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ScienceDirect Nanobiocatalytic assemblies for artificial photosynthesis Jae Hong Kim1, Dong Heon Nam1 and Chan Beum Park Natural photosynthesis, a solar-to-chemical energy conversion process, occurs through a series of photo-induced electron transfer reactions in nanoscale architectures that contain lightharvesting complexes, protein-metal clusters, and many redox biocatalysts. Artificial photosynthesis in nanobiocatalytic assemblies aims to reconstruct man-made photosensitizers, electron mediators, electron donors, and redox enzymes for solar synthesis of valuable chemicals through visible lightdriven cofactor regeneration. The key requirement in the design of biocatalyzed artificial photosynthetic process is an efficient and forward electron transfer between each photosynthetic component. This review describes basic principles in combining redox biocatalysis with photocatalysis, and highlights recent research outcomes in the development of nanobiocatalytic assemblies that can mimic natural photosystems I and II, respectively. Current issues in biocatalyzed artificial photosynthesis and future perspectives will be briefly discussed. Addresses Department of Materials Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), 335 Science Road, Daejeon 305-701, Republic of Korea Corresponding authors: Park, Chan Beum ([email protected]) These authors contributed equally to this work.

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Current Opinion in Biotechnology 2014, 28:1–9 This review comes from a themed issue on Nanobiotechnology Edited by Jonathan S Dordick and Kelvin H Lee

0958-1669/$ – see front matter, # 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.copbio.2013.10.008

Introduction In nature, green plants successfully convert solar energy into chemical energy via natural photosynthesis (6H2O + 6CO2 + solar energy ! C6H12O6 + 6O2) through multistep, photo-induced transfer of energy and electrons. This process has unparalleled, unique features such as nearunity quantum yield and operates in an environmentally friendly manner with no generation of toxic intermediates and products. Natural photosynthesis has inspired many researchers to devise an artificial photosynthetic process that can convert solar energy to fuels and valuable chemicals through the assemblies of organic and inorganic nanomaterials [1–4]. Solar energy is harvested in photosynthetic organisms using photosystems made of highly sophisticated nanostructures that include multiple organic www.sciencedirect.com

photosensitizers (e.g. chlorophyll a and carotenoids), electron mediators (e.g. plastoquinone, plastocyanine, and ferredoxin), and catalytic protein/metal clusters, which is stored in the form of high energy chemicals such as NADPH and ATP. The light reaction is closely coupled with the Calvin cycle, which occurs through a cascade of redox enzymatic reactions that consume NADPH and ATP to reduce CO2 to carbohydrates (Figure 1a). Inspired from natural photosynthesis, biocatalytic artificial photosynthesis photochemically regenerates cofactors, such as NAD(P)H and flavins, for redox enzymatic reactions by using light-harvesting nanomaterial assemblies (e.g. silicon nanowires, quantum dots, and organic dyes) (Figure 1b). The coupling of redox enzymatic reactions with photoinduced energy and electron transfer provides an opportunity for the synthesis of fine chemicals and fuels under visible light. While conventional artificial photosynthetic approaches mostly employ inorganic catalysts that can produce simple chemicals (e.g. H2, CO, methanol) [5–8], redox enzymes (or oxidoreductases) can synthesize a variety of chemicals such as fuels, chiral compounds, and drug intermediates with high specificity under mild conditions (e.g. room temperature, neutral pH, atmospheric pressure, aqueous medium) [9–13]. Recently, many remarkable photochemical routes have been reported for visible light-driven cofactor regeneration to be coupled with redox enzymatic synthesis in homogeneous systems. This review will summarize key principles and issues in the design of biocatalytic artificial photosynthesis and introduce recent advances in the development of nanobiocatalytic assemblies and light-harvesting materials for efficient photo-induced electron transfer (PET) toward biomimetic photosynthesis.

Natural versus artificial photosynthesis The light reaction in natural photosynthesis occurs through the Z-scheme by PET from photosystem (PS) II to PS I (Figure 2a) [14,15]. In PS II, chlorophyll a (i.e. P680) absorbs photon energy, which excites electrons and transfers them to plastoquinone (Pq), an electron acceptor [16]. Meanwhile, the photo-excited P680 (P680*) generates a driving force for extracting electrons from the water molecule at the calcium-manganese center, which acts as a water-oxidation catalyst [17]. The electron transport chain, which consists of Pq, cytochrome complex, and plastocyanine (Pc), carries electrons from PS II to PS I. Similarly to PS II, electrons excited by P700 are transferred to ferredoxin (Fd) and used to reduce NADP+ to NADPH through Fd-NADP reductase. The newly formed NADPH is then consumed to fix CO2 through the biocatalytic cascade of the Calvin cycle [14]. Overall, natural photosynthesis occurs through complicated Current Opinion in Biotechnology 2014, 28:1–9

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Schematic illustration of (a) natural photosynthesis and (b) biocatalytic artificial photosynthesis. In both processes, photosystems transfer photoinduced electrons from electron donors to nicotinamide cofactors under visible light, which are coupled to the redox biocatalytic cycle for solar-tochemical conversion.

