Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters

Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters Volume 1 photovoltaic solar energy 1 31 – artificial leaves towards bio inspired solar energy converters

1.31 Artificial Leaves: Towards Bio-Inspired Solar Energy Converters A Pandit and RN Frese, VU University Amsterdam, Amsterdam, The Netherlands © 2012 Elsevier Ltd All rights reserved 1.31.1 1.31.1.1 1.31.1.2 1.31.1.3 1.31.1.3.1 1.31.1.3.2 1.31.1.3.3 1.31.1.3.4 1.31.2 1.31.2.1 1.31.2.1.1 1.31.2.1.2 1.31.2.1.3 1.31.2.2 1.31.3 1.31.3.1 1.31.3.2 1.31.3.3 1.31.3.3.1 1.31.3.4 1.31.3.4.1 1.31.4 References Further reading The Design of Natural Photosynthesis Photosynthetic Light-Harvesting Antennae Photosynthetic RCs Supramolecular Organization Supercomplexes Supramolecular complexes Membranes Light harvesting and charge transport in purple bacteria Design Principles of Natural Photosynthesis Photon Absorption, Excitation Energy Transfer, and Electron Transfer Photon absorption Excitation energy transfer Electron transfer Photochemical Thermodynamics of Energy Storage The Design of an Artificial Leaf Interfacing Proteins onto Solid-State Surfaces Protein Maquettes for Artificial Photosynthesis Bio-Inspired Self-assembled Artificial Antennae Chlorosome-based, light-harvesting antennae Bio-Inspired DA Constructs Self-assembled DA constructs Outlook: The Construction of a Fuel-Producing Solar Cell Glossary ATP Adenosine-5′-triphosphate, a nucleotide used in cells as a coenzyme and energy carrier (Bacterio) pheophytin A (bacterio) chlorophyll from which the central magnesium atom has been removed Carbohydrates Literally ‘hydrates of carbon’, chemical compounds that act as the primary biological means of storing or consuming energy; other forms being via fat and protein Relatively complex carbohydrates are known as ‘polysaccharides’ Carotenoid Tetraterpenoid organic pigment; carotenoids are divided into xanthophylls (containing oxygen) and carotenes (purely hydrocarbons) Chlorophyll (Chl) Green photosynthetic pigment found in plants, algae, and cyanobacteria Chloroplast Organelles found in plant cells and eukaryotic algae that conduct photosynthesis 657 658 659 660 660 661 661 661 663 663 663 664 664 664 666 666 667 669 669 670 672 674 675 677 Chloroplasts capture light energy from the sun to produce the free energy stored in ATP and NADPH Exciton (photosynthetic) Electronically excited state of a pigment molecule in a photosynthetic system Depending on various parameters, the degree of exciton delocalization can vary from one pigment to many pigment molecules NADPH Nicotinamide adenine dinucleotide phosphate, used as reducing power for biosynthetic reactions in photosynthesis Porphyrin Pigment consisting of a heterocyclic macrocycle made from four pyrrole subunits If one of the three pyrrole subunits is reduced to pyrroline, chlorine is produced, the ring structure found in chlorophyll Quinone (photosynthetic) Mobile, lipid-soluble carriers that shuttle electrons and protons between protein complexes embedded in the membrane 1.31.1 The Design of Natural Photosynthesis Photosynthetic organisms are ubiquitous on the surface of the Earth and, in fact, responsible for the development and sustenance of all life on the planet They all use the same basic pattern whereby light energy from the sun is initially absorbed and concentrated by an antenna system, then transferred to a reaction center (RC) where charge separation takes place, followed by reactions that convert the captured light energy into a chemical form Photosynthesis can be divided into oxygenic photosynthesis, carried out by Comprehensive Renewable Energy, Volume doi:10.1016/B978-0-08-087872-0.00135-9 657 658 Technology ADP H+ Q/QH2/Q hν ATP Cytoplasm ATPase bc1 RC LH-II LH-I e− Cytochrome c2 Periplasm H + Figure Schematic view of the purple bacterial photosynthetic membrane Several components transform the incoming energy of photons LH2 and LH1 are LHCs that absorb light and transfer excited-state energy among intra- and intercomplex bound pigments The terminal acceptor is the RC, which is completely encircled by the LH1 complex There the excited-state energy induced ETs among cofactors until two electrons reside on the terminal acceptor, which is a quinone molecule This molecule becomes double protonated upon which it exits the complex into the lipid phase of the membrane, diffusing toward a proton-translocating pump, the bc1 complex A small protein cytochrome c shuttles between the bc1 complex and the RC to re-reduce the primary electron donor, thus closing the circuit When protons are actively transported back from the periplasm to the cytoplasm through the ATP synthase complex, the energy is chemically stored as ATP Reproduced from Figure in Hu XC, Damjanovic A, Ritz T, and Schulten K (1998) Architecture and mechanism of the light-harvesting apparatus of purple bacteria Proceedings of the National Academy of Sciences of the United States of America 95: 5935–5941 [1], with permission of National Academy of Sciences USA cyanobacteria, algae, and plants that produce oxygen, and nonoxygenic photosynthesis, carried out by purple, green sulfur, and heliobacteria Oxygenic organisms harness solar energy to extract the H+ and e− from H2O, required for CO2 fixation Nonoxygenic organisms cannot generate the necessary oxidizing potential to oxidize H2O and therefore extract H+ and e− from alternative substrates Under normal conditions, both processes use the derived H+ and e− for synthesis of adenosine triphosphate (ATP), nicotinamide adenine dinucleotide phosphate (NADPH) oxidase, and ultimately CO2 fixation, and to produce carbohydrates such as starch and glycogen, which can be considered to be H+ and e− ‘stores’ that can be used for the CO2 neutral production of fuels; see Figure for a schematic representation of nonoxygenic photosynthesis The factory where the photosynthetic process takes place is the cell, or a specialized compartment within the cell Each reaction is carried out by specific proteins or complexes of proteins that often bind functional molecules for light absorption, redox chemistry, and charge transfer Proteins are nanometric-sized biopo­ lymers of specific shape and function, and are dynamically organized within, or associated with, a lipid membrane Membranes allow the compartmentalization of the various reactions and are especially important for ATP formation, which is driven by the electrochemical gradient formed by the protons that are pumped across the membrane and enable the synthesis of ATP during controlled back transfer through the ATP synthase enzyme 1.31.1.1 Photosynthetic Light-Harvesting Antennae Natural light-harvesting antenna complexes (LHCs) are complexes of proteins that are organized to collect and deliver light excited-state energy to the RC where charge separation takes place [2] They permit an organism to increase greatly the absorption cross section for light without having to build an entire RC and associated electron-transfer (ET) system for each pigment, which would be very costly in terms of biosynthesis and cellular resources The intensity of sunlight is dilute so that any given pigment molecule absorbs at most a few photons per second By incorporating many pigments into a single antenna unit and creating supramolecular assemblies of antenna units, large photosynthetic membrane surfaces are covered, ensuring that photons striking any spot on the surface will be absorbed The antenna units are interconnected to carry light energy through exciton migration over long distances to the RCs They surround the RCs, optimizing the energy-transfer efficiency by multiple antenna–RC connections Photosynthetic organisms are equipped with a light-harvesting antenna containing the pigments (bacterio) chlorophylls ((B)Chl), carotenoids (Cars), or phycobilins While they share their function of funneling the excitation energy into the RC, there is a large variety in the antenna structures and macro-organization of different species Most organisms have antenna systems that are embedded in the photosynthetic membrane, but green sulfur bacteria and cyanobacteria contain aggregated antenna structures that are associated with the membrane Green sulfur bacteria contain antennae built from large 3D tubular aggregates of self-assembled (B)Chls with small amounts of Cars and quinones, contained in specialized vesicles called chlorosomes [3] (see Figure 2) The energy harvested by these chlorosomes is transferred via a protein called the Fenna–Mathews–Olson (FMO) complex to the membrane-bound RC The light-harvesting antenna of green sulfur bacteria is designed to operate at extremely low light intensities and therefore is extremely large compared to the antennae of other species This is the only species in which the antenna structures are self-assembled from pigment molecules without the aid of a protein environment Cyanobacteria use rod-like antenna structures called phycobilisomes [5], containing protein assemblies in which the proteins have prosthetic groups of linear pyrroles, the phycobilin pigments The phycobilisomes are associated with the photosynthetic membranes and transfer their excitation energy to two photosystems that are embedded in the membrane: photosystem (PS1) and photosystem (PS2) that contain the RCs This is the only species in which its antenna pigments are covalently bound to proteins Structure–function features are summarized here that are shared among different species Tightly coupled (B)Chls allow efficient energy transfer via excitonic interactions The combination of Cars in van der Waals contact with the (B)Chls allows efficient and rapid energy transfer from the Cars (absorbing in the blue-green region of the solar spectrum) to the (B)Chls that absorb in the red Artificial Leaves: Towards Bio-Inspired Solar Energy Converters (a) 659 (b) Chlorosome LH1 Reaction center LH2 Reaction center Phycobilisome (d) (c) Photosystem II LHCII Photosystem II TRENDS in Plant Science Figure Schematic view of the organization of antenna–RC complexes of different organisms: (a) light-harvesting complex (LH2) and light-harvesting complex 1–RC (LH1–RC) complexes of purple nonsulfur bacteria, (b) chlorosome antenna of green sulfur bacteria, (c) phycobilisome antenna of cyanobacteria, and (d) light-harvesting complex II (LHCII) antenna attached to photosystem in plants Reproduced from Figure in Mullineaux CW (2005) Function and evolution of grana Trends in Plant Science 10: 521–525 [4], with permission of Elsevier Science B.V or infrared region, covering a larger part of the solar spectrum The Cars also protect the organism from photo-oxidative damage by rapidly quenching potentially harmful (B)Chl triplet states that can produce singlet oxygen Pigment–protein and pigment– pigment interactions within the antennae broaden the lowest excited-state absorption spectrum (increasing the cross section for light absorption) and tune the absorption maxima of the different pigments, resulting in light energy transfer to the ‘reddest’ pigment with the lowest excited-state energy The arrangements of the antenna complexes are such that light energy can migrate among the complexes via Förster energy transfer and that the antennae surround the RC so that light energy migration is funneled into the RCs from different sites 1.31.1.2 Photosynthetic RCs RCs are complexes of proteins with embedded cofactors that act simultaneously as chromophores, redox groups, and ET factors; see Reference and Figure for a detailed description of the structural and functional characteristics of RCs In RCs, the excited-state energy generated by photon absorption is utilized for the release of electrons after which energy back transfer has become impossible ETs are directional among the cofactors and are accompanied by a loss of free energy that ensures a fast-forward and slow-backward transfer rate The primary electron donor and the terminal acceptor are separated in space close to either side of a membrane where they are coupled to other proteins or molecules via redox chemistry; at that point, the energy is stored [8] As such, RCs can carry out the primary photochemical reactions without the need of LHCs discussed in the previous section While Nature has developed a large variety of LHCs among the species [9], RCs have remained surprisingly homologous throughout billions of years of evolution This may be a reflection of the much more stringent design principles for ET compared to energy transfer, for instance, the distance dependency of the rates All RCs contain dimers of proteins that covalently link the cofactors Attached to the protein dimers are other proteins enabling redox chemistry via again other proteins or redox molecules Differentiations between the species regarding the RCs are the type of chromophores used, the wavelengths of absorption, the redox potential between first electron donor and final acceptor, and the redox reactions leading to re-reduction of the primary donor and the re-oxidation of the terminal acceptor [10] In Figure 4, the redox potentials of the components active in ETs within the four types of RCs are depicted Two types are found in anoxygenic photosynthesis, which are the evolutionary precursors of the other two oxygenic types The latter are part of the photosystem and supercomplexes (PS1 and PS2) that are coupled systems allowing the formation of NADPH When the need for NADPH is low, PS1 and PS2 can become uncoupled and ATP is produced by cyclic electron transport, similar to the process in purple bacterial RCs As can be seen in Figure 4, there is a common theme among all types of RCs regarding the redox potential generated after the initial electron donors (P870, P680, P700, or P840) have been excited (indicated by P*) Light energy is used to promote the primary electron donors to a redox state that is more negative than the subsequent electron acceptors, thus promoting electro­ chemically downhill ETs A most striking difference between the primary donor of photosystem and that of the other RCs is the extremely large redox potential of P680, +1.2 V versus standard hydrogen electrode; it can oxidize water into protons and oxygen [12] 660 Technology Q side H-polypeptide (b) (a) QB quinone QA quinone Q side Fe HA BPhe M-polypeptide L-polypeptide Symmetry axis Q QH2 HB BPhe BA BChl BB BChl PA BChl PB BChl P side P side (d) RC H Q side LH1 α LH1 β LH1 BChls Absorbance (c) RC HA/HB RC BA/BB RC-LH1 HA/HB BA/BB P RC C RC L P side RC M 700 800 Wavelength (nm) 900 Figure (a) Overall structure The protein surface shown as a semitransparent object with the backbone fold of the H, L, and M polypeptides shown as white, green, and yellow tubes, respectively The approximate position of the membrane is shown as a gray box, with the primary donor side (P side) and quinone side (Q side) of the RC labeled The embedded cofactors are shown as sticks, with the Car (bottom left) shown with teal carbons (b) Enlarged view of the BChl, BPhe, and quinone cofactors, color coded as in (a) with oxygens in red, nitrogens in blue, and Fe and Mg atoms in brown or magenta spheres Membrane-spanning ET starts from the primary donor pair of BChls (PA/PB – pink carbons) and proceeds via the BA BChl (green carbons), HA BPhe (yellow carbons), and QA ubiquinone (cyan carbons) Electrons are passed on to the dissociable QB ubiquinone (cyan carbons), which can exchange with exogenous ubiquinone The BB BChl and HB BPhe not participate in ET For clarity, the large hydrocarbon side chains of the BChl, BPhe, and quinone cofactors are not shown (c) Structure of the RC–LH1 complex from Rhodopseudomonas palustris [7]; Protein DataBank (PDB) entry 1PYH – resolution 0.48 nm The central RC, colored as for (a) and viewed from the same direction, is surrounded by concentric cylinders of multiple copies of α (cyan ribbons) and β (magenta ribbons) polypeptides, sandwiching a ring of BChls (colored alternately red and orange) (d) Absorbance spectra of the Rhodobacter sphaeroides RC and the Rhodopseudomonas acidophila RC–LH1, showing band attributions Note the real contribution of the RC pigments to the absorbance of RC–LH1 complexes can be viewed in the RC–LH1 spectrum at 800 and 750 nm (Ba/Bb and Ha/Hb pigments, respectively) Structure and pigment organization in the photosynthetic RC of purple bacteria Courtesy of Prof Michael Jones, Sheffield University In fact, only P680 possesses a redox potential higher than the constituent Chl molecules [13] The high redox potential of P680 is most likely a result of an intricate combination of various protein–Chl interactions such as hydrogen bonds, protein charges, and dielectric shielding [14] As will be discussed in Section 1.31.4, the utilization of photon energy to split water into protons and oxygen has yet to be accomplished by a man-made catalyst In fact, since protons can be redirected to form molecular hydrogen or other energy-rich compounds, PS2 mimics can be regarded as the Holy Grail in artificial photosynthesis 1.31.1.3 1.31.1.3.1 Supramolecular Organization Supercomplexes As discussed in the previous sections, photosynthesis combines complexes of proteins for light-absorbing and ETs in combination with charge carriers and proton pumps The RCs are always associated with some specific LHCs forming an RC–LHC core complex, a unit very well capable of performing primary photochemistry But because of the dim- or low-light conditions within their environment, almost all species also synthesize extra LHCs that surround the core complexes [9] In plants, PS1 [15] and PS2 Artificial Leaves: Towards Bio-Inspired Solar Energy Converters Type I reaction center Iron−Sulfur Type II reaction center Pheophytin−quinone Purple bacteria and green filamentous bacteria 661 Photosystem I Photosystem II Green sulfur bacteria and heliobacteria −1.5 P700* Em (V) −1.0 BChl BPh −0.5 0.0 P680* Ph QA hν QB QB (Mn)4 A0 A1 FX FAFB hν NADP cyt c Pc P870 H2O 1.0 P840* NADP cyt bc1 cyt bf hν cyt c 0.5 hν QA cyt bc1 A0 A1 FX FAFB P870* P840 (P800) P700 TyTz P680 Figure Diagrams of ET chains within the four types of RCs found in photosynthesis The left axis shows the approximate redox potentials of the cofactors The initial electron donors are indicated by their wavelength of absorption P870, P680, P700, and P840 Reprinted from Figure in Hillier W and Babcock GT (2001) Photosynthetic reaction centers Plant Physiology 125: 33–37 [11], with permission of American Society of Plant Physiologists [16] are large photosystems consisting of RCs linked to a variable set of LHCs In purple bacteria, the core complex is an RC surrounded by an LHC consisting of a ring of proteins [7] This core complex can form dimers with another, similar, core complex, which in turn may be surrounded by other smaller ring-like LHCs [17] 1.31.1.3.2 Supramolecular complexes Recent advances in electron microscopy [18] and atomic force microscopy [19] have shown the existence of a distinct spatial organization of the photosynthetic components within the membranes In plants, PS1 and PS2 are well separated in different membranous compartments accompanied by cytochrome b6f and ATP synthase complexes, respectively [20] Among the purple bacteria, a large variety have been found in domain formation of RC–LHC core complexes and the peripheral LHCs [21] Moreover, the supramolecular organization has been found to be dependent on the light conditions [22] Most strikingly, the photosynthetic membranes are heavily packed with RCs and LHCs, much like a 2D crystal, which places much strain on diffusive processes [23] While distinct supramolecular organizations exist, there is no underlying structure holding the components in place Therefore, a thermodynamic model has been derived showing that entropy can be a driving force for domain formation of RCs and LHCs (see Reference 24 and Figure 5) Due to heavy packing, the clustering