Crucial Roles of ElectronâProton Transport Relay in the Photosystem

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Crucial Roles of Electron-Proton Transport Relay in the Photosystem II-Photocatalytic Hybrid System for Overall Water Splitting Wangyin Wang, Zhen Li, Jun Chen, and Can Li J. Phys. Chem. C, Just Accepted Manuscript • DOI: 10.1021/acs.jpcc.6b12002 • Publication Date (Web): 16 Jan 2017 Downloaded from http://pubs.acs.org on January 17, 2017

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The Journal of Physical Chemistry

Crucial Roles of Electron-Proton Transport Relay in the Photosystem II-Photocatalytic Hybrid System for Overall Water Splitting

Wangyin Wang1, Zhen Li1,2, Jun Chen1, Can Li1*

1

State Key Laboratory of Catalysis, Dalian Institute of Chemical Physics, Chinese

Academy of Sciences, Dalian National Laboratory for Clean Energy, The Collaborative Innovation Center of Chemistry for Energy Materials (iChEM), Dalian 116023, China 2

University of Chinese Academy of Sciences, Beijing 100049, China

1

ACS Paragon Plus Environment


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ABSTRACT Redox shuttle reaction plays a crucial role in electron and proton transfer process of natural and artificial photosynthesis for the solar-to-chemical energy conversion. In nature, photosynthetic electron transfer is delivered efficiently by the elaborated redox cofactors

for generation

of

the

reducing

equivalents.

However,

efficient

electron/proton transport is still a challenge to couple the natural and artificial photosynthetic system. Herein, we demonstrate a hybrid photosystem in conjugation of plant Photosystem II (PSII) and inorganic Ru/SrTiO3:Rh (Rh doped) photocatalyst with quinone-ferricyanide relay for overall water splitting reaction under visible light irradiation. Electrons and protons from natural PSII to artificial photocatalyst by a quinone molecule are transported at the bioinorganic interface. Furthermore, the quinone-ferricyanide transport relay is found to be much more efficient in enhancement of the water splitting activity. This work makes it possible to construct the hybrid photosynthetic system by taking the advantages of both natural and artificial systems.

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INTRODUTION Artificial photosynthesis for solar fuel production has been a top concerning research to address energy and environmental issues.1-3 Photocatalytic water splitting into hydrogen and oxygen represents a promising solar conversion technology for generation of renewable fuels.4-7 Natural photosynthesis is capable of utilizing sunlight for converting water and carbon dioxide into carbohydrates. Although the total efficiency of solar-to-chemical conversion is low, nature offers efficient enzymes for photosynthetic reactions.8-9 Photosystem II (PSII) protein is responsible for catalyzing water oxidation on the Mn4CaO5 cluster10-12 with the TOFs up to 100-300 s-1 at a very low overpotential,13-15 leading to the generation of the reducing equivalents for carbon dioxide fixation. These advantages have made PSII as an extremely intriguing benchmark as water oxidation catalyst, which re-engineered with artificial materials to construct hybrid systems capable of producing solar fuels from the viewpoint of utilizing sun light.16-20 The re-engineering of PSII with abiotic materials also provide insights into understanding the photosynthetic mechanism.21 For the water splitting chemistry of PSII, electrons from water are transferred via a series of redox cofactors and finally to the membrane diffusion plastoquinone (PQ).22 The redox potential of the terminal acceptor QB is close to the thermodynamic potential of proton reduction,23-25 which can be further enhanced by artificial “PSI” using light energy for hydrogen production. In a prelimary study, a hybrid photosystem coupled PSII with artificial photocatalyst has been demonstrated to be feasible for overall water splitting under sunlight. Inorganic Fe(CN)63-/Fe(CN)64- was 3



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used as electron shuttle for solar water splitting into stoichiometric hydrogen and oxygen.26 However, it turns out that the rate of shuttle reaction from enzyme to the mediator is a rate-determining step for the water splitting of the PSII based hybrid system. This is very much the same as that in natural photosynthetic process where PSII is responsible for the water oxidation.27 Water oxidation in the OEC is relative faster than the plastoquinone reduction by electrons and protons.28 The electron transfer from PSII to the artificial shuttle is more problematic: the exchange of the shuttles accepted electrons from QB site requires fast kinetics. A process that mimics the natural function of shuttle reaction is absolutely necessary to understand the process of solar conversion mechanism in natural and artificial photosynthesis. Proton-coupled electron transfer reaction plays a crucial role in natural photosynthesis29 and artificial systems.30 The reduction of PQ to plastoquinol (PQH2) is involved in proton transport across the membrane resulting in a proton gradient. The redox state and diffusion of plastoquinone is coordinated by the related excitation of photosystems.31-32 Redox reaction kinetics of PQ analogues in PSII was studied to reveal the mechanisms of electron transfer through the QB site in PSII complex.33-34 However, the redox process of the PQs at QB site in photosynthetic electron transport is not understood clearly.34-35 Our hybrid system raises the question how the shuttle reaction influences on electron transport from PSII to artificial “PSI” photocatalyst. Therefore, to further study the role of redox shuttle in the PSII-based photocatalytic overall water splitting system, it is necessary to investigate the hybrid system by employing biologic mimic redox molecules such as quinone molecules. Plastoquinone 4