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(a) Natural photosynthesis occurs through the electron transport chain, which includes many electron mediators such as plastoquinone (Pq), Cytochrome complex, and plastocyanine (Pc). The reaction center in photosystem II triggers a photochemical water oxidation reaction at the oxygenevolving center (OEC). Photosystem I transfers excited electrons to NADP reductase through the primary acceptor, ferredoxin (Fd) for the regeneration of NADPH. The NADPH regenerated by photosystem I is then consumed during the reduction of carbon dioxide to carbohydrates in the Calvin cycle. (b) The structure of the thylakoid membrane in chloroplasts, where efficient photo-excited electron transfer occurs through precise arrangement and coordination of PS I and II components. Current Opinion in Biotechnology 2014, 28:1–9

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Nanobiocatalytic artificial photosynthesis Kim, Nam and Park 3

energy conversion processes that consist of multiple steps including water oxidation, light harvesting, electron transfer cascade, and the Calvin cycle. The biological photosystem is a molecular machinery that is based on highly sophisticated nanostructures that contain organic photosensitizers, protein/metal clusters, and electron mediators embedded within a thylakoid membrane (Figure 2b). For example, the excited electrons from the oxygen evolving center (OEC) and Pc via P680 and P700 are transferred to Pq and Fd efficiently across short distances (50 A˚ in PS II and 70 A˚ in PS I) [18]. In addition, the chain of electron transport (e.g. Pq, cytochrome complex, and Pc) makes the electron transfer from PS II to PS I energetically favorable. Furthermore, the light-harvesting complexes (LHC) in PS I and II enhance quantum efficiency (approximately 90%) by maximizing photon absorption [19]. For example, the LHC in the PS II of purple non-sulfur bacteria is a cyclic arrangement that is created through the self-assembly of bacteriochlorophyll a (27 units) and carotenoids (14 units) together with proteins [20]. The precise arrangement and molecular coordination enable efficient photon collection through energy transfer between light-harvesting pigments. The unique features of natural photosynthesis, such as nearunity quantum yield and efficient PET, originate from highly sophisticate arrangement of photosynthetic components, which hint at the design of man-made nanomaterials and their assemblies for the construction of efficient artificial photosynthetic systems. The rational design of biocatalytic artificial photosynthetic systems requires four key components (Figure 3a): firstly, electron donor to provide electrons for photo-excitation; secondly, photosensitizer to absorb photon energy from sunlight; thirdly, electron mediators to transport electrons with minimal energy loss and prevent back electron transfer; fourthly, redox biocatalysts to store light energy in chemical forms. Electron donors (e.g. water, triethanolamine, triethylamine, ethylenediaminetetraacetic acid, and ascorbic acid) are needed to provide electrons to the ground state of an excited photosensitizer. The band gap of the photosensitizer should be larger than 1.9 eV and smaller than 3.1 eV to absorb visible light. In addition, the energy level of the photo-excited electrons must be higher than the reduction potential of NAD(P)+ (0.85 V versus NHE). To minimize the loss of excited electrons during photochemical NAD(P)H regeneration, an electron mediator is crucially needed; a rhodium-based organometallic complex, Cp*Rh(bpy)H2O2+ (M, Cp* = pentamethylcyclodienyl, bpy = bipyridine), has been most widely used thus far as a primary mediator to regenerate enzymatically active NAD(P)H forms [i.e. 1.4-NAD(P)H] from NAD(P)+ [21,22]. Methyl viologen can also regenerate NAD(P)H from NAD(P)+ as an electron mediator when coupled with redox biocatalysts (e.g. diaphorase, lipoamide dehydrogenase, and ferredoxin-NADP reductase) [23]. www.sciencedirect.com