of larger photosystems, separated from the smaller LHCs, enhances the volume that can be occupied by the LHCs such that the total entropy is actually maximized This effect has been shown for colloidal particles before and may be generalized for the nanometric-sized protein complexes as well The more fluid domain of smaller LHCs may also enable diffusive pathways necessary for self-repair and adaptability The model predicts how different supramolecular organizations may be inferred by specific tuning the size and shape of the components Due to packing, also the ultrastructure of the entire photosynthetic membrane can be predicted from the same self-organizing principles [24] 1.31.1.3.3 Membranes The membrane in which the photosynthetic complexes primarily reside is a two-dimensional (2D) structure and can be regarded as a monolayer film of energy-transducing nanometric components Photosynthetic species enhance their photosynthetic volume by folding the membranes in three dimensions (see Figure 6) Plant membranes containing PS2 are layered close to each other [20]; purple bacterial membranes may be folded similarly or form small spheres, budded off from a linear membrane [25] Whether or not there exists functionality from interacting complexes embedded in different membranes has to be established 1.31.1.3.4 Light harvesting and charge transport in purple bacteria To illustrate how the different components work together as a solar energy converter, we describe here how natural photosynthesis proceeds in one of the most simple and well-characterized photosynthetic systems: the photosynthetic machinery of purple nonsulfur bacteria 662 Technology (a) Final energy acceptor/ primary electron donor Electron Primary electron (b) transfer acceptor (c) Photon Energy transfer Light-harvesting systems Figure (a) Schematic representation of a photosynthetic membrane as proposed by L Duysens in the 1950s (Leiden, The Netherlands) A membrane consists of many light-absorbing components, also named pigments that also transfer the energy among them The target is an RC where this energy triggers a series of ET events starting off at a special site, the primary donor (b) Image of protein complexes embedded within a bacterial photosynthetic membrane obtained by atomic force microscopy by Bahatyrova and co-workers (Enschede, the Netherlands) In this particular membrane, RC–LH1 complexes form dimeric supercomplexes, which in turn are arranged in rows Adapted from Figure in Bahatyrova S, Frese RN, Siebert CA, et al (2004) The native architecture of a photosynthetic membrane Nature 430: 1058–1062 [17], with permission of Nature Publishing Group (c) Result of coarse-grained modeling of the photosynthetic membrane based on colloidal theory by Frese et al [24] A 2D lattice, occupied equally with dimeric RC–LH1 and RC–LH2 complexes, is equilibrated by a Monte Carlo method Energy minimization is based only on differences in size and shape of the two components Besides the two different domains as observed in the AFM images, the model also predicts the correct shape of the entire membrane Various subsequent realizations show the green domain to be highly fluid, while the red domain remains rigid Adapted from Figure 6d in Frese RN, Pamies JC, Olsen JD, et al (2008) Protein shape and crowding drive domain formation and curvature in biological membranes Biophysical Journal 94: 640–647 [24], with permission of Biophysical Society, USA 100 nm 50 nm Figure Electron micrograph of grana membranes that primarily contain the PS2 complexes (left panel) that are indicated in green in the schematic picture on the right panel PS1 is indicated in blue, ATP synthase in red, and b6f complexes in orange Adapted from Figures and in Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants Biochimica et Biophysica Acta—Bioenergetics 1706: 12–39 [20], with permission of Elsevier Science B.V The process starts with capture of light in the peripheral light-harvesting antennae, called LH2 The LH2 are ring-shaped protein oligomers that contain a ring of eight or nine BChl a monomers, called B800, and a second ring of eight or nine BChl a dimers, called B850 [26, 27] (see Figure 7) The pigment names are based on their lowest excited-state absorption maximum In addition, the LHs contain Cars that are located in van der Waals contact with the BChls, allowing efficient and rapid energy transfer [28] Excitations of the B800 BChls are localized on a single chromophore and move by Förster-type electronic energy transfer (EET) to the B850 BChls in ∼0.7 ps [30] In contrast, the B850 BChls are strongly coupled This gives rise to excitonic interactions that distribute excitations across several chromophores of the B850 ring with an intraring ‘hopping time’ of ∼100 fs The energy is transferred from the peripheral LH2 complexes to the core antenna complexes, called LH1, in ∼3 ps [31] The larger core antennae are elliptical-shaped oligomers and contain Cars and a ring of 15 or 16 BChl a dimers, called B875 The B875 BChls are also strongly coupled and their arrangement is homologous to the B850 BChls in LH2 [7, 32] The LH1 ellipse surrounds the bacterial RC and energy transfer from the B875 BChls into the RC takes place in ∼35 ps [31] The bacterial RCs organize the pigments into two parallel ET pathways, termed the A side and the B side However, the RC only utilizes the A-side cofactors for ET In the RC, light is absorbed by two BChl molecules called the ‘special pair’ or P870 Once the special pair absorbs a photon, it ejects an electron, which is transferred via another molecule of BChl to a bacteriopheophytin (BPheo) This induces the initial charge separation P(+)BPheo(–) in ∼3 ps To prevent charge recombination in this state, the electron is transferred from BPheo(–) to a quinone, called QA at the A side, in ∼200 ps and subsequently to a quinone at the B side, called QB, in ∼200 μs While the QA is tightly bound to the RC, the QB is loosely associated and can easily detach Two electrons are required to fully reduce QB to QBH2 by taking up two protons The reduced quinone QBH2 diffuses through the membrane to another protein complex Artificial Leaves: Towards Bio-Inspired Solar Energy Converters (a) 663 (c) LH-II LH-II LH-I LH-II RC B850 (b) −1.0 (d) LH-2 P870* 0.7 ps −1−5 ps ps BChl ps BPh 200 ps −0.5 P870 hν 35 ps −1.5 ps LH-1 Em (V) B800 10 ns 0.0 QA 200 μs QB 100 ms B875 B800 P 0.5 870 Figure Photosynthetic unit of purple bacteria (a) Modeled structure of light-harvesting units and (LH1 and LH2) and the RC The structures of LH2 and the RC are from the crystal structures, and LH1 is simulated by analogy to LH2 Adapted from Figure in Hu XC, Damjanovic A, Ritz T, and Schulten K (1998) Architecture and mechanism of the light-harvesting apparatus of purple bacteria Proceedings of the National Academy of Sciences of the United States of America 95: 5935–5941 [1], with permission of National Academy of Sciences (b) Dynamics of energy-transfer processes between bacteriochlorophylls B850 and B800 in LH2, B875 in LH1, and the special pair P870 in the RC Adapted from Figure in Yang M, Agarwal R, and Fleming GR (2001) The mechanism of energy transfer in the antenna of photosynthetic purple bacteria Journal of Photochemistry and Photobiology 142: 107–119 [29], with permission of Elsevier Science B.V (c) AFM image of arrangement of LH2–RC (highlighted in green) and LH1–RC (red) complexes in the bacterial membrane The bright spots are the LH1–RC complex and the inset in the second panel is a model using the known crystal structures to reproduce the image Adapted from Figure in Bahatyrova S, Frese RN, Siebert CA, et al (2004) The native architecture of a photosynthetic membrane Nature 430: 1058–1062 [17], with permission of Nature Publishing Group (d) Energies and timescales of ET within the RC Adapted from Figure 6.3 in Blankenship RE (2002) Molecular Mechanisms of Photosynthesis Oxford, UK: Blackwell Science Ltd [2], with permission (cytochrome bc1 complex) where it is oxidized In the process, the reducing power of the QBH2 is used to pump protons across the membrane (see also Figure 1) The generated electrochemical gradient is used to drive synthesis of ATP by the membrane-bound F0F1–ATPase protein, converting the captured light energy into a chemical form 1.31.2 Design Principles of Natural Photosynthesis From an engineer’s perspective, the underlying physical chemical and physical principles of energy and ET processes in photo­ synthetic units can be described by a defined set of length and energy scales that may be used as guidelines for the design of a so-called artificial leaf An excellent overview of these engineering guidelines is presented in the work of Noy and Dutton [33, 34] 1.31.2.1 1.31.2.1.1 Photon Absorption, Excitation Energy Transfer, and Electron Transfer Photon absorption The first length scale is connected with the rate of photon absorption Kabs and the following definition is taken from Reference 33 The absorption cross section σ depends on the photon energy E and on the flux of photons in the spectrum of solar irradiance (E) In addition, there is an energetic threshold Emin, set according to the driving force of the charge separation reaction so that 664 Technology Z Kabs ẳ EịEịdE ẵ1 Emin As explained by Noy et al [33], a rough estimate of the amount of incident solar photons (φtotal =  1021 photons s− m− 2) is obtained by integrating the standard reference solar spectral irradiance at Air Mass 1.5 (ASTM G-173-03) Using this value, Kabs can be defined as Kabs = 40r2, with r being the radius of the absorbing molecule in Å Typically, r for a single Chl molecule is ∼0.03 nm and the maximal photon absorption rate for a single pigment is therefore ∼4 s− under standard solar irradiance conditions Hereby, 30–300 absorber molecules are needed in a photosynthetic unit to obtain biological catalysis rates of 102–104 s−1 1.31.2.1.2 Excitation energy transfer The second length scale