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pool as a traffic hub of electron transfer with proton transport in the intact thylakoid membrane is not well understood either.36 It is very interesting to know how the overall water splitting reaction is controlled by the shuttles between the PSII and the artificial photocatalyst in the hybrid system. Herein, we report that an artificial relay for proton and electron transport scheme in the PSII-artificial Z-scheme hybrid system for overall water splitting into H2 and O2. This scheme involves quinones and quinone-ferricyanide combination for delivering the reductive equivalents in the hybrid system, in which PSII membrane and Ru/SrTiO3:Rh photocatalyst are used as the component for the O2 and H2 evolution reactions, respectively. The artificial photocatalyst Ru/SrTiO3:Rh is known in photocatalysis for H2 evolution.37-38 Quinone derivatives can act as shuttle for electrons and protons transfer in the hybrid system for photocatalytic water splitting. Moreover, electron transfer from PSII to Ru/SrTiO3:Rh is more efficient using the relay of DCBQ and Fe(CN)63-, resulting in the water splitting activities of 21.9 µmol H2 h-1 and 10.1 µmol O2 h-1 under visible light irradiation, which is about 3.3 folds of that with only Fe(CN)63-. The architecture of the artificial proton-coupled electron transport scheme for water splitting reaction provides insights into natural and artificial photosynthesis and their hybrid systems.

EXPERIMENTAL SECTION Preparation of isolated PSII membrane fragments The oxygen-evolving PSII-membrane was isolated from fresh spinach according to a reported procedure39. The Mn-depleted PSII as a control sample was prepared 5



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from the oxygen-evolving PSII via a Tris-treatment method to remove the Mn4CaO5 cluster as described previously40. The PSII samples (~2 mg chlorophyll mL-1) were finally suspended in a SMN buffer solution (400 mM sucrose, 50 mM MES-NaOH, 15 mM NaC1, pH 6.0), and then frozen in liquid nitrogen and stored at -72°C. The O2 evolution activities were measured by a Clark-type oxygen electrode in the SMN buffer with 0.53 mM 2,6-dichlorobenzoqinone and 1 mM potassium ferricyanide as electron acceptors. The oxygen evolution activity of PSII sample is over 800 µmol O2 (mg of chlorophyll)-1 h-1. The chlorophyll a concentration was employed for calculating the quantity of the PSII reaction centers by using 274 Chl a/PSII as a reference41. The Chl concentration was determined based on the optical absorption coefficients of chlorophyll a and b in a 80% acetone aqueous solution according to the following equation 42. Preparation of Ru/SrTiO3:Rh photocatalyst The SrTiO3:Rh (SrTiO3 doped with Rh) powder was synthesized by a solid-state reaction37. SrCO3, TiO2 and Rh2O3 were mixed evenly in a mortar according to the molar ratio Sr:Ti:Rh=1.03:1:0.01. This mixture was calcined at 1100°C for 10 h. The cocatalyst Ru (0.5 wt%) was loaded on SrTiO3:Rh (denote as Ru/SrTiO3:Rh) by photo-deposition as reported previously38. Briefly, a RuCl3 aqueous solution was added dropwise to a suspension of SrTiO3:Rh powder (0.5 g) in a 10% methanol aqueous solution. This mixture was degassed under vacuum, and then irradiated for 6 h. The obtained Ru/SrTiO3:Rh particles was filtered, washed with water, and finally dried at 50°C under vacuum. 6


