Light Induced H2 Evolution from a Biophotocathode Based on

Article pubs.acs.org/JPCB

Light Induced H2 Evolution from a Biophotocathode Based on Photosystem 1 − Pt Nanoparticles Complexes Integrated in Solvated Redox Polymers Films Fangyuan Zhao,† Felipe Conzuelo,† Volker Hartmann,‡ Huaiguang Li,§ Marc M. Nowaczyk,‡ Nicolas Plumeré,§ Matthias Rögner,‡ and Wolfgang Schuhmann*,† †

Analytical ChemistryCenter for Electrochemical Sciences (CES), Ruhr-Universität Bochum, Universitätsstrasse 150, 44780 Bochum, Germany ‡ Plant Biochemistry, Ruhr-Universität Bochum, Universitätsstrasse 150, 44780 Bochum, Germany § Center for Electrochemical SciencesMolecular Nanostructures, Ruhr-Universität Bochum, Universitätsstrasse 150, 44780 Bochum, Germany S Supporting Information *

ABSTRACT: We report on a biophotocathode based on photosystem 1 (PS1)−Pt nanoparticle complexes integrated in a redox hydrogel for photoelectrocatalytic H2 evolution at low overpotential. A poly(vinyl)imidazole Os(bispyridine)2Cl polymer serves as conducting matrix to shuttle the electrons from the electrode to the PS1-Pt complexes embedded within the hydrogel. Light induced charge separation at the PS1-Pt complexes results in the generation of photocurrents (4.8 ± 0.4 μA cm−2) when the biophotocathodes are exposed to anaerobic buffer solutions. Under these conditions, the protons are the sole possible electron acceptors, suggesting that the photocurrent generation is associated with H2 evolution. Direct evidence for the latter process is provided by monitoring the H2 production with a Pt microelectrode in scanning electrochemical microscopy configuration over the redox hydrogel film containing the PS1-Pt complexes under illumination.

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INTRODUCTION The implementation of photosynthetic proteins such as photosystem 1 (PS1) for solar energy harvesting was demonstrated for current generation1−6 and for chemical fuel production. 7 Most strategies rely on the proteins in solution8−10 or in contact with electrodes.6,11,12 We proposed the use of redox hydrogels for electronic contacting of high loading of photosynthetic protein complexes.13,14 Redox polymers have been intensively used as electron conducting matrices for immobilization and contact of a variety of redox enzymes in biosensors15−18 and biofuel cells.19−22 Variations in the coordination sphere of the redox relays,23,24 the hydrophilic−hydrophobic properties of the backbones,25,26 and the mobility of the polymer-bound electron relays27,28 allow tuning the kinetics and thermodynamics of the electron transfer. We found that Os-complexes and redox-dye-modified polymers are especially well-suited as immobilization matrix for photosynthetic proteins.13,14,25,26,29 In particular, high photocurrent generation of up to 0.3 mA cm−2 was achieved with a PS1based photocathode by adjusting the solvation state of the hydrogel based on an Os-complex-modified poly(vinyl)imidazole polymer.25 In our previous reports, we demonstrated light induced electrical energy generation in a Z-scheme mimic29,30 in which the photoexcited electrons exiting PS1 from the FB site were quenched by O2 at the photocathode.25 Of greater interest © XXXX American Chemical Society

would be the recovery of this high-energy electron from PS1 in the form of chemical fuels. For instance the coupling of a catalyst for H2 evolution to isolated PS1 protein complexes was demonstrated in homogeneous conditions. A variety of catalysts31 such as metallic nanoparticles,8−10 molecular transition metal complexes,32 and enzymes such as hydrogenases33−35 were tethered in close proximity to the FB site of PS1 to induce H2 evolution. Nevertheless, all these systems rely on an artificial sacrificial electron donor in solution. Here, we demonstrated that PS1-Pt biohybrid complexes can be in contact with a photocathode via a redox hydrogel whereby the electrons for hydrogen evolution are provided by the electrode at low overpotential and hence bypass the need for a sacrificial electron donor in solution (Scheme 1).