Nanobiocatalysis for mimicking PS I In the natural PS I, photo-excited P700 transfers electrons to ferredoxin through a series of electron acceptors, such as membrane-bound quinones (e.g. phylloquinone) and four iron-sulfur clusters, which enhance the rate of charge separation. In this regard, proper coupling of a photosensitizer with an electron acceptor is the first step to be considered in the design of PET chain in biocatalytic photosynthesis. Recently, an integrated photosystem was developed by encapsulating porphyrin molecules in the lignocellulosic matrix, which is a composite of cellulose, hemicellulose, and lignin (Figure 3b) [24]. Similarly to the electron transfer by quinones in natural photosynthesis, this artificial photosynthetic wood contains free phenolic groups of lignin that enable reversible protoncoupled, two-electron redox cycling [25]. The local environment of encapsulated porphyrin in the lignocellulosic matrix energetically facilitates efficient charge transfer to an electron mediator (M) for photochemical NADH regeneration and redox enzymatic chemical synthesis. The turnover frequency of LSW was estimated to be approximately 1.25 h1, and the photoenzymatic conversion yield was enhanced as the amount of lignin in the lignocellulosic matrix increased. On the other hand, carbon-based nanomaterials have been employed recently to improve the efficiency of biocatalytic artificial photosynthesis by fast charge separation through the wiring of photosensitizers with electron donors [26]. For example, Choudhury et al. reported the synthesis of a graphenebased photosensitizer by covalently bonding multianthraquinone-substituted porphyrin to graphene sheets for photoenzymatic synthesis of 1-phenylethanols (Figure 3c) [27]. Graphene, a single-layered sheet of sp2-bonded carbon atoms, has a large surface area and high carrier mobility; thus, it can act as an electron reservoir to transport multiple electrons and enhance the PET process [28]. Owing to the facilitated hydride transfer, the graphene-based photosensitizer exhibited high activity in photocatalytic NADH regeneration as well as asymmetric enzymatic reduction of acetophenone derivatives to produce pharmaceutically useful chiral 1phenylethanols. Heterojunction-based nanostructures can also facilitate electron separation and diffusion for artificial photosynthesis in nanobiocatalytic assemblies. Recently, heterojunction-based photoelectrodes comprised of TiO2 nanotubes and CdS quantum dots were developed for visible light-driven cofactor regeneration and redox enzymatic catalysis (Figure 3d) [29]. On the CdS-coated TiO2 nanotubes, photo-excited electrons were rapidly injected from CdS to TiO2 due to the more negative position of the conduction-band edge of CdS than that of TiO2. This injection suppressed electron–hole recombination and accelerated the NADH photo-regeneration rate. In addition, a high aspect ratio of TiO2 nanotubes provided a large surface area for facilitated diffusion of Current Opinion in Biotechnology 2014, 28:1–9

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Figure 3

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(a) Nanobiocatalytic artificial photosynthesis is designed by replacing natural photosynthetic components with man-made OECs, photosensitizers, and electron mediators for visible light-driven cofactor regeneration. (b) Porphyrins encapsulated within a porous lignocellulosic support to serve as light-harvesting pigment [24]. (c) Graphene-based photosensitizer for photoenzymatic synthesis of 1-phenylethanols. Adapted with permission from Ref. [27]; Copyright (2012) Wiley-VCH. (d) Quantum-dot-sensitized TiO2 nanotube arrays for redox enzymatic synthesis coupled with NADH photoregeneration [29]. (e) Peptide self-assembly with porphyrins and further self-metallization with platinum nanoparticles to form photosynthetic nanotubes that can mimic natural PS I [31]. (f) P450-catalyzed O-dealkylation reaction coupled with sustainable NADPH regeneration under visible light [39].

electrons through nanotube channels [30]. The TiO2– CdS nanotubes regenerated NADH at least four times more efficiently than TiO2–CdS nanoparticles because of their directional morphology, enabling better collection and transport of electrons. Current Opinion in Biotechnology 2014, 28:1–9

Efficient light harvesting is another crucial factor to be considered along with proper coupling of photosensitizers and electron acceptors when mimicking a natural PS I system. Kim et al. recently reported that peptide-based nanotubes synthesized through the self-assembly of www.sciencedirect.com

