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Communication
Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation Masaru Kato, Tanai Cardona, Alfred William Rutherford, and Erwin Reisner J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/ja404699h • Publication Date (Web): 05 Jul 2013 Downloaded from http://pubs.acs.org on July 10, 2013
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Journal of the American Chemical Society
Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation Masaru Kato,† Tanai Cardona,‡ A. William Rutherford‡ and Erwin Reisner†* †
Department of Chemistry, University of Cambridge, Lensfield Road, Cambridge CB2 1EW, U.K.
‡
Department of Life Sciences, Imperial College London, London SW7 2AZ, U.K.
Supporting Information Placeholder ABSTRACT: Photosystem II (PSII) offers a biological and sustainable route of photochemical water oxidation to O2 and can provide protons and electrons for the generation of solar fuels such as H2. We present a rational strategy to elec-‐ trostatically improve the orientation of PSII from a thermo-‐ philic cyanobacterium, Thermosynechococcus elongatus, on a nanostructured indium tin oxide (ITO) electrode and to co-‐ valently immobilize PSII on the electrode. The ITO electrode was modified with a self-‐assembled monolayer (SAM) of phosphonic acid ITO linkers with a dangling carboxylate moiety. The negatively charged carboxylate attracts the posi-‐ tive dipole on the electron acceptor side of PSII via Coulomb interactions. Covalent attachment of PSII in its electrostati-‐ cally improved orientation to the SAM-‐modified ITO elec-‐ trode was accomplished via an amide bond to further en-‐ hance red-‐light driven, direct electron transfer and stability of the PSII hybrid photoelectrode.
Solar light driven splitting of water into its elements is a 1 sustainable route to generate hydrogen-‐based fuels. A major challenge in water splitting is the thermodynamically up-‐hill reaction of water oxidation to O2, which involves a four-‐ electron and four-‐proton transfer process. Photosystem II (PSII) is the natural water oxidation enzyme managing light absorption, charge separation and the extraction of electrons and protons through the oxidation of water in a pH neutral 2 aqueous solution. PSII operates at a high rate − it oxidizes approximately 100 water molecules per second during full sunlight irradiation with an upper turnover number estimat-‐ ed to be approximately one million within the lifetime of the 3 [Mn4Ca] water oxidation catalyst. PSII therefore serves as the unchallenged benchmark and an inspiration in photo-‐ 4 catalytic water oxidation. Protein film photoelectrochemistry (PF-‐PEC), the photo-‐ 5 chemical analogue to protein film electrochemistry, is cur-‐ rently in its infancy as a probe to study the function of pho-‐ 6 tosynthetic enzymes such as photosystem I and PSII. PF-‐ PEC is thereby a promising technique to study the photo-‐ catalytic rates and performance of photosynthetic enzymes under different conditions. We have recently reported on direct electron transfer (DET) from PSII to a mesoporous 6c indium tin oxide (mesoITO) electrode. PSII was adsorbed to the bare ITO surface in a random orientation and the
three-‐dimensional and transparent mesoITO electrode al-‐ lowed for good electrical conductivity and high PSII 6c loading. Several redox enzymes with biotechnological rele-‐ 7 8 vance such as hydrogenases and laccases were previously immobilized on electrodes in a controlled orientation to im-‐ prove DET and the electrostability of the enzyme in protein film electrochemistry. Compared to these enzymes, the con-‐ trolled immobilization of PSII on electrodes is not straight-‐ forward: PSII is photoactive and relatively huge (a molecular weight of approximately 700 kDa and a size of 10.5×20.5×11.0 3 2a,b nm for cyanobacterial PSII dimers), and its electron dona-‐ tion sites to electrodes are placed on one region at the stro-‐ mal side of PSII (Figure 1). In this communication, we report on a rational protocol to improve the orientation of a cyanobacterial PSII on a self-‐ assembled monolayer (SAM)-‐functionalized mesoITO elec-‐ trode resulting in improved interfacial electronic communi-‐ cation between ITO and PSII. Covalent immobilization of oriented PSII to the electrode surface further improved DET and the stability of the enzyme (Figure 1).
Figure 1. Schematic representation for the assembly of (A) mesoITO|SAM-‐CO2–, (B) electrostatic immobilization of PSII (e-‐mesoITO|SAM-‐CO2–|PSII) and (C) covalent bonding (c-‐ mesoITO|SAM-‐CO2–|PSII). (D) Red light-‐driven DET and 2,6-‐dichloro-‐1,4-‐benzoquinone-‐mediated electron transfer (MET) resulting in photocurrents with c-‐mesoITO|SAM-‐ CO2–|PSII.
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Journal of the American Chemical Society
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Chart 1. Compounds used for SAMs on mesoITO. SAM
R
n
Abbreviation
CO2H NH2 CO2H CO2H
2 2 5 15
SAM-‐C2CO2 + SAM-‐C2NH3 − SAM-‐C5CO2 − SAM-‐C15CO2
H2O3P
n
R
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diffusional redox mediator, 2,6-‐dichloro-‐1,4-‐benzoquinone, was used. This observation suggests that the negatively charged mesoITO|SAM-‐C2CO2– surface resulted in improved orientation of PSII on ITO and, consequently, enhanced in-‐ terfacial electronic communication between PSII and ITO. No photocurrent was observed in the absence of PSII for mesoITO|SAM-‐C2CO2–. PSII in the absence of the [Mn4Ca] 11 water oxidation catalyst (Mn-‐depleted PSII) on mesoI-‐ – TO|SAM-‐C2CO2 resulted in only a minor photocurrent (< 0.02 µA cm–2), demonstrating that the photocurrent respons-‐ es resulted from water oxidation.
−
MesoITO electrodes with a geometrical surface area of 0.25 2 cm were synthesized by annealing a paste of ITO nanoparti-‐ cles (