is associated with excitation energy transfer The excitation energy is transferred primarily via dipole–dipole Coulomb interactions in a Fưrster mechanism according to kEET ¼ kf  r 6 r ½2Š with kEET being the excitation energy transfer rate, kf the radiative constant, and r0 the half-radius of the Förster process Since the length scale of exciton migration in the antenna is large, the exciton lifetimes should be long enough to allow for photons striking any part of the antenna to reach the RC Typical r0 values for photosynthetic pigments are 5–10 nm Once excitons are trapped in the RC, the process of charge separation should take place faster compared to back transfer to the antenna units This is achieved by a relatively large antenna–RC distance (∼2 nm) versus a short distance for the redox pigments in the RC Furthermore, surrounding of the RCs by assemblies of antenna pigments gives a spatial arrangement in which energy transfer is optimized by multiple entries to the RC The combination of constraints (spatial distance between antenna–RC and multiple entries to the RC) is achieved by circular-like arrangements of antenna pigments around the RCs, with a ‘cordon sanitaire’ zone (see Noy et al [33]) of ∼2 nm around the RC where no antenna pigments occur 1.31.2.1.3 Electron transfer The third length scale is connected to the ET processes In the RC, electron transport via multiple steps is necessary because transfer across the membrane in a single step would be too slow to compete with decay of the excited state to the ground state and dissipation of the energy into useless heat If the electron and the hole can be further separated before charge recombination occurs, the electronic coupling and therefore the rate constant for recombination is drastically reduced The use of multiple cofactors separated by an edge-to-edge distance less than 0.6 nm ensures a rapid tunneling time of ∼10 ps or less for every step The dependence of the rates of ET reactions within covalently linked donor–acceptor (DA) molecules on the free energy of reaction and the electronic interaction between the donor and the acceptor are described well by theory Equation [3] shows how the ET rate kET depends on these quantities:   2π 2 kET ¼ e – G0 ỵ ị = 4kT ẵ3 VDA ℏ ð4πλkT Þ = where ΔG0 is the free energy of reaction, VDA the electronic coupling between the donor and the acceptor, and λ the total energy of the nuclear reorganization (structural change) within the donor, the acceptor, and the solvent required for the reaction to occur One of the key features of eqn [3] is that it predicts that the rate of an ET reaction will slow down when the free energy of reaction becomes very large This is the so-called ‘inverted Marcus region’, which has been proven experimentally [35, 36] This fact has proven critical to the design of long-lived charge separation systems The total reorganization energy λ is usually divided into contributions from nuclear motions within the donor and acceptor molecules λi and solvent molecules λs The value of λi may be calculated from the force constants for all the molecular vibrations in both the reactant and the product, while λs can be determined by application of the dielectric continuum model of a solvent 1.31.2.2 Photochemical Thermodynamics of Energy Storage The photosynthetic apparatus is connected to the steady-state network of catalytic conversion reactions in the organism that is continuously dissipating energy If there is a shortage at one spot, it can be smoothly compensated from other dynamic reservoirs in the network The storage and downstream utilization can be described as a single-step conversion of solar energy into Gibbs free energy In its simplest form, the photosynthetic solar cell is a heat engine that produces charge separation (see Figure 8) Inside the engine, a molecular absorber is excited that produces charge separation There are three basic conversion processes in the primary mechanism of the photosynthetic solar cell [38]: Excitation of a molecular absorber (Chl) with rate g Energy conversion by charge separation with rate I into an electron and hole in dynamic equilibrium with the absorber Back reaction with rate 1/τ from the excited Chl state into the ground state Artificial Leaves: Towards Bio-Inspired Solar Energy Converters TS T Iqin I g 1/τ Iqout I 665 μe μh Figure The solar energy converter as heat engine In photosynthesis, a Chl molecule is connected to a reservoir at ambient temperature T ∼ 300 K, and emitting heat flow Iqout is excited due to the heat flow Iqin from the solar reservoir at temperature T = 5800 K with a rate g to an excited state separated by an energy hν from the ground state The excited Chl state either decays with loss rate 1/τ or produces an electron–hole pair with net charge separation rate I and free energy Δμ = μe − μh Adapted from Figure in Markvart T and Landsberg PT (2002) Thermodynamics and reciprocity of solar energy conversion Physica E 14: 71–77 [37], with permission of Elsevier Science B.V The importance of a tight connection between energy conversion and energy storage was noted at an early stage [39] First, excitation of a molecular Chl absorber in exchange with the field of solar irradiation leads to a difference in chemical potential:   ẵChl abs ẳ h0 ỵ kB T ln ½4Š ½ChlŠ with [Chl]* and [Chl] being the populations of the excited and the ground state of the absorber, respectively In the dark, the excited and the ground states are in equilibrium and Δμabs = 0, leading to [Chl]*/[Chl] = exp (−hv0/kBT), that is, the Boltzmann distribution For Chl a in a plant, hν0 = 1.8 eV The upper limit at the absorber stage is η = − 4T/3TS = 93% efficiency due to entropic losses originating from the different temperatures of the incoming radiation and of the heat reservoir A photovoltaic solar cell produces electricity, while a photosynthetic RC produces a photochemical steady state with a voltage over the membrane and charge separation in dynamic equilibrium with the absorber When the light is switched on and the absorber is coupled to a storage reservoir, a steady state is produced, where the formation of the excited state is balanced by its decay due to the limited life time and the net flow of energy into the charge–separated (CT) state The quantity   p′q′ ½5Š Δμe − h ẳ e ỵ kB T ln p0 q0 represents the difference in chemical potential or free energy produced by light-induced charge separation and contains an electronic and a photochemical term that measures the probabilities p′q′ of electron and hole occupation of the acceptor and donor states in the light relative to the concentration p0′q0′ in the dark and is proportional to the temperature [37] Biochemically, it is very difficult to maintain a membrane potential, which is rapidly converted in a ΔpH that is used to produce ATP, an intermediate energy carrier When a storage reservoir is connected to the absorber, energy flows can be forwarded from the absorber into the reserve and backwarded from the reserve back into the absorber, where it can be emitted In this way, assimilation has to compete against depletion of the reserve by backward reaction coupled with radiative loss in the absorber The entire system has to operate linearly and close to the thermodynamic limit to minimize losses The net production rate of charge separation and energy extraction can be described by the solar cell equation:     Δμ –1 ½6Š I ¼ If – Ib exp kB T with If and Ib being the forward and backward reaction rates, respectively Equation [6] is the equivalent of the Shockley equation for a solar cell, in which If and Ib would be the light-generated and dark saturation current, respectively [37] The energy storage from an elementary steady-state process can be generalized according to the equation st ẳ max ỵ kB T ln ị ẵ7 Here, the first factor is due to the kinetics of the steady state, while δ measures the thermodynamic activity of the trap In order to favor the forward reaction over the backward process, the energy of the combined products is lower than that for the excited state by at least kBT ln(δ) The maximum power is generated for δ ∼ kBT/μmax, a compromise between a high conversion efficiency and a high storage efficiency For plant photosystems I and II under operational conditions, Δμst ∼ 1.2 eV and Δμmax ∼ 1.3 eV Equation [7] can be generalized to storage processes further downstream and longer timescales, where the entire system is in Boltzmann equilibrium with the initial excited state Δμst should be sufficiently low to maintain the steady state against back reactions and represents the work that can be obtained, for example, from sugar or biomass When the solar radiation is interrupted, the unavoidable back reaction causes gradual depletion of the accumulated energy For instance, a plant in the dark produces a small flux of photons (luminescence) from its reserve that was stored during illumination 666 Technology periods This leads to a generalized expression for the thermodynamic limit of energy storage in a steady-state reserve at all time and length scales, starting from the initial free energy stored in the solar energy assimilation hν0, according to t ½8Š Δμst ðt Þ ¼ hν0 – kB T ln τ with t being the storage time The highest yields and efficiencies are attainable when energy is used as soon as it is assimilated, avoiding intermediate storage, for instance, by generating and using electricity, by running nanoscale catalytic converters directly from the photoconverter and storing the energy in a redox couple, by coupling a chemical cycle directly to a photoconverter like in the chloroplast, by connecting the chloroplast directly to respiration like in the plant, or by using light-driven cell factories for production of food and chemical feedstock 1.31.3 The Design of an Artificial Leaf What is an artificial leaf? The answer depends on the focus point that one has when talking about a leaf Is a leaf a high surface area for the