Light as Trigger for Biocatalysis: Photonic Wiring of Flavin Adenine

Research Article Cite This: ACS Catal. 2018, 8, 5212−5220

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Light as Trigger for Biocatalysis: Photonic Wiring of Flavin Adenine Dinucleotide-Dependent Glucose Dehydrogenase to Quantum DotSensitized Inverse Opal TiO2 Architectures via Redox Polymers Marc Riedel,*,† Wolfgang J. Parak,‡ Adrian Ruff,§ Wolfgang Schuhmann,§ and Fred Lisdat*,† †

Biosystems Technology, Institute for Applied Life Sciences, Technical University Wildau, Hochschulring 1, D-15745 Wildau, Germany ‡ Fachbereich Physik und Chemie, CHyN, University Hamburg, Luruper Chaussee 149, D-22607 Hamburg, Germany § Analytical ChemistryCenter for Electrochemical Sciences (CES), Faculty of Chemistry and Biochemistry, Ruhr-Universität Bochum, Universitätsstr. 150, D-44780 Bochum, Germany S Supporting Information *

ABSTRACT: The functional coupling of photoactive nanostructures with enzymes creates a strategy for the design of lighttriggered biocatalysts. This study highlights the efficient wiring of flavin adenine dinucleotide (FAD)-dependent glucose dehydrogenase (FAD-GDH) to PbS quantum dot (QD)-sensitized inverse opal TiO2 electrodes (IO-TiO2) by means of an Oscomplex-containing redox polymer for the light-driven glucose oxidation. For the construction of IO-TiO2 scaffolds, a template approach has been developed, enabling the tunability of the surface area and a high loading capacity for the integration of QDs, redox polymer, and enzyme. The biohybrid signal chain can be switched on with light, generating charge carriers within the QDs, triggering a multistep electron-transfer cascade from the enzyme toward the redox polymer via the QDs and finally to the IO-TiO2 electrode. The resulting anodic photocurrent can be modulated by the potential, the excitation intensity, and the glucose concentration, providing a new degree of freedom for the control of biocatalyic reactions at electrode interfaces. Maximum photocurrents of 207 μA cm−2 have been achieved in the presence of glucose, and a first gain of electrons from the biocatalytic reaction is found at −540 mV vs Ag/AgCl, 1 M KCl, which lowers the working potential by >500 mV as compared to light-insensitive electrodes. The biohybrid system combines the advantages of a high surface area of IO films, an efficient charge-carrier generation and separation at the QDs/TiO2 interface, and an efficient wiring of FAD-GDH to the QDs via a redox polymer, resulting in photo(bio)anodes of high performance for sensing and power supply. KEYWORDS: photobioelectrochemical fuel cells, biocatalysis, photoelectrochemical sensor, quantum dots, enzymes, osmium polymer

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INTRODUCTION Mimicking photosynthetic proteins by combination of lightinsensitive enzymes with artificial light-harvesting entities in a functional biohybrid system has gained great interest in the past decade.1−4 Such approaches combine both biocatalytic activity and photophysical properties in one integrated system with potential applications for sensing,5,6 light-to-current,3,7−10 or light-to-chemical conversion.1,11,12 Introducing light-sensitivity offers the possibility to switch on/off enzymatic reactions and thus to manipulate electron-transfer reactions at electrode interfaces but also can be useful for bioenergetics. Light triggers the generation of electron−hole pairs within the light-sensitive entity and, thus, allows electron-transfer reactions from the enzyme toward the light-sensitive element to the electrode (anodic direction) or vice versa (cathodic direction). Light as trigger provides an additional tool to control electron-transfer processes at electrodes, extending the © 2018 American Chemical Society

application range of electrochemical-detection methods. Because the photoelectrochemical cell (PEC) signal chain is only switched on at the illuminated area, also multiplex analysis becomes feasible if different biocatalysts are immobilized spatially separated from each other on a PEC electrode and readout with a spatial focused light beam.13 In addition to using light as a reaction trigger, the energy gained during illumination can also improve the performance of biocatalytic electrodes in terms of the onset potential of the substrate turnover.14,15 Besides nanomaterials such as dyes,2,16,17 gold nanoclusters,18 and polymers15 or biomolecules such as photosynthetic proteins (e.g., photosystem I (PSI)),3,14,19,20 particularly quantum dots (QDs),4,21 have been used for photonic Received: March 9, 2018 Revised: April 26, 2018 Published: April 27, 2018 5212