Nanobiocatalytic artificial photosynthesis Kim, Nam and Park 5

diphenylalnine (Phe-Phe, FF) and tetra(p-hydroxyphenyl)porphyrin (THPP) were successfully applied to redox enzymatic reaction that was coupled with visible lightdriven cofactor regeneration (Figure 3e) [31]. The Jaggregates formed by hydrogen bonding and electrostatic interaction of THPP with FF induced exciton coupling between THPP monomers to enhance light-harvesting capacity, similar to LHC in a natural photosystem. Furthermore, platinum nanoparticles (nPt) deposited on FF/THPP nanotubes by self-metallization accelerated the rate of charge separation from the electron donor (triethanolamine) to the electron mediator (M). The enzymatic conversion yield obtained with FF/THPP/ nPt nanotubes was 48.3 and 2.7 times more than that with free THPP monomers and FF/THPP nanotubes, respectively. In a similar way, Tian et al. synthesized platinized porphyrin microstructures by ionic self-assembly of Zn(II) and Sn(IV) derivatives of porphyrins and applied them to hydrogen evolution under visible light [32]. The combination of ZnTPPS and SnT(N-EtOH-4Py)P results in the diffusion-limited crystallization of oppositely charged porphyrins to form four-leaf cloverlike structures in nanoscale. Because of the cooperative interactions between porphyrin subunits, porphyrin microstructures exhibited higher catalytic activity and durability than individual porphyrins. In hydrogen evolution tests, porphyrin microstructures produced approximately five times more H2 than free porphyrins even with a smaller surface area. The final step of PET in biocatalytic artificial photosynthesis is the reduction of chemicals by cofactor-dependent redox enzymes, the artificial dark reaction. While there is a variety of redox enzymes that are capable of accelerating complex synthetic reactions, thus far, rather stable and inexpensive dehydrogenases have been utilized to demonstrate their coupling with visible lightdriven NAD(P)H regeneration [33–36]. Recently, cytochrome P450 monooxygenases have come into the spotlight for artificial photosynthesis because of their unique and versatile catalytic ability in the synthesis of steroids, fatty acids, and vitamins. While cytochrome P450s have extensive potentials in biocatalytic industry and biotechnology, practical applications of P450s have been limited by many problems that include the requirement of expensive nicotinamide cofactors as a reducing equivalent [37,38]. Recently, Lee et al. successfully performed a P450-catalyzed O-dealkylation reaction coupled with NADPH photo-regeneration through mimicking natural photosynthesis (Figure 3f) [39]. In their study, P450 BM3 monooxygenase variant (Y51F/F87A, BM3m2) was used as a model enzyme because of its high catalytic activity, solubility, and ease of expression. Eosin Y was used as an organic photosensitizer to absorb visible light and generate photo-excited electrons, which were transferred to M (i.e. an electron mediator) and the heme domain of P450 via catalyzed NADP+ reduction. The www.sciencedirect.com

production of 7-hydroxycoumarin was proportional to the intensity of incident light; the turnover frequency at 90 mW cm2 was three times higher than that at 15 mW cm2. Furthermore, P450-catalyzed O-dealkylation was significantly accelerated under the illumination of a green LED, indicating that the matching between the absorption spectrum of the photosensitizer and the emission spectrum of the light source is crucial in photoenzymactic reactions.

Nanobiocatalysis for mimicking PS II Organic electron donors, such as triethanloamine, accumulate their oxidized forms as by-products in the reactor during photosynthesis [40]. Many researchers have attempted to use water molecules, which generate only oxygen and protons as an electron donor — as occurs in the natural PS II — by developing various water oxidation catalysts (e.g. metal oxides; namely, IrO2, Fe2O3, CaMn2O4, and molecular catalysts containing metal ions such as ruthenium, cobalt, iridium, and manganese) [41–44]. Ideally, artificial photosynthesis should occur through two half-reactions consisting of water oxidation and reduction, both of which require the transportation of multiple electrons and protons, making efficient transfer of photo-excited electrons difficult [45]. From an electrochemical point of view, multiple electrons and protons can be simultaneously transferred from anode to cathode; by contrast, electron transfer in a photochemical system is triggered by a photosensitizer upon the absorption of a single photon. The rate of one-electron transfer from OEC to the reaction center via photosensitizer is closely related to the efficiency of water splitting under visible light. In nature, PS II has two redox active amino acids, such as tyrosine and histidine, which assist in the transfer of electrons and protons from CaMn4O5 to photo-excited P680 through deprotonation and protonation of the phenyl and imidazole groups of tyrosine and histidine [46,47]. Furthermore, the LHC is closely assembled with OEC to enhance the quantum efficiency of natural photosynthesis. The increased efficiency of water oxidation by tyrosine and histidine in natural PS II inspired researchers to explore novel redox mediators to enhance the water oxidation process. For example, Zhao et al. synthesized benzimidazole-phenol (BIP) ligands that were covalently bound to OEC (e.g. IrO2 nanoparticles) for efficient electron transfer to ruthenium polypyridyl sensitizer (Figure 4a) [48]. While the quantum yield of photoelectrochemical water oxidation by dye-sensitized photoelectrodes had been quite low due to the rapid rate of charge recombination [49], the BIP-functionalized IrO2 nanoparticles accelerated the rate of electron injection from IrO2 to a ruthenium polypyridyl sensitizer. The quantum yield of the BIP-modified photoanode was more than double that of the photoanode without BIP. Similarly, the incorporation of Ru(bipyridine), a redox Current Opinion in Biotechnology 2014, 28:1–9