capture of photons? Or is it a natural design of a light energy to fuel converter? Or perhaps, is it an example of high­ density-packed nanomachines that capture and utilize light energy? The term ‘artificial leaf’ was introduced by Gratzel in 1991 [40] describing a new generation of solar cells, in which a Chl-mimicking sensitizer is bound as a monomolecular coating on the surface of a TiO2 membrane Upon light absorption, the sensitizer is excited and ejects an electron in the TiO2 conduction band Here, we like to expand the definition and point out that the main feature of a leaf lies in its biological nature It represents Nature’s approach toward light energy utilization It features self-assembly, self-repair, and adaptability Furthermore, a leaf constitutes different, well-defined nanometric systems, each of them precisely tuned to carry out a specific task and to interrelate with each other As such, the most prominent feature of how a leaf utilizes light energy is the supramolecular functioning of the several building blocks The artificial leaf represents a different approach toward (photosynthesis) solar energy conversion compared to bio-based fuel production where natural or genetically modified organisms are used in an agricultural fashion An artificial leaf is a device where biological material may well be entirely absent At the same time, it has to feature some of the crucial aspects of natural photosynthesis Minimally, this is the self-assembly of building blocks into a functional supramolecular network that operates on fine-tuned length and timescales constrained by physical rules The hypothetical device constitutes three aspects of photosynthesis: (1) light capture, (2) charge separation and ET, and (3) catalysis The first two cover also the main aspects of photovoltaics In photosynthesis though, ETs can trigger the splitting of water into oxygen and protons, the cycling of electrons, or the generation of proton-motive force Artificial photosynthesis research targets all these aspects of natural photosynthesis and can be separated into two main approaches: bio-based systems and bio-inspired synthetic systems The first approach utilizes integrated biological components, isolated via biochemistry techniques from living organisms The latter approach mimics the biological systems by means of synthetic chemistry or surface physics For both lines of research, there is a necessity to interconnect compounds or systems with conducting material in order to extract electrons and re-reduce the primary electron donor In other words, the photovoltaic aspect of the artificial leaf constitutes the primary mode of operation and has to be solved for any artificial photosynthetic design 1.31.3.1 Interfacing Proteins onto Solid-State Surfaces Biology may serve as a template for a bottom-up approach in nanotechnology [41] Ever since the discovery of the protein, it has been recognized that biological function is carried out starting from the nanoscale to higher length scales At the nanoscale, matter has several properties that are different from larger scales, notably large reactive surfaces and a molecular thermodynamic regime In biology, these properties lead to dynamic properties of the systems, allowing rapid response to changing impulses from the outside world Measuring or utilizing environmental impulses that interact with biology in a technological fashion may utilize biological components [42] Such devices have been constructed, most famously the electrochemical blood glucose test strips for diabetes [43] Here, for an artificial leaf harboring features as in a biological cell but which is not a (synthetic) biological cell itself, adaptability implies nanometric components that are embedded within a flexible matrix To date, proteins or protein complexes are the only compounds known that may provide this adaptability outside a cell And for solar energy uses, photosynthetic proteins are the first to be utilized Early research on interfacing photosynthetic proteins and conducting surfaces concentrated on the purple bacterial RC since it has been the best characterized photosynthetic complex [44] The RC encompasses the key features sought after in an artificial leaf: a self-assembling and high-pigment-density nanometric structure, with a near-unity quantum yield of directional energy and electron-transferring capability Likewise, LHCs enhance the absorption cross section considerably with only minimal energy losses [9] Ongoing photosynthesis research elucidates to more and more detail how pigments are organized by the proteins to accomplish these feats [45, 46] Fine-tuning includes the mutual orientation and distances of cofactors within degrees and angstroms relative to each other, leading to very precise energy-transfer and ET reactions While the research on protein functionality transferred into a device may have started (and perhaps still is) a proof-of-principle type of investigation, it will be hard to find any other matrix that can arrange light-active molecules with such precision [34] In this section, we will present an overview of the investigations on the interfacing of protein complexes and conducting material Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 667 The first attempts to derive electric currents from purple bacterial RCs in vitro were reported around 30 years ago [47] These experiments utilized RCs embedded within a membrane that separated two aqueous compartments containing electron carriers similar to those used by the organism: cytochrome c in one compartment and short-chain (i.e., water-soluble) quinones in the other These measurements showed the possibility of utilizing isolated RCs to generate a photocurrent, but the currents obtained were low, with a peak value less than a pA cm−2 Much higher light-induced currents were subsequently obtained with bacterial RCs adhered onto a conducting surface immersed in a liquid and under potentiostatic control [48] The surface functions as an electrode, with an extrinsic electric potential applied between the surface and a counter electrode The potential can, in principle, be used to drive electrons in either direction between the RCs and the surface, and to control the redox state of both the RC chromophores and extrinsic charge carriers Charge carriers such as cyt-c and water-soluble quinones have been used to shuttle electrons between the RCs and the electrode(s) This method was used by Katz [49] to derive currents up to 80 nA cm−2 using a functionalized surface with special linkers that connected with the terminal electron acceptor, QB, site of the RC Work by Trammell et al [50] also indicated that the RC can be linked to a surface with either the P or the Q side facing the electrode, with photo-induced electron tunneling being proposed to occur between either P or QB and the surface A large body of research focused on the bacterial RC alone, with special linkers adhered to surfaces serving as electrodes (see Figure 9(a)) The surfaces were functionalized with a self-assembled monolayer (SAM) of molecules and a variety of redox mediators were employed (for review, see Reference 52, 53) Similar light-induced electrochemistry experiments have also been reported on RCs surrounded by the LH1 LHC [54, 55] An enormous increase in photocurrent has been reported after an electrode with linked RCs was exposed to a solution of water-soluble protein cytochrome c2 (see Reference 51 and Figure 9(b)) This finding indicated that this relatively small protein interspersed between the RCs and the electrode surface to form an electron relay that enhanced ETs for nonfavorable oriented RCs RCs and RC–LH1 complexes also adhere onto a gold surface in the absence of any engineered linkers onto the proteins and SAMs covering the surface Bacterial photosynthetic membranes can also be functionally adhered onto a conducting surface [56] Such design may be favorable, since the membrane provides a matrix allowing diffusive processes to occur, necessary for self-organization and adaptability More recently, electric currents have been derived from protein complexes from oxygenic photosynthetic organisms, such as Photosystem (PS1) or Photosystem (PS2) adhered onto metal electrodes [57–60] A fully functional photocell has been constructed using spinach PS1 or bacterial RCs, sandwiched between two electrodes [61] Although the energy conversion of this cell proved to be low, it did show the possibility to construct a photovoltaic device using photosynthetic components All these designs discussed here can be characterized as proof of principle showing the applicability of biological material for solar energy devices The highest light-induced current densities obtained were on the order of 10–100 µA cm−2 [58], still a factor of 100 lower compared to a Grätzel cell [62] Likely, the rate-limiting step in all these cases is electron tunneling from the RCs to the surface On the other hand, some designs showed to be functional while exposed to air, a major advantage in solar energy conversion, especially when combined with a water-splitting catalyst On a final note, we stress here that a protein is a structured polymer The usage of polymers as matrices for light-active molecules is a large research field [63] and research pushing the limit on utilizing biological material may well be leading the way for improving synthetic solar energy materials 1.31.3.2 Protein Maquettes for Artificial Photosynthesis Artificial proteins connect bio-based and bio-inspired solar energy converters The protein matrix is used, and in fact indispensable, to fine-tune position and orientation of pigments, to create directional ET pathways, and to provide a proper scaffold for catalytic reactions, all of which processes have been characterized in great detail in natural proteins In 1987, Ho and Degrado [64] programmed peptides to assemble into an amphiphilic four-helix bundle protein through hydrophobic