DOI: 10.1021/acscatal.8b00951 ACS Catal. 2018, 8, 5212−5220

Research Article

ACS Catalysis wiring of light-insensitive enzymes. Therefore, first the lightsensitive entity needs to be attached to the electrode, which is often realized via electrostatic attraction, chemisorption, or covalent binding.5 However, QD-based approaches are often limited by particle aggregation22,23 and the stabilizing ligands,24 influencing not only particle assembly but also the interaction with enzymes. An alternative way can be seen in the synthesis of QDs directly on top of the electrode material via successive ionic layer adsorption and reaction (SILAR).25−27 This easy and low-cost procedure allows for control of the QD growth by means of the number of SILAR cycles and passes over the need for surface ligands. The design of efficient photoreducing or -oxidizing systems are based on a biocatalyst electronically linked to a lightharvesting entity. First approaches have exploited the activity of the light-active element itself for the detection of enzymatic cosubstrates or products, giving information about the enzyme activity and analyte concentration.28−31 Until now, only a few examples have demonstrated the direct or mediated electron transfer between enzymes and the light-active entities in a lightdirected operation.2−4,15,16,21,32 However, most of these approaches are characterized by some drawbacks: e.g., limited wavelength excitation range, the need for freely diffusing mediators, or a low efficiency for the light-to-current conversion. The efficiency is often limited by an insufficient charge-carrier separation as a result of recombination processes at the electrode/light-active entity interface. In nature, the electron/hole separation has been optimized by combination with a cascade of electron-transfer steps, resulting in higher quantum efficiencies. Such pathways can be simulated in artificial systems by a combination of different semiconducting materials. Here, a large-band-gap semiconductor (e.g., TiO2) with a conduction band acting as an electron trap for excited electrons of a second visible-light-sensitive semiconducting material (e.g., QDs, dyes, or polymers) has proven to be promising for solar cell and photocatalytic applications.33−35 Another optimization parameter arises from the electronic linkage of the light-sensitive entity to the biocatalyst. Even if the direct electron transfer with biocatalysts is a desired task, such electrodes often lack in efficiency due to inhomogeneous orientation of the enzyme and the restriction of enzyme immobilization to a monolayer. One strategy to overcome such limitations can be the entrapment of the enzyme within a redox-active polymer.36−38 The biocatalysts are efficiently wired within the polymer matrix independent of the orientation. A further efficiency boost can be expected if enzyme/redox polymer matrices are integrated into 3D electrode architectures.9,10 Here, we report on a novel high-performance glucose oxidizing photoanode, which combines the advantages of efficient charge-carrier separation within a multicomponent semiconductor electrode, and the efficient wiring of the biocatalyst via a redox polymer and QDs in a functional system. Therefore, a new strategy for the construction of hierarchical inverse opal TiO 2 architectures has been investigated. Visible-light sensitivity has been introduced by the growth of PbS QDs via a SILAR approach directly on top of the IO-TiO2 electrodes. Finally, FAD-GDH has been integrated within the architectures by means of a redox polymer, resulting in an efficient linkage of the biocatalyst to the QDs. The IOTiO2|PbS|POs|FAD-GDH (POs = osmium polymer) architectures demonstrate the potential of light-driven electron-transfer

chains. Here the electrons are transferred via several steps from the enzyme via the redox polymer toward the QDs and finally to the IO-TiO2 electrode, giving access to pronounced glucosedependent anodic photocurrents.

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RESULTS AND DISCUSSION The artificial signal chain is depicted in Scheme 1 consisting of three components: (1) a light-active component (TiO2 Scheme 1. Schematic Illustration of (A) the Electron Transfer Steps within the Light-Driven Signal Cascade and (B) the Energetic Level E of TiO2, PbS QDs, OsmiumContaining Redox Polymer (POs), and FAD-Dependent Glucose Dehydrogenase (FAD-GDH)a

a

For FAD-GDH a redox potential of free FAD has been assumed, because the redox potential of the enzyme is not yet known. VB = valence band, CB = conduction band.

electrode and PbS QDs), (2) an electron-shuttling component between the QDs and enzyme (Os-complex modified polymer, POs), and (3) a biocatalytic component (FAD-dependent glucose dehydrogenase, FAD-GDH). Under illumination with visible light, the signal chain is switched on and electrons from the enzymatic glucose conversion are transferred from the enzyme toward POs to the QDs and finally to the TiO2 electrode with a concomitant generation of an anodic photocurrent. The TiO2/QD interface is of importance for the light-directed functionality of the whole biohybrid system, because electron−hole pairs are first generated within the QDs and are subsequently efficiently separated at the TiO2 electrode via injection of excited electrons from the QD into the TiO2 conduction band.39 If the light source is switched off, no free charge carriers are available within the semiconductor (QD) and the signal chain is interrupted with no current flow. In the dark the redox polymer remains completely reduced due to the lack of light-directed oxidation; thus, the enzyme can no longer transfer electrons and is switched off. Therefore, the whole IOTiO2|PbS|POs|FAD-GDH architecture can be controlled with light as trigger for glucose oxidation. 5213