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Preparation of the PSII-photocatalytic hybrid system To prepare the water splitting hybrid system, first of all, PSII samples are mixed with the quinone derivative on ice bath under dark condition. And then the component was integrated with the Ru/SrTiO3:Rh dispersed buffer solution slowly. Typically, photocatalyst powder (0.1 g) was first dispersed in 85 mL of the buffer solution (50 mM sodium phosphates, 15 mM NaCl, pH 6.0) by sonication. With potassium ferricyanide (2 mM) dissolved in this solution or not. Next, PSII samples (1 mg chlorophyll) are mixed with the DCBQ (10-100 µM) in 15 mL of the buffer solution for 1 hour on ice bath under dark condition and then the component was added in the Ru/SrTiO3:Rh dispersed buffer solution slowly under stirring at room temperature in the dark. Once the hybrid was completed, this aqueous mixture would be used for water splitting measurement. Measurement of photocatalytic water splitting reaction Photocatalytic water splitting reactions of the hybrid system were carried out under vacuum in a Pyrex reaction cell connected to a closed gas circulation and evacuation system and maintained at 25°C. The visible-light-driven water splitting reaction was conducted by the irradiation (250 mW cm-2) from a xenon lamp with a long-pass filter (λ>420 nm). The amounts of H2 and O2 evolution were monitored by online gas chromatography (5A zeolite column and Ar carrier gas, Agilent GC 7890A, USA). The water splitting tests of other reactant combinations were performed in a similar way, unless specific mentions.

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The photocatalytic water splitting of the hybrid system was carried out under irradiation with a solar simulator (AM 1.5G 100 mW cm-2, XES-40S2-CE). The STH efficiency (η) was determined as follows: η (%) =100⋅[(∆G0 ⋅R(H2)] /[ (P(solar light) ⋅ Α] Where ∆G0, R(H2), P(solar light) and A denote Gibbs free energy of water splitting (237.13 ⋅103 J mol-1), the rate of H2 evolution (mol s-1), the energy intensity of incident solar light (0.1 W cm-2) and the irradiation area (15.9 cm-2), respectively. The apparent quantum efficiency of water oxidation reaction by PSII was measured under the same reaction conditions with incident light at 680 nnm by using band-pass filter. The QE was calculated as follows: QE (%)= 100×(number of evolved O2 molecules×4)/(number of incident photons) Characterization Transmission electron microscopy (TEM) images were collected on a JEM-2000EX TEM. Ru/SrTiO3:Rh particles and PSII membrane were placed on a carbon-coated copper grid. The morphologies of the PSII-Ru/SrTiO3:Rh hybrid were examined by high resolution scanning electron microscopy (SEM) (S-5500, Hitachi and JSM-7800F, JEOL). The scanning and transmission modes can be operated simultaneously. The samples were placed on a carbon-coated copper grid. Atomic force microscopy (AFM) imaging was carried out in a tapping mode in air (Nanoscope 3D, Veeco, USA). Antimony-doped silicon cantilevers (tip radii of 8 nm) with resonant frequencies of 280-350 kHz were used, and nominal spring constant 8


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was 20 N/m. AFM samples were prepared by placing a diluted 10-µL drop of the hybrid system on a freshly cleaved mica surface for 10 min and washed with water to remove the buffer.

RESULTS AND DISCUSSION Inspired by biologic shuttle reaction, we employ quinone derivatives including 2,6-dichloro-1,4-benzoquinone

(DCBQ),

phenyl-p-benzoquinone

(PPBQ),

methyl-p-benzoquinone (MBQ) and benzoquinone (BQ) as PQ analogues to deliver electrons and protons through shuttle redox reaction in the PSII-Ru/SrTiO3:Rh hybrid system. The PSII-Ru/SrTiO3:Rh hybrid system was formed through nonspecific adsorptive interaction between proteins and solid particles43, in which the PSII membrane was made to interact with relative hydrophobic quinone completely at the beginning and then with semiconductor Ru/SrTiO3:Rh nanoparticles in the buffer solution before conducting the overall water splitting reaction . Imaging characterization of the PSII-Ru/SrTiO3:Rh hybrid system The isolated PSII membrane was a layered nanosheet with the size of about 700 nm (Figure 1a), in according with the AFM representations (Figure S1a). Figure 1b shows the TEM image of the formed PSII-Ru/SrTiO3:Rh hybrid system. It was found a portion of PSII membrane and Ru/SrTiO3:Rh were in combination with each other. Further analysis indicated that PSII membranes were adsorbed on the surface of the Ru/SrTiO3:Rh nanoparticles and the PSII protein particles were well-distributed (Figure 1c and 1d). The control Ru/SrTiO3:Rh photocatalyst showed a few Ru nanoparticles on the clear surface (Figures S1b and S1c). It was noted that due to the 9