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RESULTS AND DISCUSSION For hydrogel formation and immobilization of the PS1-Pt complexes on electrodes, we used the previously reported Oscomplex-modified poly(vinyl)imidazole polymer designed for cathodic photocurrent generation. The redox potential of the Special Issue: Wolfgang Lubitz Festschrift Received: April 11, 2015 Revised: May 29, 2015

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DOI: 10.1021/acs.jpcb.5b03511 J. Phys. Chem. B XXXX, XXX, XXX−XXX

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The Journal of Physical Chemistry B Scheme 1. Schematic Representation of PS1-Pt Complexes Embedded within the Os-Complex-Modified Redox Polymer Matrixa

Figure 1. Cyclic voltammograms for the evaluation of Pt loading in the absence of PS1-Pt complexes obtained at gold electrodes modified with the redox hydrogel in the presence of different amounts of Pt nanoparticles under dark conditions at 5.0 mV s−1 in Ar-saturated 50 mM citrate buffer solution, pH 4.0. The number of moles of Pt nanoparticle used during hydrogel formation is indicated in the figure.

a

Arrows depict the electron transfer pathway by a hopping mechanism. Upon absorption of photons, the charge-separated state P700+−FB− transfers an electron from PS1 to the Pt nanoparticle surface which enables subsequent H2 production. The electrode surface wired through the redox polymer to PS1 acts as electron donor for the P700+ site.

680 nm immediately after film preparation and after washing off the unbound polymer and protein (Supporting Information Figure S3). The value for ΓPS1‑Pt is (271 ± 16) pmol cm−2 before washing and is (238 ± 7) pmol cm−2 after washing of the hydrogel with buffer. Hence, only 12% of PS1 is lost in the washing step. In comparison, in absence of Pt, 75% of the native PS1 used for film preparation is lost in the washing process,25 confirming the role of the Pt particles in film stability. The activity of PS1 in the various hydrogel films was first tested by measuring the photocurrents in the presence of methyl viologen (MV2+) as electron mediator and oxygen as the final electron acceptor (Figure 2B,D). The largest photocurrents were obtained with the native PS1 immobilized in the hydrogel while films modified with Pt show only negligible photocurrents. The absence of photocurrent from inactivated PS1-Pt complex (iPS1-Pt)-modified electrodes under illumination demonstrates that the thermal treatment fully denatures the PS1-Pt complexes. The photocurrents obtained for the native PS1-Pt complex with O2 as final electron acceptor are about 25% of those obtained for native PS1 only, indicating that the Pt nanoparticle either hinder electron transfer from FB to the viologen or induce partial deactivation of the protein. Nevertheless, the photocurrents remain 49-fold larger than that measured with deactivated PS1Pt. The electrodes prepared with native PS1 and Pt nanoparticles mixed briefly before deposition showing photocurrents values lying between that of PS1 only and those of PS1-Pt complexes indicating that the complex assembly may also take place, at least partially, within the solution for hydrogel formation. In the next step we tested the generation of photocurrent with the modified electrodes under anaerobic conditions and in the absence of any freely diffusing electron mediator (Figure 2C,E). Hence, protons are the only possible electron acceptor in solutions. Under these conditions, the hydrogels containing native PS1 only now display the lowest photocurrents demonstrating that the reduced FB site cannot induce H2 evolution from anaerobic aqueous solutions at pH 4. The electrode modified with the hydrogel containing the PS1-Pt complex displays the highest photocurrent (Figure 2C,E) indicating that the electrons from FB are transferred to the Pt nanoparticle to catalyze H2 evolution. When PS1 and the Pt nanoparticles are mixed on the electrode surface briefly before deposition, the photocurrents are 33% lower, confirming that the PS1-Pt complex can form in situ as well, however, with a