Research Article

ACS Catalysis Synthesis and Characterization of the Light-Sensitive Entity. The light-sensitive entity consisting of TiO2 and PbS QDs has been successively synthesized on a transparent fluorine-doped tin oxide (FTO) electrode. First, we have established a new procedure for the construction of TiO2 electrodes with a macroporous inverse opal structure. TiO2 has been chosen due to its favorable energetic states, which promote the charge-carrier separation within the QDs and, thus, increase the light-to-current efficiency.40 The application of a macroporous structure is assumed to be beneficial for the stable integration of a large amount of polymer and enzyme. The IO-TiO2 electrodes have been prepared using a template approach: by spin-coating a mixture of latex beads and titanium tetraisopropoxide (TTIP) onto a cleaned FTO slide, followed by a sintering step, an inverse opal TiO2 scaffold is formed (see details in Methods). First, the morphology of the final IO-TiO2 electrodes has been investigated with scanning electron microscopy. As illustrated in Figure 1A, the procedure results in an inverse

between 2 and 8 layers, the height per layer is found to increase linearly (1.2 ± 0.1 μm per layer) without indication of a limitation (Supporting Information, Figure S1D). Control experiments of electrodes prepared without latex beads show that both TTIP and latex beads are needed for the successful construction of the IO-TiO2 film (Figure S1). The optical features of the IO-TiO2 electrodes have been investigated with UV/vis absorption spectroscopy. The IOTiO2 films are of high transparency, which decreases linearly with increasing number of layers (Figures S2 and S3). Interestingly, the transmittance of the IO film is found to be noticeably higher than that of the planar TiO2 film (prepared without LB, Figure S4), which can be attributed to the absence of dense agglomerates within the IO-TiO2 structure. In comparison to IO films prepared in a template approach with TiO2 nanoparticles, the structures produced in this work show a higher transparency.15,41,42 This significantly expands the field of applications of our IO films. Also the fast construction and easy scalability of the electrodes is a clear advantage compared to other approaches.43−45 To introduce sensitivity for the visible spectral range, PbS QDs have been selected. The QDs have been synthesized directly on top of the IO-TiO2 film with a SILAR approach as reported before.25,27 For this, the electrode is immersed alternately in Pb2+ and S2− containing solutions, resulting in a growth of PbS QDs with increasing number of cycles (a cycle is defined as one reaction with Pb2+ and S2−, respectively). The successful synthesis of the QDs within the IO-TiO2 electrode can be confirmed by a coloration of the structure from white to brown. The UV/vis absorption spectra of a 4-layered IO-TiO2 electrode exhibit an increase of the absorbance over the whole visible wavelength range with increasing number of cycles from 2 up to 8 cycles (Figure S5). HR-TEM measurements show that the QDs reach a diameter between 3 and 4 nm after 4 cycles (Figure 1B), which is in good agreement with a previous report.27 According to this the band gap is in the range of 1.92−1.47 eV.46 Consequently, the energy gained during illumination is high enough to inject excited electrons into the conduction band of TiO233,39 and, thus, to provide visible light sensitivity for the light-driven signal chain. Next the functionality of IO-TiO2|PbS electrodes has been investigated in photochronoamperometric measurements at 0 mV vs Ag/AgCl, 1 M KCl, using a white light source without a UV share (Figure S6). Therefore, the photocurrent responses of a 4-layered IO-TiO2 electrode before and after deposition of PbS QDs (4 cycles) in buffer have been compared (Figure S7). As expected, no photocurrent response is obtained for the pure IO-TiO2 (which can be attributed to the large band gap of TiO2, enabling only excitation at wavelength 500 mV by using the IO-TiO2|PbS4cycle|POs|FAD5217


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ACS Catalysis

separation with the efficient wiring of a specific enzymatic reaction via a redox polymer. This approach provides the basis for the efficient photonic wiring of other light-insensitive biocatalysts for light-directed sensing and power supply.