interactions by imposing an alternating pattern of hydrophilic and hydrophobic helix-forming residues Using histidines as ligands, self-assembled four-helix bundles were designed to bind heme cofactors, introducing the elementary design of an artificial photosynthetic pigment–protein complex [65] For selective incorporation of electron-donor and electron-acceptor cofactors, a family of four-helix bundle peptides was designed with distinct hydrophilic and hydrophobic domains along the length of the helices, allowing light-induced ET along the helices across a surface between polar and nonpolar media [66] The four-helix bundle families show the advantage of bottom-up approach, in which synthetic peptides are step-by-step assembled into more complex structures Alternatively, a top-down approach uses natural proteins as templates, stripping down their complexity to create a minimal functional design Back in the 1980s, it was found that the LH1 antenna complex of purple bacteria could be reconstituted from isolated antenna peptides and pigments and this process turned out to be reversible and controlled by its thermodynamic parameters [67–69] By mutational approaches, the minimal requirements for self-assembly into subunits and into a ring-shaped complex were evaluated [70–73] Absorption, fluorescence, and circular dichroism spectroscopy on reassembled LH1 antenna systems verified that pigment and antenna polypeptides were assembled together into functional antenna complexes with excitonic pigment–pigment and structural pigment–protein interactions Its reversible assembly makes the purple bacterial antenna complex very accessible for substitution with synthetic components to create an artificial antenna Based on LH1 polypeptides, a minimal polypeptide unit was designed that is capable of intermediate self-assembly into subunits and binding of pigments [74] (see Figure 10); LHCs have been reassembled from natural polypeptides and Zn BChls [75], and zinc porphyrins were immobilized on a surface by assembly of the pigments with synthetic peptides that contained LH1 polypeptide sequences [76] 668 Technology (a) Cytochrome c Ubiquione-10 (Q2) H LB QB P H hν hν H M QA P QB 12 Å NH BL Ni(NTA) H O QA M HN O 4Å Carbon electrode Carbon electrode Cysteine (Cys) = Polyhistidinetag = (b) RC tilting RC lying RC standing SAM gold Figure (a) Schematic presentation showing two possible ways of RC binding and ET pathways between RC and electrode P, primary electron donor (special pair); B, monomeric bacteriochlorophyll; H, BPheo; QA and QB primary and secondary electron acceptors (quinones), respectively The structure of the bifunctional linkers used for binding to carbon electrodes is labeled and Adapted from Figure 1B in Trammell SA, Spano A, Price R, and Lebedev N (2006) Effect of protein orientation on electron transfer between photosynthetic reaction centers and carbon electrodes Biosensors and Bioelectronics 21: 1023–1028 [50], with permission of Elsevier Science B.V (b) Molecular wiring RCs via cytochrome c2 complexes onto a SAM-covered electrode Proteins: red (helices) and yellow (strands); his-tag: blue; pigments: green and orange Inset shows the possible RC (red) orientation relative to SAM (blue) surface and the main orientation of which a molecular relay via cytochrome c2 (brown) enhances electron-tunneling rates Adapted from Figure in Lebedev N, Trammell SA, Spano A, et al (2006) Conductive wiring of immobilized photosynthetic reaction center to electrode by cytochrome c Journal of the American Chemical Society 128: 12044–12045 [51], with permission of American Chemical Society, USA Figure 10 Reversible self-assembly of the purple bacterial LH1 antenna ring from isolated pigments and polypeptides The impact of the protein matrix on the pigment properties and vice versa have been investigated in great detail in numerous studies Recent nuclear magnetic resonance (NMR) studies showed how mechanistic pigment–protein interactions are translated into subtle electronic perturbations [77–80] The protein matrix induces pigment structural deformations that can create electronic polarization, and Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 669 Chemical shift mapping of pigment−protein interactions (a) (b) Mg Mg Figure 11 Pigment–protein interactions in the light-harvesting antenna of Rps acidophila induce electronic perturbations that may tune the light-harvesting function (a) Displacements in the protein backbone structure (colored in red) correlate with pigment–protein and protein–protein interactions (b) The BChl electronic structures compared to free BChl in solution show perturbations induced by the protein matrix Partial charges are drawn as spheres in red (positive) and blue (negative) pigment–pigment distances are fine-tuned by balancing forces in the pigment–protein complex This is illustrated in Figure 11 Since the structure–electronic details are revealed hereon an atomic scale, these features could in principle be rebuilt in artificial constructs Summarizing, the LH antenna polypeptides position and fine-tune the interpigment distances with nanometric precision and induce oligomerization into ring-shaped structures, controlling the functionality on length scales ranging from subnanometer distances to supramolecular scales All of these features are ready for adaptation in artificial photo-antenna devices through programmed self-assembly of protein building blocks The design of photosynthetic RC protein mimics for light-driven electron transport is a more challenging task Through protein engineering of a cytochrome b, artificial proteins that mimic the ET from a light-activated chlorine to a bound quinone molecule were constructed by Hay et al [81] A quinone-binding site was engineered into the Escherichia coli cytochrome b(562) by introducing a cysteine within the hydrophobic interior of the protein and reconstituting its heme-binding site with a Zn-chlorine More recently, bacterioferritin (cytochrome b1 from E coli) was used as a scaffold [82] The heme was replaced with Zn chlorine and the diiron-binding sites were replaced by two manganese ions Upon illumination, the bound Zn chlorines initiate ET followed by oxidation of the manganese center, possibly via an inherent tyrosine residue This novel artificial RC potentially mimics the assembly of a water oxidation center, heading toward the design of a water-splitting artificial RC 1.31.3.3 Bio-Inspired Self-assembled Artificial Antennae The photosynthetic apparatus consists of self-assemblies that bridge length scales from fine-tuned subnanometer distances between connecting chromophores to the macroscopic scales of supramolecular aggregates This allows the incoming light energy to migrate over long distances to the RC and to separate charge and transport charges to the catalytic sites A major challenge in artificial photosynthesis is to develop functional components that equivalently self-organize themselves into an interconnected system This section will focus on the self-assembly of artificial antenna pigments to create antennae that transport light energy over long distances In the subsequent section, artificial RC constructs are described that can create spatially separated CT states or transport holes and charges for directed charge injection into a solid surface We limit the discussion to noncovalent assembled antennae, but it is stressed that significant progress has also been made toward the synthesis of bio-inspired covalent antenna structures [83, 84] For instance, various dendrimer type of antennae have been constructed based on polyphenylene [85], porphyrin, or phthalocya­ nine [86] building blocks Inspired by the oligomeric structures of purple bacterial antenna systems that allow for efficient excitation energy transfer (EET) between the protein-bound BChls, different types of cyclic porphyrin wheels have been designed as artificial light-harvesting antennae that allow for efficient EET between the porphyrins [87, 88] 1.31.3.3.1 Chlorosome-based, light-harvesting antennae In contrast to the antenna apparatus of all other photosynthetic organisms, chlorosome antennae of green photosynthetic bacteria contain rod-shaped oligomers of BChl c/d/e molecules that self-aggregate without assistance of a protein scaffold This fact was discovered in the early 1990s by the notion that chlorosome preparations compared with those of artificial pigment aggregates had striking similar spectroscopic properties [89] A few years later, a model study applying resonance Raman and a cross-polarization 670 Technology magic-angle-spinning (CP-MAS) solid-state NMR study proved that also the structural organization of the pigment assemblies in chlorosomes was similar to the structural arrangements of in vitro pigment aggregates [90, 91] The chlorosome self-organized structures possess characteristic redshifted Qy absorption of the oligomerized BChls Their structural functional features have been the inspiration for self-assembled artificial antennae In chlorosomes, the self-assemblies are stabilized by C=O∙∙∙H–O∙∙∙Mg interactions between the 31 hydroxy group, the 13 carbonyl groups, and the central magnesium, and by π–π interactions between the tetrapyrrole macrocycles [92] Starting from biological material, that is, Chl a isolated from natural photosynthetic organisms, metal complexes of 31-hydroxy-131-oxo-chlorins lacking the 132-COOCH3 group were synthesized as model compounds by chemical modification In particular, Zn chlorines were synthesized with various side-chain patterns, which self-assembled into oligomers with different degrees of redshifted Qy absorption [93] The efficiency of chlorosomal-based antennae depends on their excitation energy-transfer dynamics and exciton delocaliza­ tion properties These properties have been determined for different species of natural chlorosomes as well as for artificial pigment aggregates EET between BChls in natural chlorosomes was