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Figure 4

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Nanobiocatalytic assemblies for mimicking PS II. (a) Molecular arrangement of BIP-modified IrO2 nanoparticles and Ru(bpy)32+ in dye-sensitized TiO2 with photoanode. Adapted with permission from Ref. [48]; Copyright (2012) National Academy of Sciences, USA. (b) M13 virus-templated assembly of porphyrins for the fabrication of light-harvesting nanoantenna. Adapted with permission from Ref. [51]; Copyright (2010) American Chemical Society. (c) Structure and mechanism of Pt, Co, and TiO2-decorated Au nanorod for solar water splitting. Adapted with permission from Ref. [54]; Copyright (2013) Nature Publishing Group.

mediator, into Ru(terpyridine), an OEC, via bipyrimidine resulted in a high turnover number (28 000) and 95% Faradaic efficiency because of the efficiency of the electron transfer by the redox mediator [50]. Recently, M13 viruses were utilized as a novel template to mimic natural LHC for efficient photochemical water oxidation (Figure 4b) [51,52]. In the work, porphyrin photosensitizers were covalently attached to the primary amine group of lysine on the surface of the M13 viruses. An enhanced energy transfer phenomenon was observed with the porphyrin-assembled virus nanowires, which Current Opinion in Biotechnology 2014, 28:1–9

originated from the precise arrangement of porphyrin molecules due to the regular distance between lysine sites on M13 virus. When assembled with IrO2 nanoparticles, the porphyrin-M13 nanowires further enhanced the turnover number (796) of water oxidation due to the close arrangement of each component. Enhanced water oxidation by the creation of an artificial LHCincorporated photosystem was also demonstrated by the application of light-harvesting cross-linked polymer (CP) through the polymerization of tetrahedral tetra(pethynylphenyl)-methane with Ru(bpy)32+ for Sonogashira cross-coupling reactions (e.g. aza-Henry reaction, www.sciencedirect.com

Nanobiocatalytic artificial photosynthesis Kim, Nam and Park 7

aerobic amine coupling, and dehalogenation of benzyl bromoacetate) under visible light [53]. Despite the nonporous nature of Ru(bpy)32+-CP, its catalytic activity on aza-Henry reactions was much higher than that of free Ru(bpy)32+ due to efficient light-harvesting through the interaction between the excited states of Ru(bpy)32+ in CP, as with natural LHC. Recently, Mubeen et al. developed heterogeneous photosystem on an Au nanorod array using alumina templates for visible light-driven hydrogen evolution coupled with water oxidation (Figure 4c) [54]. The Au nanorod array was incorporated with TiO2, Pt, and Co to generate electron–hole pairs under visible light in which Pt and Co played the role of hydrogen and oxygen evolution center, respectively. The incorporation of TiO2, Pt and Co on the Au nanorod array could drive the forward electron transfer and enable long-term operationality.

Conclusion The goal of biocatalyzed artificial photosynthesis is to store solar energy in chemicals using nanobiocatalytic assemblies that can perform redox biocatalysis and photocatalysis under visible light. The design of nanobiocatalytic assemblies that mimic natural PS I and II is a promising strategy to improve the efficiency of PET and the yield of redox enzymatic reactions. While many opportunities exist for nanobiocatalytic artificial photosynthesis in the future, crucial challenges still remain to be resolved for their practical applications, which include the synthesis of more efficient water oxidation catalysts and electron mediators, the design of robust light-harvesting assemblies, direct injection of photo-excited electrons into enzymatic redox centers, the application of a wider spectrum of redox biocatalysts (e.g. monooxygenases, CO2 fixing enzymes) to artificial photosynthesis, and nanoscale assemblies of artificial PS I and II systems. Several different types of nanobiocatalytic assemblies have been recently reported for artificial photosynthesis as described in this review, but most of them are applied to the half reaction of photosynthesis. In particular, sustainable and efficient water oxidation is needed to supply electrons to reaction center for redox enzymatic reaction without accumulating oxidized organic electron donors in the reactor. Currently, research works are undergoing to accelerate PET while using water as an electron donor through the modification of electron mediators and their hybridization with conducting materials. In case of photochemical NADH regeneration using eosin Y and carbon nitride, quantum efficiency is approximately 3.5% and 0.52%, respectively [55,56]. For the achievement of higher quantum efficiency, a precise arrangement and coordination between key photosynthetic components, such as electron donors, photosensitizers, and electron mediators, is required to advance multi-step PET without backward electron transfer and charge recombination. Direct injection of photo-induced electrons to the redox center of oxidoreductases without the use of electron mediators can be another solution to simplify complex www.sciencedirect.com