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contrast of membrane on the Ru/SrTiO3:Rh surface is relatively weak, the membrane is not observed clearly from the images in the same region (Figures S1d and S1e). The morphology is consistent with previous report44. Figures 1e and 1f show that AFM images of the integration of PSII-Ru/SrTiO3:Rh hybrid system. A piece of the PSII membrane fragment was integrated on the surface of the Ru/SrTiO3:Rh nanoparticle from the height and phase image. This is in agreement with the resulting images of TEM and SEM. Hence, part PSII membrane fragment is free in the buffer solution of our hybrid system and the part membrane absorbed on the surface of the Ru/SrTiO3:Rh, forming the bio-inorganic interface for efficient electron transfer. Interfacial electron and proton transport by quinones for overall water splitting Water oxidation reaction by PSII was investigated using quinones as acceptor under red light irradiation. We assumed that all PSII samples are photoactive and the change of quinone concentration is not limited the activities during initial irradiation time.

Initial rates were calculated according to the oxygen concentration change

linearly for the first 20 s after irradiation with saturated red light to analyze the kinetic behaviors of oxygen evolution. Figure 2a shows the initial rates as a function of the concentration of different quinone derivatives. It was found that different oxygen evolution rate was achieved with DCBQ, PPBQ, MBQ and BQ as electron acceptors respectively, suggesting the water oxidation turnover of PSII is limited by the redox reaction at QB site. DCBQ was more efficient to accept electron from PSII. However, As seen in Figure 2b, photocatalytic overall water splitting into H2 and O2 proceeded with the comparative reaction rate for the first hour when quinone derivatives as 10


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shuttles are integrated within the PSII-Ru/SrTiO3:Rh hybrid respectively with the same method and at the same concentration (50 µM). This means that these quinone derivatives have the equivalent capabilities of electron and proton transport between PSII and Ru/SrTiO3:Rh in the hybrid systems. But it was found that higher initial rates of oxygen evolution were achieved with DCBQ and PPBQ than that of MBQ and BQ respectively at the same concentration level (50 µM) in half reaction (Figure 2a and Figure S2). The behaviors of quinones in overall water splitting reaction are different from that of water oxidation half reaction. Redox potentials of these quinone derivatives obtained by electrochemical measurement are not well associated with the photoreduction rates of the quinones (Table S1), indicating this is not key parameter of the quinone reduction. Quinone derivatives with different functional groups have different binding affinity with QB site of PSII, which leads to the difference in oxygen evolution33,

45

. The diffusion and exchange of hydroquinone and quinone at the

binding cavity is also one possibility for the activity discrepancy of different quinones in the water oxidation half reaction. The role of quinones is to shuttle electrons and protons in the PSII-[Quinone]-Ru/SrTiO3:Rh hybrid from water oxidation of PSII to Ru/SrTiO3:Rh where H2 is produced under visible light irradiation. Hence, the property of the microdomain at the bio-inorganic interfacial region decreases the resistance and distance of the shuttle diffusion in the hybrid system. Microdomain of PSII and artificial photocatalyst ensure rapid exchange of shuttle molecules and improve the efficiency of electron transport46. Figure 2c shows that DCBQ is employed to shuttling electrons and protons in the 11



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PSII-Ru/SrTiO3:Rh hybrid system for overall water splitting. When the DCBQ is integrated in the PSII-Ru/SrTiO3:Rh hybrid system, Simultaneous evolutions of H2 and O2 with stoichiometric ratio were detected, suggesting that electrons and protons are transferred from PSII to Ru/SrTiO3:Rh through redox reaction of DCBQ. It was noted that no H2 and O2 was detected in the PSII-Ru/SrTiO3:Rh hybrid system in the absence of DCBQ. We then investigated the kinetics of shuttle reaction in the hybrid system by changing the concentration of DCBQ. The water splitting activity of the PSII-Ru/SrTiO3:Rh hybrid system was found to be dependent on the initial concentration of the shuttle DCBQ. Catalytic water oxidation activity of PSII is increasing with a function of DCBQ concentration and the overall water splitting activities to be 14.9 µmol H2 h-1 and 7.9 µmol O2 h-1. Figure 2d shows typical time courses of H2 and O2 evolution of the PSII-[DCBQ]-Ru/SrTiO3:Rh system. The stability of the hybrid system was dependent on the isolated PSII protein, owing to the photodamage under continuous light irradiation for a few hours. Enhanced photocatalytic performance via biomimic electron transport relay To better understand the communication between PSII and Ru/SrTiO3:Rh, we constructed an electron transport relay coupling DCBQ and Fe(CN)63- in the overall water splitting hybrid system via an approach unavailable for nature. Figure 3a and the insert show that the initial rate of water oxidation was the same using DCBQ-Fe(CN)63- combination as that of DCBQ alone but higher than that of Fe(CN)63- at the beginning of illumination. The quantum efficiencies of water oxidation by PSII is about 20% for DCBQ and DCBQ-Fe(CN)63- combination and 3% 12