GDH architecture and light-directed readout. Consequently, the biohybrid architecture provides both a high driving force for the withdrawal of electrons from the enzyme by the redox polymer and a low working potential under illumination, resulting in a unique light-directed electrode arrangement with high performance. To estimate the amount of FAD-GDH bound to the 8-layered IO-TiO2 electrodes, the enzyme activity has been determined with a spectroscopic assay (for details, see Figure S17). An enzyme-surface concentration of 20 ± 2.7 pmol cm−2 has been estimated. By knowing the amount of bound FAD-GDH and the glucose-dependent current of the 8layered IO-TiO2|PbS4cycle|POs|FAD-GDH electrode under illumination with 100 mW cm−2 in the presence of 100 mM glucose (ΔI = 165 μA cm−2 at 0 mV vs Ag/AgCl, 1 M KCl), the electron turnover rate of the enzyme has been calculated to be ket = 85 ± 10 e− s−1. Long-term experiments with glucose in solution and under illumination with high intensity (100 mW cm−2) reveal a rather constant electron-transfer rate at the electrode, yielding a transferred charge of 220 mC cm−2 in 30 min (Figure S15). This demonstrates that electrode functionality even remains preserved under continuous irradiation with high light intensity, without observing a significant degradation of the enzyme. Under these conditions the cumulative anodic photocurrent output in the presence of glucose is found to be at least 70-fold higher than in previous studies with immobilized light-sensitive entity and enzyme on rather flat electrodes3,4,16 and 5-fold higher than on 3D electrodes.15 This can be attributed to the high surface area of the IO-TiO2 architectures but also to the efficient charge-carrier generation and separation at the QD/ TiO2 interface and the efficient wiring of FAD-GDH to the QDs via POs. Thus, our developed architecture gives access to an overall improved photo(bio)anode and may stimulate the interest in developing light-triggered biosensors, as well as solar-to-energy and solar-to-chemical converting biohybrid devices.

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METHODS Materials. N-(2-Hydroxyethyl)piperazine-N-(2-ethansulfonic acid) (99.5%; HEPES), D-glucose, fluorine-doped tin oxide-coated glass slides (7 Ω cm−1; FTO), lead(II) nitrate (99.999%; Pb(NO3)2), ammonium sulfide solution (20% in H2O; (NH4)2S), polystyrene latex beads (LBs, diameter 0.8 μm), and titanium tetraisopropoxide (97%; TTIP) were purchased from Sigma-Aldrich (Steinheim, Germany). Poly(1vinylimidazole-co-allylamine)-Os(bipy)2Cl-redox polymer has been synthesized as reported before.55 FAD-dependent glucose dehydrogenase from Aspergillus sp. has been obtained from SEKISUI CHEMICAL. Construction of IO-TiO2 Electrodes. First, FTO-coated glass slides have been successively immersed in deionized water, isopropanol, and acetone for 15 min each under ultrasonification. The cleaned slides have been dried before further use. A mixture of 100 mg mL−1 of latex beads (LBs; 0.8 μm diameter) and 100 mg mL−1 of titanium tetraisopropoxide (TTIP) in isopropanol has been prepared. Therefore, 200 μL of aqueous 100 mg mL−1 LB dispersion was mixed with 800 μL of ethanol and centrifuged at 25 000 g for 8 min to remove the water. The supernatant has been discarded, and the LB pellet has been suspended in 1 mL of ethanol followed by centrifugation at 25 000 g for 8 min. After removing the supernatant, the pellet has been suspended in 180 μL of isopropanol in an ultrasonication bath for 5 min. Finally, 20 μL of TTIP has been added fast to the LB suspension, which has been again ultrasonicated for 5 min. Afterward 6 μL per layer of the LB/TTIP-mixture has been dropped onto the cleaned FTO slides and spin-coated at 80 rps with a waiting time of 15 s between the deposition steps. The electrode area then has been limited to 0.071 cm2 by wiping away the superfluous material. The prepared electrodes have been sintered at 450 °C under air for 2 h, resulting in the final IO-TiO2 electrodes. Flat TiO2 electrodes have been prepared in an identical manner to the IO-TiO2 electrodes, but without LBs. Synthesis of PbS QDs. PbS QDs have been directly synthesized on the final IO-TiO2 electrodes with a SILAR approach.25−27 Therefore, the electrodes have been alternately immersed in aqueous 0.02 M Pb(NO3)2 and aqueous 0.02 M (NH4)2S for 1 min each, starting the SILAR process with the Pb2+ precursor. Between the deposition steps the electrode has been carefully rinsed with deionized water and ethanol to remove unbound precursors. In this respect one cycle is defined as one reaction with Pb2+ and S2−, respectively. IO-TiO2|PbS electrodes with up to 8 cycles have been prepared according to this procedure. Assembly of Redox Polymer and FAD-GDH. Four μL of a mixture containing 5 mg mL−1 poly(1-vinylimidazole-coallylamine)-Os(bipy)2Cl-redox polymer and 5 mg mL−1 FADGDH in 5 mM HEPES, pH 7, has been directly drop-casted on the IO-TiO2|PbS electrode and allowed to incubate for 15 min at room temperature in the dark. The drop spread over the whole IO film, indicating the filling of the pores with POs and FAD-GDH due to capillary forces. Subsequently, the modified electrode has been extensively rinsed with buffer to remove unbound material.