steps of PET process. Regarding the utilization of various redox enzymes, one of major challenges is the construction of efficient biocatalytic system that can produce methanol from CO2 using solar energy. This can be achieved by precisely positioning three NADH-dependent enzymes (firstly, formate dehydrogenase for CO2 ! formate; secondly, formaldehyde dehydrogenase for formate ! formaldehyde; thirdly, alcohol dehydrogenase for formaldehyde ! methanol) on nanoscale scaffolds for efficient and forward cascaded reactions through solar light-driven NADH regeneration. At the present time, it is crucially needed to screen robust formate dehydrogenase that can accelerate CO2 reduction since most formate dehydrogenases in nature favor the oxidation of formate. Overall, such achievements will help solve global energy and environmental problems, hopefully in a decade, toward the realization of biocatalyzed artificial photosynthesis.

Acknowledgements CBP appreciates the support of the National Leading Research Laboratory (NRF-2013R1A2A1A05005468), the Intelligent Synthetic Biology Center of Global Frontier R&D Program (2011-0031957), and the Converging Research Center (2009-0082276) funded by the National Research Foundation, Korea.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of outstanding interest 1.

Lewis NS, Nocera DG: Powering the planet: chemical challenges in solar energy utilization. Proc Natl Acad Sci U S A 2006, 103:15729-15735.

2.

Tachibana Y, Vayssieres L, Durrant JR: Artificial photosynthesis for solar water-splitting. Nat Photon 2012, 6:511-518.

3.

Balzani V, Credi A, Venturi M: Photochemical conversion of solar energy. ChemSusChem 2008, 1:26-58.

4.

Benniston AC, Harriman A: Artificial photosynthesis. Mater Today 2008, 11:26-34.

5.

Izumi Y: Recent advances in the photocatalytic conversion of carbon dioxide to fuels with water and/or hydrogen using solar energy and beyond. Coord Chem Rev 2013, 257:171-186.

6.

Li Q, Guo B, Yu J, Ran J, Zhang B, Yan H, Gong JR: Highly efficient visible-light-driven photocatalytic hydrogen production of CdS-cluster-decorated graphene nanosheets. J Am Chem Soc 2011, 133:10878-10884.

7.

Huang J, Mulfort KL, Du P, Chen LX: Photodriven charge separation dynamics in CdSe/ZnS core/shell quantum dot/ cobaloxime hybrid for efficient hydrogen production. J Am Chem Soc 2012, 134:16472-16475.

8.

Gust D, Moore TA, Moore AL: Solar fuels via artificial photosynthesis. Acc Chem Res 2009, 42:1890-1898.

9.

Obert R, Dave BC: Enzymatic conversion of carbon dioxide to methanol: enhanced methanol production in silica sol-gel matrices. J Am Chem Soc 1999, 121:12192-12193.

10. Schmid A, Dordick JS, Hauer B, Kiener A, Wubbolts M, Witholt B: Industrial biocatalysis today and tomorrow. Nature 2001, 409:258-268. 11. Hall M, Bommarius AS: Enantioenriched compounds via enzyme-catalyzed redox reactions. Chem Rev 2011, 111: 4088-4110. Current Opinion in Biotechnology 2014, 28:1–9

8 Nanobiotechnology

12. Hollmann F, Arends IWCE, Holtmann D: Enzymatic reductions for the chemist. Green Chem 2011, 13:2285-2314. 13. Hollmann F, Arends IWCE, Buehler K, Schallmey A, Buhler B: Enzyme-mediated oxidations for the chemist. Green Chem 2011, 13:226-265. 14. Hohmann-Marriott MF, Blankenship RE: Evolution of photosynthesis. Ann Rev Plant Biol 2011, 62:515-548. 15. Vinyard DJ, Ananyev GM, Charles Dismukes G: Photosystem II: the reaction center of oxygenic photosynthesis. Ann Rev Biochem 2013, 82:577-606.

31. Kim JH, Lee M, Lee JS, Park CB: Self-assembled light harvesting peptide nanotubes for mimicking natural photosynthesis. Angew Chem Int Ed 2012, 51:517-520. The authors proposed photochemical cofactor regeneration using lightharvesting nanotubes synthesized through self-assembly of peptides with photosensitizers for mimicking natural photosystem I. 32. Tian YM, Martin KE, Shelnutt JYT, Evans L, Busani T, Miller JE, Medforth CJ, Shelnutt JA: Morphological families of selfassembled porphyrin structures and their photosensitization of hydrogen generation. Chem Commun 2011, 47:6069-6071.

16. Herek JL, Wohlleben W, Cogdell RJ, Zeidler D, Motzkus M: Quantum control of energy flow in light harvesting. Nature 2002, 417:533-535.