Os-complex is adjusted for fast electron transfer at low overpotential from the electrode to the P700 redox center of PS1. The polymer backbone based on pH responsive imidazole groups13 is designed to tune the solvation state of the hydrogel for optimum PS1 activity and electron transfer.25 Pt nanoparticles (2.7 nm in diameter, Supporting Information Figure S1) of low polydispersity capped with mercaptosuccinic acid (MSA) were prepared by a single-phase method in water.36 The noncovalent PS1-Pt complexes were obtained from electrostatically directed assembly between the native photosystems and the negatively charged Pt nanoparticles.8 The absorbance spectra of the PS1-Pt complexes show the expected bands at 439 and 678 nm corresponding to chlorophyll and are not distinguishable from unmodified PS1 (Supporting Information Figure S2) indicating no sign of decoupling of PS1 and chlorophyll. The redox hydrogel films on Au electrodes were formed with (i) the native PS1-Pt complex biohybrid, (ii) the denatured PS1-Pt complex, (iii) the native PS1 only, (iv) the Pt particles only, and (v) the native PS1 and Pt nanoparticles mixed only shortly before deposition. The denatured PS1-Pt complex was produced by treating the native PS1-Pt complexes in a water bath at 100 °C for 30 min.9 It is interesting to notice that the properties of the redox hydrogels strongly depend on the presence of Pt nanoparticles. The loading in Os-complexes increases with the amount of Pt nanoparticle used for film preparation (Figure 1). This indicates that the Pt nanoparticles contribute to film stabilization possibly via coordination of free imidazole to the Pt nanoparticle or via electrostatic interactions between the negatively charged mercaptosuccinic acid capped nanoparticles and the positively charged Os-complex-modified polymer. The surface concentration in Os-complexes (ΓOs) in the redox hydrogel film was extracted from the charge resulting from complete OsII/III interconversion during cyclic voltammetry. When Pt nanoparticles are used either in their isolated form or complexed to PS1, ΓOs = (6.9 ± 1.4) nmol cm−2 while the films free of Pt have a surface coverage in Os-complexes of only 0.43 nmol cm−2 (Figures 1 and 2A). The surface concentration in PS1-Pt complexes (ΓPS1‑Pt) compared to the one of the native PS1 in the redox hydrogels show a similar trend. ΓPS1‑Pt was determined by measuring the absorbance of chlorophyll at B


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The Journal of Physical Chemistry B

Figure 2. Gold electrodes modified with a film of an Os-complex-based redox polymer matrix containing PS1, iPS1-Pt (denatured PS1-Pt complex), Pt (Pt nanoparticles only), PS1 + Pt (PS1 and Pt nanoparticles mixed shortly before deposition at the electrode surface), or PS1-Pt (PS1-Pt complex biohybrid). (A) Cyclic voltammograms of the modified gold electrodes obtained under dark conditions at 1.0 mV s−1 in Ar-saturated 50 mM citrate buffer solution, pH 4.0. (B) Photocurrents obtained for the modified gold electrodes in air-saturated buffer, in the presence of 2 mM MV2+. (C) Photocurrents obtained for the modified gold electrodes in Ar-saturated buffer only. (D) Mean photocurrent densities recorded at the modified electrodes as in part B after the first and second irradiation. Error bars estimated as the standard deviation of the measurements (n = 3). (E) Mean photocurrent densities recorded at the modified electrodes as in part C after the first and second irradiation. Error bars estimated as the standard deviation of the measurements (n = 3). Irradiation at 152 mW cm−2 with visible light using a 600 nm high pass filter was turned on for 20 s intervals as indicated by the yellow shaded regions in the graph. The applied potential was 0.0 mV vs Ag/AgCl/3 M KCl.

lower efficiency. The control experiments with Pt only, or with denatured PS1-Pt complexes (iPS1-Pt), showed photocurrents that are, respectively, about 20% and 15% of those obtained from the native PS1-Pt complexes (Figure 2E). This confirms that the photocurrent related with H2 production is only dependent on the presence of the functional photosystem 1. Since the presence of traces of oxygen cannot be excluded, a control experiment using an enzyme-catalyzed system consisting of glucose oxidase, glucose, and catalase for O2 removal37 was performed in order to demonstrate that O2 is not the final electron acceptor. As shown in Figure 3, under the strict absence of oxygen in the solution, the electrode modified with a hydrogel containing only native PS1 displays negligible photocurrents. Conversely, the hydrogel containing the PS1Pt complex displays the highest photocurrent, confirming H2 evolution. The intensity of the photocurrent obtained from the PS1-Pt complex increases with decreasing pH value (Supporting Information Figure S4). This observation is consistent with an increased electron transfer rate within the hydrogel film. The cyclic voltammograms of the redox hydrogel recorded in the

Figure 3. Photocurrents obtained for the gold electrodes modified with a film of an Os-complex-based redox polymer matrix containing PS1 or the PS1-Pt complex biohybrid, in Ar-saturated buffer and in the presence of glucose oxidase, glucose, and catalase for O2 removal. Irradiation at 152 mW cm−2 with visible light using a 600 nm high pass filter was turned on during different time intervals as indicated by the yellow shaded regions in the graph. The applied potential was 0.0 mV vs Ag/AgCl/3 M KCl.

dark for increasing pH values show decreasing peak currents and peak shapes shifting from surface confined to diffusion controlled characteristics (Supporting Information Figure S5). At the lower pH values (pH < 5), the polyvinylimidazole backbone in the film is mostly protonated and solvated. Under these conditions, the mobilities of the tethered Os-complexes C