estimated to be 4–6 ps [94, 95] Based on two-pulse, photon-echo and transient absorption techniques, delocalization over 2–3 pigments was estimated for the species Chlorobium tepidum and over 10–12 pigments for Chloroflexus aurantiacus [96] For artificial Zn-chlorine aggregates coaggregated with an energy trap, similar delocalization over 10–15 pigments was found [97] Exciton theory calculations on chlorosomal model aggregates showed that the excitation energy transport occurs along helical trajectories, which reflects the presence of the macroscopic chirality in the tubular aggregates [98] In the last years, there have been several breakthroughs in resolving the pigment-packing structure in natural and artificial chlorosome-like assemblies Single-crystal X-ray diffraction of BChl c mimics showed extended BChl stacks that are packed by hydrophobic interactions, with weak interactions between carbonyl groups and the central Zn atom [99] Recently, the chlorosome BChl aggregate structure was revealed of a triple mutant of the green sulfur bacteria Chlorobaculum tepidum, by a combination of solid-state NMR, cryo-electron microscopy (cryo-EM), and biological mutagenesis [100] (Figures 12 and 13) The absence of a methyl group at C-20 in the triple mutant and of side-chain heterogeneity and the very limited stereochemical heterogeneity at position 31 in the BChl d pigments provided very high-resolution MAS solid-state NMR data Combining the NMR results with cryo-EM data that revealed a helical arrangement of Chl stacks, for the first time the molecular and supramolecular structure of a chlorosome was solved together Combining solid-state NMR with X-ray diffraction techniques, the molecular packing structure in Zn-chlorine aggregates could be obtained without isotope labeling of compounds by similar methodologies [101] The approach now allows for fast screening of new compounds in terms of the novel supramolecular structures with altered light-harvesting properties Zn porphyrin assemblies have been used for photosensitization of TiO2 and SnO2 Self-assembling chlorosome-mimicking porphyrin stacks were used to photosensitize wide-band-gap semiconductors with a 2.2% incident photon to charge separation efficiency [102] In bilayers of porphyrin derivatives and a TiO2 surface, exciton lengths up to 20 nm were observed for nematic layers at room temperature conditions [103], showing that it is possible to realize long exciton diffusion lengths by varying the design of porphyrin derivatives with different stacking tendencies Similar to chlorosome aggregates, the organic dye perylene tetracarboxylic acid bisimide (PBI) can assemble into supramolecular structures, directed by altering hydrogen bonding, metal–ligand interactions, and π–π stacking interactions This way, structures such as squares, rosettes, and extended fibrous assemblies have been obtained in solution and at interfaces [104] PBIs have favorable properties for applications in semiconductor solar cells, such as intense photoluminescence and n-type semiconductivity Additional chromophores can be attached at the imide groups to induce energy and ET processes upon photoexcitation Chen et al [105] recently describe a trialkylphenyl-functionalized PBI, which formed extended fluorescent aggregates in nonpolar solvent and possesses liquid crystalline properties The dye aggregates contained strong electronic coupling and charge-transfer interaction Nanowires of this dye are considered ideal candidates for further investigations as n-type semiconducting materials 1.31.3.4 Bio-Inspired DA Constructs In the late 1970s, the first DA dyads were constructed based on porphyrin–quinone (P–Q) systems In the P–Q system, the covalently linked porphyrin and quinone function as the electron-donor chromophore and the electron acceptor, respectively COOR OH O OH COOR Mg OH O COOR O OH O Mg COOR O Mg OH COOR OH COOR OH O Mg OH O Mg COOR O COOR OH Mg O Mg COOR Mg Figure 12 Syn–anti stacking of BChls in the triple bchQRU mutant of Chlorobium tepidum chlorosomes Mg Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 671 0.83 nm (a) a b (c) b a 1.25 nm 0.83 nm (b) γ II 1.25 nm a b Figure 13 The structure of the triple bchQRU mutant of Chlorobium tepidum Pairs of alternating syn–anti-ligated BChl d stacks form sheets that self-assemble into coaxial tubes (a) Syn–anti arrays with the stacks indicated by red lines (b and c) The H-bond helices that connect BChl stacks via the carbonyls are shown in blue and are right handed in (b) and left handed in (c) Adapted from Figure in Ganapathy S, Oostergetel GT, Wawrzyniak PK, et al (2009) Alternating syn–anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes Proceedings of the National Academy of Sciences of the United States of America 106: 8525–8530 [100], with permission of National Academy of Sciences [106] While these simple DA systems could elucidate basic photochemical principles, they were unable to maintain long CT P+ −Q−, with typical values of a few hundred picoseconds or less in solution before charge recombination takes place to the ground state The CT state lifetimes were significantly improved by introduction of a third building block in a Car–P–Q triad, in which a porphyrin (P) is linked to a Car electron donor on one side and to a quinone (Q) electron acceptor on the other side [107] Upon photoexcitation of the porphyrin in the triad, the first excited singlet-state Car−P*−Q decays via a two-step ET process, leading to the formation of a Car+−P−Q− CT state that decays on a microsecond timescale The triad contains three basic properties that mimic the functional design of natural RCs First, a long-lived CT state is created via multielectron steps Second, the structure allows the CT state to be spatially well separated Third, coupling between the building blocks is weak and the first step endergonic so that charge recombination is slow [108] The special properties of fullerene (C60) and its capability to uptake several electrons have led to various DA dyads, triads, and more complex systems that include fullerene–porphyrin building blocks (see Figure 14) [108, 109] 672 Technology H N C N O N N H H N N CH3 2.0 C-1P-C60 C-P-1C60 + – Energy (eV) C-P -C60 1[C+-P-C– ] 60 1.0 3[C+-P-C– ] 60 C-P-C60 10 0.0 C-P-C60 Figure 14 High-energy states and interconversion pathways for a Car–P–C60 triad artificial RC Adapted from Figure in Gust D (2001) Mimicking photosynthetic solar energy transduction Accounts of Chemical Research 34: 40–48 [110], with permission of American Chemical Society In natural systems, ET is often coupled to proton motions in proton-coupled electron transfer (PCET), avoiding high-energy intermediates by concerted electron and proton transfer reactions In plant photosystem II (PS2), a tyrosine called TyrZ is a redox mediator that is oxidized by the electron donor P●+ The oxidation step likely is combined with the protonation of a hydrogen-bonded histidine residue (His+) by the TyrZ phenol OH so that the combined, chemically reversible reactions His => His+ and TyrZ+ => TyrZ● occur The reaction has been mimicked in a hybrid system composed of TiO2 nanoparticles to which photochemically active mimics of the photosynthetic Chl–Tyr–His complex were attached [111] The construct undergoes photo-induced stepwise ET coupled to proton motion and is thermodynamically capable of water oxidation Bio-inspired DA constructs with PCET make the step from photo­ voltaics that generate electricity toward a fuel-producing solar cell, which is the outlook described in the next section Despite many efforts to create multistep ET DA constructs, their performance in creating a long-lived CT state is still low compared to natural RCs In alternative constructs, the special photophysical properties of ruthenium (Ru) dyes are used rather than porphyrins After light excitation, Ru rapidly decays to the triplet state, with minimal losses from the (nanosecond) decay to the ground state The long-lived (approximately millisecond) triplet state is used to create a CT state As we will see in the next section, promising design for photoelectrochemical fuel cells use Ru-sensitized TiO2 as an anode Another approach totally opposed to the concept of multielectron steps is to create dyads that operate in the so-called ‘inverted Marcus region’, where the rate of an ET reaction will slow down when the free energy of reaction becomes very large, as can be deduced from eqn [3] (Section 1.31.2.1), and it is theoretically possible to create long charge separation lifetimes without loss of energy [112] The boundary conditions for such ‘inverted region’ dyads is that they should have low reorganization energy (using short spacers between the donor and acceptor units) and that the charge separation energy should be lower than the triplet excited state The latter prevents the CT state to decay rapidly to the triplet excited state in the Marcus normal region and decays to the ground state in the Marcus inverted region An example of such a dyad is given by 9-mesityl­ 10-methylacridinium ion (Acr+–Mes), in which an electron-donor moiety (mesityl group) is directly connected at the position of the acridinium ion [112] The dyads can be further developed to form self-assembled DA constructs that are linked by covalent and noncovalent bonds, combining ‘nonnatural’ design for charge separation with bio-inspired approaches for supramolecular assembly 1.31.3.4.1 Self-assembled DA constructs Different self-assembly strategies have been put forward using π-stacking interactions between small covalent building blocks based on perylene and naphthalene diimides (PDIs and NDIs) and porphyrin-based molecules Wasielewski [113] has demonstrated the emergent behavior of self-assembled synthetic light-harvesting antenna structures that induce self-assembly of a functional special pair of five PDI molecules undergoing ultrafast, quantitative charge separation The formed DA self-assemblies can be