA was present within the electrodeposited DA, and the ensconced material appeared to play an essential role in the composite’s electroactivity. Our electroactive hydrogel has many potential applications as a bioelectronic interface or energy-storage material, i.e., as a supercapacitor or, when coupled with an Ag/AgCl electrode (e.g., those used in implantable amperometric glucose sensors), a potentially implantable battery with an operating voltage ∼0.85 V. Redox hydrogels used in physiological systems to connect enzymes with amperometric biosensor electrodes typically contain ferrocene or osmium−bipyridine complexes whose redox potentials are poised ∼200 mV positive of an implantable Ag/AgCl reference electrode.22−24,36,43 Although this strategy minimizes oxidative interference from other biomolecules,43 it also renders the operating voltages too small for practical use in implantable energy-storage materials. In contrast, redox hydrogels based on conducting polymers such as polypyrrole polythiophene and polyaniline operate at higher voltages but exhibit capacitance and capacity lower than that of activated p(DAHA) reported in this study.44 In addition, we expect that the ease of synthesis of DAHA and the endogenous origin of its components will offer an intrinsic advantage for utilization in biological systems for a multitude of applications (e.g., implantable biosensors, neuronal prostheses, electrostimulated therapeutics, etc.).21,45 However, further investigation is necessary to verify the biocompatibility of p(DAHA) and confirm its functionality as an implantable energy-storage material.

capacitance of p(DAHA) as a function of DA substitution (10% and 30%) and number of activation sweeps (20, 40, 60, 80 segments). Given the result described in Figure 3e, the capacitance as a function of the number of deposition segments is not presented. In absolute terms, the pseudocapacitance of the electrodeposited material increased ∼0.2 mF per 20 activation segments for both 10%- and 30%-substituted DAHA. Figure S4 depicts the cycle-by-cycle variation of charge passed during electrodeposition. Although the pseudocapacitance of p(DAHA) generated from DAHA with 30% DA substitution was ∼30% higher than that of p(DAHA) from 10% DAHA, the gravimetric pseudocapacitance and energy density of 10% DAHA were larger because less mass was deposited during electrodeposition of 10% DAHA. This result suggests that the electrodeposition process for the 10% DAHA may have created more uniform p(DAHA) surface layers and/or that the layers were more efficiently activated after synthesis and indicates that further optimization of the electrosynthesis is possible. Although our pseudocapacitance estimates were high compared to conventional, carbon-based supercapacitors,37 they are similar to those reported for thin-film supercapacitors of approximately the same thickness (0.5 μm) containing oxidized lignin, a biopolymer with electroactive quinone moieties.38 However, the capacitance of oxidized lignin was observed to decline significantly in thicker films, a commonly observed phenomenon in capacitive materials. The galvanostatic discharge profiles for p(DAHA) were flat (Figure 3f) and exhibited a stable operational cell potential near −0.85 V and a high discharge capacity up to ∼130 mAh g−1 at current densities ∼10−15 A g−1, which compares well with previous studies of melanin-based active materials.18,19 Surface Analysis. Figure 4 contains SEM images of the electrodeposited and cycled p(DAHA). Samples were imaged

Figure 4. SEM images of (a−c) p(DAHA) after electrodeposition, CV testing, and critical-point drying in CO2; (d) bare ITO.

after drying at the CO2 critical point. Small spheres of dried HA were visible across the electrode surface where p(DAHA) had been electrodeposited (Figure 4a) and were found to overlay the electrodeposited p(DA) granules (Figure 4b). The exposed, electrodeposited product displayed a dense concentration of nanoscale granules 20−100 nm in diameter (Figures 4c), consistent with previous descriptions of dopamine−melanin,39 auto-oxidized polydopamine,33 and chemically/electrochemically synthesized dopa-derived melanin.18,19 These features were not observed on bare ITO slides (Figure 4d). 675

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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.6b00334. Experimental methods section; capacitance and energy density of p(DAHA) (Table 1); SEM and NMR of lyophilized DAHA (Figure S1); optical profilometry of electrodeposited p(DAHA) (Figure S2); electrochemical analysis of activated p(DAHA) (Figure S3); charge passed during electrodeposition (Figure S4); XPS analyses (Figure S5); schematic of assemblies used for electrodeposition and electrochemical analysis (Figure S6) (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Science Foundation Nanosystems Engineering Research Center (NERC) for Nanomanufacturing Systems for Mobile Computing and Mobile Energy Technologies (NASCENT) through Award Number EEC-1160494. The authors thank Dwight Romanovicz (Microscopy and Imaging Facility, Institute for Cellular and Molecular Biology) for invaluable assistance with critical point drying and SEM imaging; Richard Piner (Texas Materials Institute) for assistance with the micro-Raman and optical profilometry measurements; members of the Suggs’ research group for graciously storing the lyophilized material at −20° C; and Dr. Longjun Li, Dr. Henghui Xu, Dr. Netzahualcóyotl Arroyo Currás, Dr. Matthew Dixon (Biolin Scientific), and Professor Adam Heller for their invaluable discussions.

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