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for Fe(CN)63- respectively. Oxygen evolution rate of PSII can keep long time at high water oxidation rate with DCBQ-Fe(CN)63- combination. The O2 evolution activity was improved obviously up to 28.6 µmol h-1 using DCBQ-Fe(CN)63- combination, resulting in a nearly 6-fold enhancement compared with that of using DCBQ alone (Figure 3b, and Table 1, entries 1 and 3). Figure 3c shows the rate of water oxidation as a function of the concentration of DCBQ, in which ferricyanide is constant (2 mM). The activity is found to increase linearly with the concentration of DCBQ and the maximum rate was achieved at the concentration of 100 µM. When water splitting reaction was carried out by the PSII-[DCBQ-Fe(CN)63-]-Ru/SrTiO3:Rh hybrid system, it was found that overall water splitting was achieved and the H2 and O2 evolution activities were linearly increased (Figure 3d), in agreement with the results of the PSII-[DCBQ]-Ru/SrTiO3:Rh hybrid system (Figure 2c). The kinetic process correlates well with the enzyme kinetic process of oxygen evolution in PSII28. Therefore, these results lead us to the conclusion that the interfacial electron transport by electron shuttles is a kinetically controlled for overall water splitting. The water splitting activity is significantly increased up to around 21.9 µmol H2 h-1 and 10.1 µmol O2 h-1 in the first hour (Table 1, entry 6). However, turnover frequencies (TOFs) for PSII were determined to be 2527 mol H2 (mol PSII)-1 h-1 and 7143 mol O2 (mol PSII)-1 h-1 in overall water splitting reaction and water oxidation half reaction respectively, assuming all PSII dimer were capable of water oxidation (Table 1, entries 3 and 6). The effect of the Ru/SrTiO3:Rh on the oxygen evolution of the PSII was investigated under red light irradiation (λ>600 nm) and it was found that the activity of oxygen 13



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evolution decreased obviously when PSII was integrated with the Ru/SrTiO3:Rh (Figure S3). This indicates that the interaction of the biologic membrane and the inorganic Ru/SrTiO3:Rh surface might change the electron transport channel or a shielding effect by Ru/SrTiO3:Rh. The solar-to-hydrogen energy conversion efficiency using the shuttle combination was determined to be 0.043%, which is 3.6 times enhancement compared with only Fe(CN)63-/Fe(CN)64- shuttle under simulated sunlight (AM 1.5G, 100 mW cm-2) (Table S2). To verify electron is transferred from the PSII to the Ru/SrTiO3:Rh through DCBQ in the hybrid photosystem, water splitting reaction was tested using an inhibitor to block electron transport chain of PSII. DCMU (3-(3,4-dichlorophenyl)-1,1 -dimethylurea) is a special inhibitor of the PSII. It could selectively bind to the QB site of PSII to block the electron transfer pathway of PSII27. After treated with DCMU, the PSII-Ru/SrTiO3:Rh hybrid didn’t produce O2 under visible light irradiation (Table 1, entry 8). This result clearly convinces that the electrons are transferred from PSII to artificial photocatalyst via the shuttle reaction. In the case of Mn-depleted PSII, the result is in consistent with the case of adding the inhibitor because water oxidation is stopped without Mn4CaO5 cluster (Table 1, entry 9). It’s noted that the negligible amount of H2 in the two experiments was due to the background reaction of the H2 evolution photocatalyst. These evidences unambiguously demonstrated that electrons for H2 production are from water oxidation of PSII. Electron and proton transport pathways from PSII to Ru/SrTiO3:Rh Insight into the mechanism for the enhancement of water splitting activity is 14