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Figure 4. SECM images of a Pt-PS1/Os-complex-based redox hydrogel partial spot on a gold wafer, showing the current recorded at the tip: (A) under dark conditions, (B) under illumination of the sample. (C) The depicted tip current corresponds to the difference between the current recorded at localized illumination of the sample and under dark conditions. The contrast between H2 photogenerated at Pt-PS1 and absence of H2 evolution at the unmodified gold wafer is inferred from the oxidative currents recorded at the tip microelectrode. Esample = 0.0 mV, Etip = 150 mV (both vs Ag/AgCl/3 M KCl). Electrolyte solution: Ar-saturated 50 mM citrate buffer, pH 4.0. SECM tip: 25 μm Ø Pt disk.

splitting catalyst in a second cell compartment29,30 and hence provide electrons without sacrificial electron donor while bypassing potential interference from O2 with the H2 evolving photocatalyst.

serving as electron relays and hence the kinetics of the electron hopping are highest.25 Moreover, the increased driving force for H2 evolution at the Pt particle with decreasing pH values may also account for the higher photocurrents. The photocurrent under anaerobic conditions obtained from the PS1-Pt−Os-complex-modified redox hydrogel exposed to electrolyte only indicates that H2 evolves under illumination. Direct evidence for hydrogen evolution at the PS1-Pt biohybrids was achieved by means of scanning electrochemical microscopy (SECM). This high-resolution technique was used to sense the photoelectrochemically evolved hydrogen. A previous study reported on preliminary SECM experiments for the analysis of platinum clusters deposited on PS1 multilayer films.38 Pt was photoreduced onto the protein from a Pt salt solution using long irradiation times (2 h). The study was intended for the detection of deposited Pt-clusters through the detection of catalytically generated H2 in acidic solution. However, the detection of H2 evolution induced by photoexcited PS1 was not demonstrated. In the present work, to provide for the first time direct evidence for H2 production from the PS1-Pt complexes in the redox hydrogel, we performed the SECM analysis under dark and illumination of the sample. Light induced H2 generation at the modified substrate was detected at a closely positioned Pt tip microelectrode by H2 oxidation. Under dark conditions no significant oxidative currents (Figure 4A) were recorded at the SECM tip, while under illumination the recorded response at the SECM tip on top of the modified gold substrate exhibited currents for H2 oxidation at the Pt microelectrode surface (Figure 4B). The difference between the current recorded at the tip under illumination and that under dark conditions is depicted in Figure 4C, showing higher oxidative currents at the region of the gold substrate modified with PS1-Pt and a clear contrast in comparison with the unmodified substrate. A control experiment was performed recording an SECM scan on a gold wafer modified with a mixture of the redox polymer and Pt nanoparticles, i.e., in the absence of PS1-Pt biohybrid. No significant oxidative current was recorded at the tip, indicating the absence of evolved H2 (Supporting Information Figure S6). The successful demonstration of the integration of PS1-Pt biohybrid complexes in a redox hydrogel for light induced H2 evolution opens new possibilities for the immobilization in high loading and electronic contacting of various other (bio)photocatalysts to photocathodes. The main advantage of this concept lies in the possibility to physically separate the photocathode from a photoanode modified with a water