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CONCLUSION In summary, this work has introduced a new concept for the coupling of biocatalytic reactions to the light-triggered readout of QD electrodes. Here, a procedure for the scalable construction of IO-TiO2 electrodes has been established, serving as electrode platform for the integration of PbS QDs, a redox polymer, and FAD-GDH. Under illumination electron−hole pairs are generated within the PbS QDs and separated at the TiO2 interface, leaving behind holes that oxidize POs. As a result of glucose turnover, POs becomes regenerated, supplying the photoelectrochemical reaction with new electrons from the biocatalytic reaction for an enhanced photocurrent output. The signal response can be modulated by the potential, the light intensity, and the wavelength used during illumination, allowing the accurate control of the biohybrid system. Increasing glucose-dependent photocurrents have been obtained with rising QD loading and electrode height, showing a concentration-dependent behavior between 10 μM and 50 mM glucose. A first gain of electrons from the biocatalytic reaction has been found at rather negative potential of around −540 mV vs Ag/AgCl, 1 M KCl, giving access to the design of high-performance photobioelectrochemical cells using glucose as fuel. Such light-driven biohybrids are desirable due to their unique electrode properties, combining the photophysical features of the IO-TiO2|PbS electrode for charge-carrier generation and 5218


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Sensors for Chemical and Biological Detection. ACS Appl. Mater. Interfaces 2013, 5, 2800−2814. (6) Zhao, W.-W.; Xu, J.-J.; Chen, H.-Y. Photoelectrochemical Enzymatic Biosensors. Biosens. Bioelectron. 2017, 92, 294−304. (7) Woolerton, T. W.; Sheard, S.; Chaudhary, Y. S.; Armstrong, F. A. Enzymes and Bio-Inspired Electrocatalysts in Solar Fuel Devices. Energy Environ. Sci. 2012, 5, 7470−7490. (8) Feifel, S. C.; Stieger, K. R.; Lokstein, H.; Lux, H.; Lisdat, F. High Photocurrent Generation by Photosystem I on Artificial Interfaces Composed of π-System-Modified Graphene. J. Mater. Chem. A 2015, 3, 12188−12196. (9) Sokol, K. P.; Mersch, D.; Hartmann, V.; Zhang, J. Z.; Nowaczyk, M. M.; Rögner, M.; Ruff, A.; Schuhmann, W.; Plumeré, N.; Reisner, E. Rational Wiring of Photosystem II to Hierarchical Indium Tin Oxide Electrodes Using Redox Polymers. Energy Environ. Sci. 2016, 9, 3698− 3709. (10) Stieger, K. R.; Feifel, S. C.; Lokstein, H.; Hejazi, M.; Zouni, A.; Lisdat, F. Biohybrid Architectures for Efficient Light-to-Current Conversion Based on Photosystem I within Scalable 3D Mesoporous Electrodes. J. Mater. Chem. A 2016, 4, 17009−17017. (11) Reisner, E.; Powell, D. J.; Cavazza, C.; Fontecilla-Camps, J. C.; Armstrong, F. A. Visible Light-Driven H2 Production by Hydrogenases Attached to Dye-Sensitized TiO2 Nanoparticles. J. Am. Chem. Soc. 2009, 131, 18457−18466. (12) Mersch, D.; Lee, C.-Y.; Zhang, J. Z.; Brinkert, K.; FontecillaCamps, J. C.; Rutherford, A. W.; Reisner, E. Wiring of Photosystem II to Hydrogenase for Photoelectrochemical Water Splitting. J. Am. Chem. Soc. 2015, 137, 8541−8549. (13) Lisdat, F.; Schäfer, D.; Kapp, A. Quantum Dots on Electrodes new Tools for Bioelectroanalysis. Anal. Bioanal. Chem. 2013, 405, 3739−3752. (14) Tapia, C.; Milton, R. D.; Pankratova, G.; Minteer, S. D.; Åkerlund, H.-E.; Leech, D.; De Lacey, A. L.; Pita, M.; Gorton, L. Wiring of Photosystem I and Hydrogenase on an Electrode for Photoelectrochemical H2 Production by Using Redox Polymers for Relatively Positive Onset Potential. ChemElectroChem 2017, 4, 90−95. (15) Riedel, M.; Lisdat, F. Integration of Enzymes in PolyanilineSensitized 3D Inverse Opal TiO2 Architectures for Light-Driven Biocatalysis and Light-to-Current Conversion. ACS Appl. Mater. Interfaces 2018, 10, 267−277. (16) Tel-Vered, R.; Yildiz, H. B.; Yan, Y.-M.; Willner, I. Plugging into Enzymes with Light: Photonic “Wiring” of Enzymes with Electrodes for Photobiofuel Cells. Small 2010, 6, 1593−1597. (17) Hwang, E. T.; Sheikh, K.; Orchard, K. L.; Hojo, D.; Radu, V.; Lee, C.-Y.; Ainsworth, E.; Lockwood, C.; Gross, M. A.; Adschiri, T.; Reisner, E.; Butt, J. N.; Jeuken, L. J. A Decaheme Cytochrome as a Molecular Electron Conduit in Dye-Sensitized Photoanodes. Adv. Funct. Mater. 2015, 25, 2308−2315. (18) Zhang, J.; Tu, L.; Zhao, S.; Liu, G.; Wang, Y.; Wang, Y.; Yue, Z. Fluorescent Gold Nanoclusters Based Photoelectrochemical Sensors for Detection of H2O2 and Glucose. Biosens. Bioelectron. 2015, 67, 296−302. (19) Lubner, C. E.; Knörzer, P.; Silva, P. J. N.; Vincent, K. A.; Happe, T.; Bryant, D. A.; Golbeck, J. H. Wiring an [FeFe]-Hydrogenase with Photosystem I for Light-Induced Hydrogen Production. Biochemistry 2010, 49, 10264−10266. (20) Ciornii, D.; Riedel, M.; Stieger, K. R.; Feifel, S. C.; Hejazi, M.; Lokstein, H.; Zouni, A.; Lisdat, F. Bioelectronic Circuit on a 3D Electrode Architecture: Enzymatic Catalysis Interconnected with Photosystem I. J. Am. Chem. Soc. 2017, 139, 16478−16481. (21) Zeng, T.; Leimkühler, S.; Koetz, J.; Wollenberger, U. Effective Electrochemistry of Human Sulfite Oxidase Immobilized on Quantum-Dots-Modified Indium Tin Oxide Electrode. ACS Appl. Mater. Interfaces 2015, 7, 21487−21494. (22) Aldana, J.; Wang, Y. A.; Peng, X. Photochemical Instability of CdSe Nanocrystals Coated by Hydrophilic Thiols. J. Am. Chem. Soc. 2001, 123, 8844−8850. (23) Green, M. The Nature of Quantum Dot Capping Ligands. J. Mater. Chem. 2010, 20, 5797−5809.