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provided by the photocatalytic reaction in the absence of the artificial photocatalyst. The electrochemical measurement indicated that the redox potential of the Fe(CN)63-/4- couple is more positive than that of the DCBQ couple (Table S1), thus electron can be transfer from the reduced DCBQ to Fe(CN)63- thermodynamically. We found that when the two components were mixed, the color of solution was changed immediately, indicating the redox reaction between DCBQH2 and Fe(CN)63- is very fast. Absorption spectra revealed that this was a stoichiometric redox reaction (Figure S4). The absorption peak change of shuttle molecule was monitored by UV-Vis absorbance spectroscopy when the acceptors were reduced by PSII under red light irradiation with a function of time. The peak at 274 nm due to DCBQ was decreased, indicating DCBQ was reduced to DCBQH2 (295 nm) by PSII gradually (Figure S5). Absorbance values of DCBQ at 274 nm and Fe(CN)63- at 420 nm were traced at intervals (Figure S6a). The absorbance value of DCBQ remains the same as the initial level but the value of Fe(CN)63- is linearly decreased in the first 30 seconds (Figure S6b). As irradiation time goes on, both of the values are decreasing. Likewise, kinetics plots of photoreduction of DCBQ and Fe(CN)63- by PSII measured under in situ reaction indicate that electrons is transferred to DCBQ and then to Fe(CN)63quickly (Figure S7). Therefore, using the DCBQ-Fe(CN)63- combination increases the efficiency of electron transfer from PSII to Ru/SrTiO3:Rh in the hybrid system. Once DCBQ is reduced by the electrons form PSII, the reduced DCBQ is oxidized by the Fe(CN)63- immediately. Namely, the electron transfer from DCBQ to Fe(CN)63- is facile. This redox reaction makes DCBQ in the oxidation state. Ferricyanide plays the 15



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partial role of the Cyt b6f protein complex in photosynthesis. In natural photosynthesis, diffusion process of the plastoquinone in thylakoid is important to control photosynthetic electron transfer between PSII and Cyt b6f complex.31, 36, 47 A plastoquinone pool between PSII and Cyt b6f in the thylakoid membrane is used to store the PQs and regulate the redox state of PQs. Thus, in the hybrid system, the formed microenvironment at the bio-inorganic interface is favorable for shuttle redox reaction of quinones, where the function is equivalent to the plastoquinone pool in natural process. Quinone diffusion confined to the small microdomain nearby active PSII complex and artificial photocatalyst is in favor of improving the catalytic cycle reaction of quinone. As partial PSII membrane is not integrated on the surface of the Ru/SrTiO3:Rh according to the imaging results, the relative hydrophobic quinone shuttle has to diffuse long distance for the faraway unbounded PSII far from the Ru/SrTiO3:Rh photocatalyst. The quinone-ferricyanide shuttle combination can improve the efficiency of electron transport. Thus, we propose that the hybrid system provides two pathways of electron transport from PSII to Ru/SrTiO3:Rh for overall water splitting reaction as shown in Figure 4: (a) direct transfer via DCBQ at the interfacial microdomain and (b) transfer through DCBQ to Fe(CN)63- in the bulk solution.

CONCLUSIONS The present work has introduced an artificial electron and proton transport pathway based on quinone molecule in the bio-artificial PSII-Ru/SrTiO3:Rh hybrid photosystem, which catalyzes overall water splitting into H2 and O2 under visible light 16


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irradiation. Quinones play a crucial role in electron and proton transfer from PSII to Ru/SrTiO3:Rh via shuttle reactions. The hybrid systems with different quinone derivatives as shuttle at the interfacial microdomain show a comparable water splitting activities without limited by diffusion kinetics. Furthermore, combination of DCBQ and Fe(CN)63- as electron transport relay in the hybrid system enhanced the activity of overall water splitting up to 5466 mol H2 (mol PSII)-1 h-1 which increased by 3.3 times compared with the only Fe(CN)63-. Correspondingly, the efficiency for solar energy to hydrogen conversion is increased from 0.012% to 0.043% under simulated sunlight (AM 1.5G 100 mW cm-2). The conjugation of biological protein and inorganic semiconductor-based photocatalyst through bio-inspired approach conceptually provides us insights into understanding the electrons and protons transfer pathways in biological and artificial photosynthetic system. Our work reported here also paves a new way to develop the advanced bio-hybrid photosynthetic systems, as well as explore the nature behind the mechanisms of photosynthesis.

AUTHOR INFORMATION Corresponding author E-mail: [email protected] Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENTS This work was financially supported by National Natural Science Foundation of China (21603224) and 973 National Basic Research Program of the Ministry of 17



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Science and Technology (Grant 2014CB239403). The authors would like to thank Mr. Linyan Hu for AFM experiments and thank Mr. Xuming Wei for SEM experiments.