33. Lavandera In, Kern A, Resch V, Ferreira-Silva B, Glieder A, Fabian WMF, de Wildeman S, Kroutil W: One-way biohydrogen transfer for oxidation of sec-alcohols. Org Lett 2008, 10:2155-2158.

17. Umena Y, Kawakami K, Shen JR, Kamiya N: Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A˚. Nature 2011, 473:55-60.

34. Lee HY, Kim JH, Son EJ, Park CB: Silicon nanowires as a rechargeable template for hydride transfer in redox biocatalysis. Nanoscale 2012, 4:7636-7640.

18. Song WJ, Chen ZF, Brennaman MK, Concepcion JJ, Patrocinio AOT, Iha NYM, Meyer TJ: Making solar fuels by artificial photosynthesis. Pure Appl Chem 2011, 83:749-768.

35. Nam DH, Park CB: Visible light-driven NADH regeneration sensitized by proflavine for biocatalysis. ChemBioChem 2012, 13:1278-1282.

19. Frischmann PD, Mahata K, Wurthner F: Powering the future of molecular artificial photosynthesis with light-harvesting metallosupramolecular dye assemblies. Chem Soc Rev 2013, 42:1847-1870.

36. Todd King M: Thermodynamics of the reduction of NADP with 2-propanol catalyzed by an NADP-dependent alcohol dehydrogenase. Arch Biochem Biophys 2003, 410:280-286.

20. Mcdermott G, Prince SM, Freer AA, Hawthornthwaitelawless AM, Papiz MZ, Cogdell RJ, Isaacs NW: Crystal-structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 1995, 374:517-521. 21. Hollmann F, Witholt B, Schmid A: [CpRh(bpy)(H2O)]2+: a versatile tool for efficient and non-enzymatic regeneration of nicotinamide and flavin coenzymes. J Mol Catal B: Enzym 2002, 19–20:167-176. 22. Lo HC, Leiva C, Buriez O, Kerr JB, Olmstead MM, Fish RH: Bioorganometallic chemistry, 13. Regioselective reduction of NAD+ models, 1-benzylnicotinamde triflate and bnicotinamide ribose-50 -methyl phosphate, with in situ generated [Cp*Rh(Bpy)H]+: structure–activity relationships, kinetics, and mechanistic aspects in the formation of the 1,4NADH derivatives. Inorg Chem 2001, 40:6705-6716. 23. Mandler D, Willner I: Photoinduced enzyme-catalyzed synthesis of amino-acids by visible-light. J Chem Soc Chem Commun 1986:851-853. 24. Lee M, Kim JH, Lee SH, Lee SH, Park CB: Biomimetic artificial photosynthesis by light-harvesting synthetic wood. ChemSusChem 2011, 4:581-586. 25. Milczarek G: Preparation and characterization of a lignin modified electrode. Electroanalysis 2007, 19:1411-1414. 26. Toma FM, Sartorel A, Iurlo M, Carraro M, Parisse P, Maccato C, Rapino S, Gonzalez BR, Amenitsch H, Da Ros T et al.: Efficient water oxidation at carbon nanotube-polyoxometalate electrocatalytic interfaces. Nat Chem 2010, 2:826-831. 27. Choudhury S, Baeg J-O, Park N-J, Yadav RK: A photocatalyst/ rnzyme couple that uses solar energy in the asymmetric reduction of acetophenones. Angew Chemie Int Ed 2012, 124:11792-11796. 28. Yadav RK, Baeg JO, Oh GH, Park NJ, Kong KJ, Kim J, Hwang DW,  Biswas SK: A photocatalyst-enzyme coupled artificial photosynthesis system for solar energy in production of formic acid from CO2. J Am Chem Soc 2012, 134:11455-11461. This report describes carbon dioxide fixation via biocatalyzed artificial photosynthesis that utilizes graphene-based nanomaterials. 29. Ryu J, Lee SH, Nam DH, Park CB: Rational design and  engineering of quantum-dot-sensitized TiO2 nanotube arrays for artificial photosynthesis. Adv Mater 2011, 23:1883-1888. First report on biocatalyzed artificial photosynthesis using integrated photo-electrodes such as CdS-incorporated TiO2 nanotube arrays. 30. Shankar K, Basham JI, Allam NK, Varghese OK, Mor GK, Feng XJ, Paulose M, Seabold JA, Choi KS, Grimes CA: Recent advances in the use of TiO2 nanotube and nanowire arrays for oxidative photoelectrochemistry. J Phys Chem C 2009, 113:6327-6359. Current Opinion in Biotechnology 2014, 28:1–9