SEM and HR-TEM Experiments. Scanning electron microscopy (SEM) measurements have been performed with a JSM-6510 from JEOL at an acceleration voltage of 30 kV with a 2 500-fold, 8 000-fold, and 25 000-fold magnification. The layer height of the IO-TiO2 electrode has been determined by scratching away a part of the structure and recording the IO film under an angle of 45° with a 2 500-fold magnification. HRTEM measurements have been performed with a FEI TITAN 80-300 transmission electron microscope (TEM). Photoelectrochemical Experiments. Photoelectrochemical measurements have been performed with an integrated photoelectrochemical workstation from Zahner, containing a potentiostat for the light control and a second potentiostat (Zennium) for the electrochemical control. For the illumination a white light source (410−800 nm) has been used unless stated otherwise. Wavelength-resolved measurements have been performed with a monochromator (Polychrome V, Till Photonics) with a bandwidth of 15 nm. All electrochemical experiments have been performed in a homemade electrochemical cell with a three-electrode arrangement, consisting of an IO-TiO2 working electrode, a platinum wire as counter electrode, and an Ag/AgCl, 1 M KCl, reference electrode.

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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/acscatal.8b00951. Additional SEM, transmittance, UV/vis, and photoelectrochemical data (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: fl[email protected]. ORCID

Marc Riedel: 0000-0001-6408-6067 Wolfgang Schuhmann: 0000-0003-2916-5223 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the German Research Foundation (DFG Grants Li 706/8-1 and Pa 794/15-1). REFERENCES

(1) Ipe, B. I.; Niemeyer, C. M. Nanohybrids Composed of Quantum Dots and Cytochrome P450 as Photocatalysts. Angew. Chem., Int. Ed. 2006, 45, 504−507. (2) Metzger, T. S.; Chandaluri, C. G.; Tel-Vered, R.; Shenhar, R.; Willner, I. Donor/Acceptor-Modified Electrodes for Photoelectrochemical and Photobioelectrochemical Applications. Adv. Funct. Mater. 2016, 26, 7148−7155. (3) Efrati, A.; Lu, C.-H.; Michaeli, D.; Nechushtai, R.; Alsaoub, S.; Schuhmann, W.; Willner, I. Assembly of Photo-Bioelectrochemical Cells Using Photosystem I-Functionalized Electrodes. Nat. Energy 2016, 1, 15021. (4) Riedel, M.; Sabir, N.; Scheller, F. W.; Parak, W. J.; Lisdat, F. Connecting Quantum Dots with Enzymes: Mediator-Based Approaches for the Light-Directed Read-out of Glucose and Fructose Oxidation. Nanoscale 2017, 9, 2814−2823. (5) Yue, Z.; Lisdat, F.; Parak, W. J.; Hickey, S. G.; Tu, L.; Sabir, N.; Dorfs, D.; Bigall, N. C. Quantum-Dot-Based Photoelectrochemical 5219