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Photo-Bioelectrochemical Cells. Photosynth Res. 2014, 120, 71-85. (19) Wang, W.; Wang, Z.; Zhu, Q.; Han, G.; Ding, C.; Chen, J.; Shen, J.-R.; Li, C. Direct Electron Transfer from Photosystem II to Hematite in a Hybrid Photoelectrochemical Cell. Chem. Commun. 2015, 51, 16952-16955. (20) Wang, W.; Wang, H.; Zhu, Q.; Qin, W.; Han, G.; Shen, J.-R.; Zong, X.; Li, C. Spatially Separated Photosystem II and a Silicon Photoelectrochemical Cell for Overall Water Splitting: A Natural–Artificial Photosynthetic Hybrid. Angew. Chem. Int. Edit. 2016, 55, 9229-9233. (21) Kato, M.; Zhang, J. Z.; Paul, N.; Reisner, E. Protein Film Photoelectrochemistry of the Water Oxidation Enzyme Photosystem II. Chem. Soc. Rev. 2014, 43, 6485-6497. (22) Kern, J.; Renger, G. Photosystem II: Structure and Mechanism of the Water:Plastoquinone Oxidoreductase. Photosynth Res. 2007, 94, 183-202. (23) Shibamoto, T.; Kato, Y.; Sugiura, M.; Watanabe, T. Redox Potential of the Primary

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Transfer Regulation. Proc. Natl Acad. Sci. USA 2016, 113, 620-625. (26) Wang, W.; Chen, J.; Li, C.; Tian, W. Achieving Solar Overall Water Splitting with Hybrid Photosystems of Photosystem II and Artificial Photocatalysts. Nat. Commun. 2014, 5, 4647. (27) Ulas, G.; Brudvig, G. W. Redirecting Electron Transfer in Photosystem II from Water to Redox-Active Metal Complexes. J. Am. Chem. Soc. 2011, 133, 13260-13263. (28) Khan, S.; Sun, J. S.; Brudvig, G. W. Cation Effects on the Electron-Acceptor Side of Photosystem II. J. Phys. Chem. B 2015, 119, 7722-7728. (29) McEvoy, J. P.; Brudvig, G. W. Water-Splitting Chemistry of Photosystem II. Chem. Rev. 2006, 106, 4455-4483. (30)Weinberg, D. R.; Gagliardi, C. J.; Hull, J. F.; Murphy, C. F.; Kent, C. A.; Westlake, B. C.; Paul, A.; Ess, D. H.; McCafferty, D. G.; Meyer, T. J. Proton-Coupled Electron Transfer. Chem. Rev. 2012, 112, 4016-4093. (31) Millner, P. A.; Barber, J. Plastoquinone as a Mobile Redox Carrier in the Photosynthetic Membrane. FEBS Lett. 1984, 169, 1-6. (32) Tikhonov, A. N. The Cytochrome B6f Complex at the Crossroad of Photosynthetic Electron Transport Pathways. Plant Physiol. Biochem. 2014, 81, 163-183. (33) Kashino, Y.; Yamashita, M.; Okamoto, Y.; Koike, H.; Satoh, K. Mechanisms of Electron Flow through the Qb Site in Photosystem II. 3. Effects of the Presence of Membrane Structure on the Redox Reactions at the Qb Site. Plant Cell Physiol. 1996, 22


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Photosystem II Preparations from Cyanobacteria and Plants. Biochemistry 1996, 35, 7802-7811. (42) Lichtenthaler, H. K. Chlorophylls and Carotenoids-Pigments of Photosynthetic Biomembranes. Methods Enzymol. 1987, 148, 350-382. (43) Katz, E.; Willner, I. Integrated Nanoparticle–Biomolecule Hybrid Systems: Synthesis, Properties, and Applications. Angew. Chem. Int. Edit. 2004, 43, 6042-6108. (44) Kaftan, D.; Brumfeld, V.; Nevo, R.; Scherz, A.; Reich, Z. From Chloroplasts to Photosystems: In Situ Scanning Force Microscopy on Intact Thylakoid Membranes. Embo J. 2002, 21, 6146-6153. (45) Shevela, D.; Messinger, J. Probing the Turnover Efficiency of Photosystem II Membrane Fragments with Different Electron Acceptors. Biochim. Biophys. Acta 2012, 1817, 1208-1212. (46) Johnson, M. P.; Vasilev, C.; Olsen, J. D.; Hunter, C. N. Nanodomains of Cytochrome B6f and Photosystem II Complexes in Spinach Grana Thylakoid Membranes. Plant Cell 2014, 26, 3051-3061. (47) Lavergne, J.; Joliot, P. Restricted Diffusion in Photosynthetic Membranes. Trends Biochem. Sci. 1991, 16, 129-134.