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EXPERIMENTAL SECTION

PS1 was prepared as described previously.14 Poly(vinyl) imidazole polymers modified with [Os(bpy)2Cl]+ were synthesized according to ref 13. Preparation of Pt Nanoparticles.36 Aqueous solutions of chloroplatinic acid hexahydrate (H2PtCl6, 10 mL, 3.38 mM) and mercaptosuccinic acid (MSA, 1 mL, 23.7 mM) were vigorously mixed under stirring and argon bubbling for 10 min. The molar ratio between MSA and H2PtCl6, S/Pt, equals 0.7. Then, freshly prepared aqueous NaBH4 solution (5 mL, 110 mM) was added to the mixture with continuous argon bubbling and under vigorous stirring for another 30 min. The color of solution changed from yellow to light brown, and then gradually to deep brown due to the formation of Pt nanoparticles. Dynamic light scattering experiments (measured with a Malvern Zetasizer) yield a mean size distribution by number for the Pt nanoparticles of 2.7 nm. The PS1-Pt complexes were assembled according to ref 8. The denatured PS1-Pt complexes (iPS1-Pt) were obtained by treating PS1-Pt in buffer at 100 °C for 30 min. Electrode Modification. Gold electrodes (2 mm diameter) were polished on polishing cloth using decreasing sizes of diamond suspension (Leco) and then electrochemically cleaned by cyclic voltammetry (20 scans in 0.5 M H2SO4 at 100 mV s−1) prior to modification. A droplet (3 μL) of a mixture of the polymer (5 μg μL−1), poly(ethylene glycol) diglycidyl ether (0.02 μg μL−1), and PS1-Pt (1 μg PS1 μL−1) or the control sample was deposited on the electrode surface. The modified electrodes were incubated in the dark at 4 °C for 24 h. Afterward, they were immersed for 30 min in Tris-HCl buffer solution (50 mM, pH 9) containing KCl (100 mM), MgCl2 (10 mM), and CaCl2 (10 mM) to induce polymer collapse. Electrochemical and Photoelectrochemical Measurements. All electrochemical measurements were performed in a light dense photoelectrochemical cell using a PalmSensII (PalmSens) as potentiostat as described previously.26 A threeelectrode system was used, with an integrated Pt-wire counter electrode, a Ag/AgCl/3 M KCl reference electrode, and the modified gold electrode as working electrode. All potentials are referred to the Ag/AgCl/3 M KCl reference electrode. D


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The Journal of Physical Chemistry B Notes

Scanning Electrochemical Microscopy. SECM measurements were performed in a four-electrode configuration using a Pt-microelectrode tip fabricated as described elsewhere39 using 25 μm Ø Pt wire (Goodfellow), a Pt cylindrical mesh as counter electrode, a homemade double junction reference electrode (Ag/AgCl/3 M KCl), and a modified gold wafer as sample. The SECM setup has been described previously.40 Main components are step-motor driven micrometer screws (Owis) for positioning of the tip electrode in x−y−z directions, a bipotentiostat (PGU-BI 100, IPS-Jaissle), and in-house written control software. Local illumination of the sample during the scan was performed with a LC8 type 03 lamp (visible light) with an integrated shutter coupled to the top glass wall of the tip microelectrode by means of a light guide made of synthetic silica (both Hamamatsu Photonics). The samples for SECM measurements were prepared on a gold wafer. Briefly, Au-coated Si wafers were prepared in a metal vaporization setup (Leybold Univex 300) on Si(100) wafers (Wacker) by vapor deposition of a 50 Å titanium layer and a 1000 Å gold layer. A spot of PS1-Pt/redox polymer mixture was drop casted on the surface of the Au wafer and incubated overnight at 4 °C before the measurement. The surface scan was recorded at a constant tip-to-sample separation within the feedback response of the SECM tip. Measurements were carried out in Ar-saturated citrate buffer 50 mM, pH 4.0. The sample potential was held at 0.0 V while the tip potential was held at 150 mV (both vs Ag/AgCl/3 M KCl). The sample was scanned under dark and under illumination conditions. UV−Vis Spectroscopy. PS1-Pt redox hydrogel films were prepared on a quartz surface under the same conditions as those for electrode modification. The UV−vis spectra of the films in the dried state were collected in air at room temperature using a Shimadzu UV-2450 spectrophotometer according to ref 25. The light beam cross-section was a square of 4 × 4 mm2. The PS1-modified film was restricted to a circular area with a diameter of 2 mm and was positioned fully in the light beam to ensure measurement of the absorbance from the complete PS1-modified film. A calibration curve was prepared from PS1 solutions of various concentrations dried on the quartz surface as described above but in the absence of polymer and cross-linker. The calibration based on dried PS1Pt yielded a molar extinction coefficient of (26.9 ± 7.4) × 103 M−1 s−1 at 680 nm (for comparison the value for PS1 in solution is 57 × 103 M−1 s−141) which was used for quantification of the PS1 surface coverage in the hydrogel films.

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The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the Cluster of Excellence RESOLV (EXC 1069) funded by the Deutsche Forschungsgemeinschaft (DFG), by the COST Action TD1102 PHOTOTECH, and the Deutsch-Israelische Projektkooperation (DIP) in the framework of the project “Nanoengineered Optoelectronics with Biomaterials and Bioinspired Assemblies”. F.Z. and H.L. are grateful for the support by the China Scholarship Council (CSC).

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ASSOCIATED CONTENT

S Supporting Information *

Additional experimental data and figures as noted in text. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.5b03511.

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REFERENCES

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