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ACS Catalysis (24) Khalid, W.; El Helou, M.; Murböck, T.; Yue, Z.; Montenegro, J.M.; Schubert, K.; Göbel, G.; Lisdat, F.; Witte, G.; Parak, W. J. Immobilization of Quantum Dots via Conjugated Self-Assembled Monolayers and Their Application as a Light-Controlled Sensor for the Detection of Hydrogen Peroxide. ACS Nano 2011, 5, 9870−9876. (25) Pathan, H. M.; Lokhande, C. D. Deposition of Metal Chalcogenide Thin Films by Successive Ionic Layer Adsorption and Reaction (SILAR) Method. Bull. Mater. Sci. 2004, 27, 85−111. (26) Lee, H.; Wang, M.; Chen, P.; Gamelin, D. R.; Zakeeruddin, S. M.; Grätzel, M.; Nazeeruddin, M. K. Efficient CdSe Quantum DotSensitized Solar Cells Prepared by an Improved Successive Ionic Layer Adsorption and Reaction Process. Nano Lett. 2009, 9, 4221−4227. (27) Lee, H.; Leventis, H. C.; Moon, S.-J.; Chen, P.; Ito, S.; Haque, S. A.; Torres, T.; Nüesch, F.; Geiger, T.; Zakeeruddin, S. M.; Grätzel, M.; Nazeeruddin, Md. K. PbS and CdS Quantum Dot-Sensitized SolidState Solar Cells: “Old Concepts, New Results. Adv. Funct. Mater. 2009, 19, 2735−2742. (28) Pardo-Yissar, V.; Katz, E.; Wasserman, J.; Willner, I. Acetylcholine Esterase-Labeled CdS Nanoparticles on Electrodes: Photoelectrochemical Sensing of the Enzyme Inhibitors. J. Am. Chem. Soc. 2003, 125, 622−623. (29) Tanne, J.; Schäfer, D.; Khalid, W.; Parak, W. J.; Lisdat, F. LightControlled Bioelectrochemical Sensor Based on CdSe/ZnS Quantum Dots. Anal. Chem. 2011, 83, 7778−7785. (30) Sabir, N.; Khan, N.; Völkner, J.; Widdascheck, F.; del Pino, P.; Witte, G.; Riedel, M.; Lisdat, F.; Konrad, M.; Parak, W. J. PhotoElectrochemical Bioanalysis of Guanosine Monophosphate Using Coupled Enzymatic Reactions at a CdS/ZnS Quantum Dot Electrode. Small 2015, 11, 5844−5850. (31) Riedel, M.; Hölzel, S.; Hille, P.; Schörmann, J.; Eickhoff, M.; Lisdat, F. InGaN/GaN Nanowires as a New Platform for Photoelectrochemical Sensors − Detection of NADH. Biosens. Bioelectron. 2017, 94, 298−304. (32) Stoll, C.; Kudera, S.; Parak, W. J.; Lisdat, F. Quantum Dots on Gold: Electrodes For Photoswitchable Cytochrome c Electrochemistry. Small 2006, 2, 741−743. (33) Grätzel, M. Photoelectrochemical Cells. Nature 2001, 414, 338− 344. (34) Grätzel, M. Solar Energy Conversion by Dye-Sensitized Photovoltaic Cells. Inorg. Chem. 2005, 44, 6841−6851. (35) Schneider, J.; Matsuoka, M.; Takeuchi, M.; Zhang, J.; Horiuchi, Y.; Anpo, M.; Bahnemann, D. W. Understanding TiO2 Photocatalysis: Mechanisms and Materials. Chem. Rev. 2014, 114, 9919−9986. (36) Heller, A. Electron-Conducting Redox Hydrogels: Design, Characteristics and Synthesis. Curr. Opin. Chem. Biol. 2006, 10, 664− 672. (37) Tsujimura, S.; Murata, K.; Akatsuka, W. Exceptionally High Glucose Current on a Hierarchically Structured Porous Carbon Electrode with “Wired” Flavin Adenine Dinucleotide-Dependent Glucose Dehydrogenase. J. Am. Chem. Soc. 2014, 136, 14432−14437. (38) Zafar, M. N.; Wang, X.; Sygmund, C.; Ludwig, R.; Leech, D.; Gorton, L. Electron-Transfer Studies with a New Flavin Adenine Dinucleotide Dependent Glucose Dehydrogenase and Osmium Polymers of Different Redox Potentials. Anal. Chem. 2012, 84, 334− 341. (39) Hyun, B.-R.; Zhong, Y.-W.; Bartnik, A. C.; Sun, L.; Abruña, H. D.; Wise, F. W.; Goodreau, J. D.; Matthews, J. R.; Leslie, T. M.; Borrelli, N. F. Electron Injection from Colloidal PbS Quantum Dots into Titanium Dioxide Nanoparticles. ACS Nano 2008, 2, 2206−2212. (40) Kamat, P. V. Quantum Dot Solar Cells. Semiconductor Nanocrystals as Light Harvesters. J. Phys. Chem. C 2008, 112, 18737−18753. (41) Shin, J.-H.; Kang, J.-H.; Jin, W.-M.; Park, J. H.; Cho, Y.-S.; Moon, J. H. Facile Synthesis of TiO2 Inverse Opal Electrodes for DyeSensitized Solar Cells. Langmuir 2011, 27, 856−860. (42) Seo, Y. G.; Woo, K.; Kim, J.; Lee, H.; Lee, W. Rapid Fabrication of an Inverse Opal TiO2 Photoelectrode for DSSC Using a Binary Mixture of TiO2 Nanoparticles and Polymer Microspheres. Adv. Funct. Mater. 2011, 21, 3094−3103.