37. Zanger UM, Schwab M: Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther 2013, 138:103-141. 38. O’Reilly E, Kohler V, Flitsch SL, Turner NJ: Cytochromes P450 as  useful biocatalysts: addressing the limitations. Chem Commun 2011, 47:2490-2501. Great review on the potential of cytochrome P450 for the catalysis of regiospecific and stereospecific oxidation of hydrocarbons. 39. Lee SH, Kwon Y-C, Kim D-M, Park CB: Cytochrome P450 catalyzed O-dealkylation coupled with photochemical NADPH regeneration. Biotechnol Bioeng 2013, 110:383-390. First application of visible light-driven cofactor regeneration to cytochrome P450 catalysis. 40. Teoh WY, Scott JA, Amal R: Progress in heterogeneous photocatalysis: from classical radical chemistry to engineering nanomaterials and solar reactors. J Phys Chem Lett 2012, 3:629-639. 41. Yin QS, Tan JM, Besson C, Geletii YV, Musaev DG, Kuznetsov AE, Luo Z, Hardcastle KI, Hill CL: A fast soluble carbon-free molecular water oxidation catalyst based on abundant metals. Science 2010, 328:342-345. 42. Najafpour MM, Ehrenberg T, Wiechen M, Kurz P: Calcium manganese(III) oxides (CaMn2O4xH2O) as biomimetic oxygenevolving catalysts. Angew Chem Int Ed 2010, 49:2233-2237. 43. Harriman A, Nahor GS, Mosseri S, Neta P: Iridium oxide hydrosols as catalysts for the decay of zinc porphyrin radical cations in water. J Chem Soc Faraday Trans 1 1988, 84:2821-2829. 44. Osterloh FE: Inorganic nanostructures for photoelectrochemical and photocatalytic water splitting. Chem Soc Rev 2013, 42:2294-2320. 45. Inoue H, Shimada T, Kou Y, Nabetani Y, Masui D, Takagi S, Tachibana H: The water oxidation bottleneck in artificial photosynthesis: how can we get through it? An alternative route involving a two-electron process. ChemSusChem 2011, 4:173-179. 46. Keough JM, Jenson DL, Zuniga AN, Barry BA: Proton coupled electron transfer and redox-active tyrosine Z in the photosynthetic oxygen-evolving complex. J Am Chem Soc 2011, 133:11084-11087. 47. Barry BA: Proton coupled electron transfer and redox active tyrosines in photosystem II. J Photochem Photobiol B 2011, 104:60-71. 48. Zhao YX, Swierk JR, Megiatto JD, Sherman B, Youngblood WJ, Qin DD, Lentz DM, Moore AL, Moore TA, Gust D et al.: Improving www.sciencedirect.com

Nanobiocatalytic artificial photosynthesis Kim, Nam and Park 9

the efficiency of water splitting in dye-sensitized solar cells by using a biomimetic electron transfer mediator. Proc Natl Acad Sci U S A 2012, 109:15612-15616. 49. Abe R: Recent progress on photocatalytic and photoelectrochemical water splitting under visible light irradiation. J Photochem Photobiol C 2010, 11:179-209. 50. Concepcion JJ, Jurss JW, Hoertz PG, Meyer TJ: Catalytic and surface-electrocatalytic water oxidation by redox mediator–catalyst assemblies. Angew Chem Int Ed 2009, 48:9473-9476. 51. Nam YS, Shin T, Park H, Magyar AP, Choi K, Fantner G,  Nelson KA, Belcher AM: Virus-templated assembly of porphyrins into light-harvesting nanoantennae. J Am Chem Soc 2010, 132:1462-1463. An innovative approach to integrate porphyrin molecules at controlled sites in M13-virus nanowires for the synthesis of efficient light-harvesting materials.

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52. Nam YS, Magyar AP, Lee D, Kim J-W, Yun DS, Park H, Pollom TS, Weitz DA, Belcher AM: Biologically templated photocatalytic nanostructures for sustained light-driven water oxidation. Nat Nanotechnol 2010, 5:340-344. 53. Wang C, Xie Z, deKrafft KE, Lin W: Light-harvesting cross-linked polymers for efficient heterogeneous photocatalysis. ACS Appl Mater Interfaces 2012, 4:2288-2294. 54. Mubeen S, Lee J, Singh N, Kramer S, Stucky GD, Moskovits M: An autonomous photosynthetic device in which all charge carriers derive from surface plasmons. Nat Nano 2013, 8:247-251. 55. Lee SH, Lee HJ, Won K, Park CB: Artificial electron carriers for photoenzymatic synthesis under visible light. Chem Eur J 2012, 18:5490-5495. 56. Liu J, Antonietti M: Bio-inspired NADH regeneration by carbon nitride photocatalysis using diatom templates. Energy Environ Sci 2013, 6:1486-1493.

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