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Figure 1. Images of the PSII-Ru/SrTiO3:Rh hybrid. (a) TEM image of the spinach PSII membrane and (b) the PSII-Ru/SrTiO3:Rh hybrid system. (c, d) SEM image of the PSII-Ru/SrTiO3:Rh hybrid system. AFM image of the PSII-Ru/SrTiO3:Rh hybrid system, (e) height image and (f) phase image.

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Figure 2. Quinones as electron and proton transport shuttle in the hybrid system for overall water splitting. (a) The initial rate of oxygen evolution by PSII membrane depends on the concentration of different quinones. (b) H2 and O2 evolution activities of the hybrid photosystems with 50 µM different quinone derivatives as shuttles, respectively. (c) The activities of H2 and O2 evolution depend on the concentration of DCBQ. (d) Time course of overall water splitting by the PSII-[DCBQ]-Ru/SrTiO3:Rh hybrid system using 100 µM DCBQ. The systems dispersed in the phosphates buffer solution containing 50 mM sodium phosphate and 15 mM sodium chloride (pH=6.0), (a) the initial rate of PSII was calculated from the data of the first 20 s after irradiation with saturated red light (λ>600 nm) and the increasing concentration of oxygen evolution were measured by Clark-type oxygen electrode. (b-d) the H2 and O2 rates 26


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were an average rate per hour, calculating from the amount of gas evolved in the first hour. The gases were detected by GC. The light source is Xe lamp (250 mW cm-2) with a long-pass filter (λ>420 nm) at the temperature of 298 K. Error bars represent the standard deviation of three experimental results.

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Figure 3. Overall water splitting by the hybrid system with the DCBQ-Fe(CN)63relay. (a and insert) The initial kinetic plots of photocatalytic water oxidation and (b) time courses of photocatalytic O2 evolution using 100 µM DCBQ, 2 mM [Fe(CN)6]3and their combination as electron acceptors. (c)The oxygen evolution activities of PSII and (d) overall water splitting activity of the hybrid system dependence on the concentration of DCBQ shuttle with constant ferricyanide (2 mM). The systems dispersed in the phosphates buffer solution (100 mL) containing 50 mM sodium phosphate and 15 mM sodium chloride (pH=6.0).Error bars represent the standard deviation of three experimental results.

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Table 1. Water splitting activities of the PSII-photocatalytic hybrid system under visible light irradiation

Entry

Shuttle

Artificial photocat.

TOFb mol gas (mol PSII)-1 h-1

H2

O2

H2

O2

1

PSII

DCBQ

0

4.6±0.6

0

1147±139

2

PSII

Fe(CN)63-

0

3.5±0.3

0

881±67

3

PSII

DCBQFe(CN)63-

0

28.6±3.2

0

7143 ± 802

4

PSII

DCBQ

Ru/SrTiO3:Rh 14.9±1.1 7.9±0.4

3729±275

1976±91

5

PSII

Fe(CN)63-

Ru/SrTiO3:Rh 6.7±2.3 3.1±0.4

1681±567

770±91

6

PSII

DCBQFe(CN)63-

Ru/SrTiO3:Rh 21.9±0.6 10.1±0.7 5466±143

7

PSII

8

PSII+ DCMU

9 a

Enzyme

Activitya µmol gas h-1

2527±175

Ru/SrTiO3:Rh 0.3±0.1

0

85±23

0

DCBQFe(CN)63-


0

366±103

0

Mn-depleted DCBQPSII Fe(CN)63-


0

438±92

0

The activities were the amount of gas evolved in the first hour. b TOF (h-1) based on

the concentration of PSII reaction center ([Chl]/[RC]=274). The amounts of components (if used) were: photocatalysts, 0.1 g; DCBQ, 0.1 mM; Fe(CN)63-, 2 mM; PSII or Mn-depleted PSII, 1 mg chlorophyll; DCMU, 12 µM. They were dispersed in 100 mL of the buffer solution (50 mM sodium phosphates, 15 mM NaCl, pH 6.0) at 298 K. The light source was a xenon lamp with a long-pass filter (λ>420 nm), and the power density was 250 mW · cm-2. 29



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Figure 4. Schematic representation of H+/e- transport pathway. Biomimic electron transport relay combined quinone derivative and ferricyanide are constructed in the PSII-Ru/SrTiO3:Rh hybrid system for solar water splitting into H2 and O2 under visible light irradiation. There are two paths of electron transfer from PSII protein to Ru/SrTiO3:Rh photocatalyst in the hybrid system: (1) direct transfer via DCBQ at the interfacial microdomain and (2) indirect transfer from DCBQ to Fe(CN)63- in the bulk solution.

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