(43) Waterhouse, G. I. N.; Waterland, M. R. Opal and Inverse Opal Photonic Crystals: Fabrication and Characterization. Polyhedron 2007, 26, 356−368. (44) Kwak, E. S.; Lee, W.; Park, N.-G.; Kim, J.; Lee, H. Compact Inverse-Opal Electrode Using Non-Aggregated TiO2 Nanoparticles for Dye-Sensitized Solar Cells. Adv. Funct. Mater. 2009, 19, 1093− 1099. (45) Liu, L.; Karuturi, S. K.; Su, L. T.; Tok, A. I. Y. TiO2 InverseOpal Electrode Fabricated by Atomic Layer Deposition for DyeSensitized Solar Cell Applications. Energy Environ. Sci. 2011, 4, 209− 215. (46) Jasieniak, J.; Califano, M.; Watkins, S. E. Size-Dependent Valence and Conduction Band-Edge Energies of Semiconductor Nanocrystals. ACS Nano 2011, 5, 5888−5902. (47) Pankratov, D.; Conzuelo, F.; Pinyou, P.; Alsaoub, S.; Schuhmann, W.; Shleev, S. A Nernstian Biosupercapacitor. Angew. Chem., Int. Ed. 2016, 55, 15434−15438. (48) Hines, D. A.; Kamat, P. V. Quantum Dot Surface Chemistry: Ligand Effects and Electron Transfer Reactions. J. Phys. Chem. C 2013, 117, 14418−14426. (49) Giansante, C.; Infante, I.; Fabiano, E.; Grisorio, R.; Suranna, G. P.; Gigli, G. Darker-than-Black” PbS Quantum Dots: Enhancing Optical Absorption of Colloidal Semiconductor Nanocrystals via Short Conjugated Ligands. J. Am. Chem. Soc. 2015, 137, 1875−1886. (50) Sauvé, G.; Cass, M. E.; Coia, G.; Doig, S. J.; Lauermann, I.; Pomykal, K. E.; Lewis, N. S. Dye Sensitization of Nanocrystalline Titanium Dioxide with Osmium and Ruthenium Polypyridyl Complexes. J. Phys. Chem. B 2000, 104, 6821−6836. (51) Monošík, R.; Streďanský, M.; Lušpai, K.; Magdolen, P.; Šturdík, E. Amperometric Glucose Biosensor Utilizing FAD-Dependent Glucose Dehydrogenase Immobilized on Nanocomposite Electrode. Enzyme Microb. Technol. 2012, 50, 227−232. (52) Zafar, M. N.; Beden, N.; Leech, D.; Sygmund, C.; Ludwig, R.; Gorton, L. Characterization of Different FAD-Dependent Glucose Dehydrogenases for Possible Use in Glucose-Based Biosensors and Biofuel Cells. Anal. Bioanal. Chem. 2012, 402, 2069−2077. (53) Milton, R. D.; Hickey, D. P.; Abdellaoui, S.; Lim, K.; Wu, F.; Tan, B.; Minteer, S. D. Rational Design of Quinones for High Power Density Biofuel Cells. Chem. Sci. 2015, 6, 4867−4875. (54) Gross, A. J.; Chen, X.; Giroud, F.; Abreu, C.; Le Goff, A.; Holzinger, M.; Cosnier, S. A High Power Buckypaper Biofuel Cell: Exploiting 1,10-Phenanthroline-5,6-Dione with FAD-Dependent Dehydrogenase for Catalytically-Powerful Glucose Oxidation. ACS Catal. 2017, 7, 4408−4416. (55) Badura, A.; Guschin, D.; Esper, B.; Kothe, T.; Neugebauer, S.; Schuhmann, W.; Rö gner, M. Photo-Induced Electron Transfer Between Photosystem 2 via Cross-Linked Redox Hydrogels. Electroanalysis 2008, 20, 1043−1047.

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Light as Trigger for Biocatalysis: Photonic Wiring of Flavin Adenine

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