modified to assemble into higher organized stacks with controlled DA geometry, creating efficient charge transport along molecular wires Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 673 Self-assembled DA triads having a primary and a secondary donor attached to PDI imide nitrogen atoms had an average distance between the two radical ions that was much larger than in their monomeric building blocks (3.1 vs 2.3 nm), demonstrating that electron hopping through the π-stacked PDI molecules is fast enough to compete with the charge recombination time of 40 ns [114] A remaining challenge in those systems is to induce unidirected transport of charge, efficiently coupled to a surface In bilayer and bulk n/p heterojunction organic solar cells, electron-transporting materials are arranged via conductive materials, while hole-transporting materials need efficient charge separation at very large electron DA interfaces For this purpose, Matile et al [115–117] have developed supramolecular n/p heterojunctions with oriented multicolored antiparallel redox gradients, called OMARG-SHJs, that mimic Nature in capturing as much light as possible and quickly funnel electrons and holes in opposite directions The self-assemblies include 3D zipper architectures, positioned on a surface, of NDIs attached to p-oligophenyl (POP) or p-oligophenylethynyl (OPE) chromophores The NDIs build up redox gradients for electron transport, while the POP/OPE DA systems create hole transport in the opposite direction (Figure 15) h+ (a) OA e− AO O R− N O NH O N N O H Br N H NH H OA AO H N N N O O Br H O O e− AO O− O O O H N O R+ OA H H OA O AO H AO + NH3 Y− N N H O O H N N O H H O H N N AO OA O O O h+ O− O N N H O O OA H O O O O Y+ OA O O O OPE AO NH3+ N− O N OA O O N N O H H N H O n Au-1-(2−3-)m−(4-5)n− OA AO AO p OA 4: A = R+ (OPE-R+) 5: A = R− (OPE-R−) AO O −4 h+ −5 −6 −7 OA O e− e− e− AO − e− eV −3 H O O (b) POP Y R OPE h+ h+ POP 2: A = Y+ (POP-Y+) 3: A = Y− (POP-Y−) 6: A = R+ (POP-R+) 7: A = R− (POP-R−) O NH N h+ 1: A = N− (POP-N-) = S S Figure 15 Hypothetical architectures of OMARG-SHJs with two-component redox gradients The constructs contain a zipper assembly of stacks of red NDI electron donors along strings of OPE hole acceptors on top of yellow NDI electron acceptors along POP hole donors By inducing gradients along both the electron- and hole-transporting pathways, photo-induced charge separation over very long distances is achieved Adapted from Figure in Sakai N, Bhosale R, Emery D, et al Supramolecular n/p-heterojunction photosystems with antiparallel redox gradients in electron- and hole-transporting pathways Journal of the American Chemical Society 132: 6923–6925 [116], with permission of American Chemical Society 674 Technology 1.31.4 Outlook: The Construction of a Fuel-Producing Solar Cell The final goal in creating artificial leaves is to build a fuel-producing solar cell as depicted in the scheme in Figure 16 For this aim, natural photosynthesis serves as a blueprint for clean hydrogen production We described here in various sections the different materials that are being used as a starting point for the construction of an artificial leaf Where one material is ready to use, the photosynthetic proteins, and research focuses on the integration within artificial devices, others are synthesized and tested for function, like the synthetic dyads and triads Yet others are merely on the drawing board, the synthetic proteins In any case, all research directions are facing major challenges of which we list here the most important ones Although the principal products of photosynthesis in plants and bacteria are carbohydrates, certain algae and cyanobacteria can produce hydrogen directly from water using sunlight, thus providing a basis for the creation of suitable artificial systems Yet, considerable challenges need to be overcome in mimicking the functioning of natural photosynthetic systems for a water-splitting and hydrogen-producing device In Nature, biological systems operate at ambient temperatures and neutral pH and evidently are built from earth-abundant materials Considerable research effort is directed into constructing synthetic compounds that can catalyze light-activated water splitting Although successful compounds have been presented, the major hurdle to overcome is to utilize earth-abundant materials instead of Ru, palladium, or platinum Proteins use molecular recognition to establish reactions on a nanoscale Molecular and supramolecular assemblies are not fixed but flexible and exist in thermodynamic equilibria and metastable states Their components can reversibly be dissociated and reassembled, permitting an organism to adapt to external influences such as sunlight conditions Nanometric building blocks such as proteins not exist outside Nature, other than synthetic proteins Directing the synthesis of proteins, natural or synthetic, outside a cell is still an elaborate task, but after a proof-of-principle demonstration has been shown for its usefulness, technological progress is expected Currently, biochemical methods are easily applied and purifying proteins outside organisms is a routine procedure Although progress has been made in adhering proteins and membranes onto surfaces, light activation and catalytic machineries have not been coupled yet Furthermore, biological systems feature self-repair to replace damaged components, which is how they cope with photodamage by reactive side products of the water oxidation reaction Component replacement, but also the coupling of reaction output to input of various components, requires a dynamic environment Nanopatterned surfaces accompanied with chemical activation for specific binding may direct artificial supramolecular constructs of photosynthetic and other proteins But likely such designs will not incorporate dynamics Membranes ensure such flexibility and have been adhered onto surfaces functionally; here, the durability of the material or else the cost-effectiveness for replacement has to become more detailed Biological membranes form a natural barrier for charge carriers (protons) and can build up a membrane potential Once charge separation is converted into a membrane potential, the energy is stored in electrical form without losses due to back transfer, a feature that is not easily mimicked in an artificial device In general, energy storage on all timescales is the main challenge for artificial photosynthesis It has proven very difficult to design a water-splitting catalyst because of the multiple ETs necessary (and thus the storage of electrons during these transfers) Synthetic compounds that can transfer two electrons per excitation may be a solution to this problem Similarly, synthetic compounds will need to store molecular excitations waiting for demand of charge-transfer compounds The major challenge will be the coupling of light-activated and catalytic compounds and the removal of bottlenecks in both reactions ensuring small recombination losses Tuning the rates of two nonrelated processes will be necessary as well as the fast electron relay of the light-activated compound into an electrode without charge recombination and under low overpotential While at this time, the many different approaches toward artificial photosynthetic solar cells still focus on the different materials that could be used, the main breakthrough in this field will be proof-of-principle design incorporating light-absorbing units, coupled to redox catalysts and proton pumps or proton-to-hydrogen converters A main theme within these designs will be the e− EET Reaction center e− Antenna R (H+, CO2) Catalytic site P (H2, MeOH) e− Catalytic site R (H2O, HA) P (O2, A, H+) Figure 16 Schematic picture of an integrated artificial device for production of hydrogen and methanol Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 675 utilization of a larger part of the solar spectrum than is used by natural photosynthesis, for instance, one part driving water splitting and another proton pumping or hydrogen production It is likely that only at that stage, when all units have become interconnected, the true functioning of components will become apparent As many research collaborations are aiming at just that, tremendous progress in this field is expected between now and 2015 References [1] Hu XC, Damjanovic A, Ritz T, and Schulten K (1998) Architecture and mechanism of the light-harvesting apparatus of purple bacteria Proceedings of the National Academy of Sciences of the United States of America 95: 5935–5941 [2] Blankenship RE (2002) Molecular Mechanisms of Photosynthesis Oxford, UK: Blackwell Science Ltd [3] Oostergetel GT, van Amerongen H, and Boekema EJ The chlorosome: A prototype for efficient light harvesting in photosynthesis Photosynthesis Research 104: 245–255 [4] Mullineaux CW (2005) Function and evolution of grana Trends in Plant Science 10: 521–525 [5] Su HN, Xie BB, Zhang XY, et al The supramolecular architecture, function, and regulation of thylakoid membranes in red algae: An overview Photosynthesis Research 106: 73–87 [6] Deisenhofer J, Epp O, Sinning I, and Michel H (1995) Crystallographic refinement at 2.3-angstrom resolution and refined model of the photosynthetic reaction-center from Rhodopseudomonas viridis Journal of Molecular Biology 246: 429–457 [7] Roszak AW, Howard TD, Southall J, et al (2003) Crystal structure of the RC–LH1 core complex from Rhodopseudomonas palustris Science 302: 1969–1972 [8] Zinth W and Wachtveitl J (2005) The first picoseconds in bacterial photosynthesis – Ultrafast electron transfer for the efficient conversion of light energy ChemPhysChem 6: 871–880 [9] Vangrondelle R, Dekker JP, Gillbro T, and Sundstrom V (1994) Energy-transfer and trapping in photosynthesis Biochimica et Biophysica Acta—Bioenergetics 1187: 1–65 [10] Heathcote P, Fyfe PK, and Jones MR (2002) Reaction centres: The structure and evolution of biological solar power Trends in Biochemical Sciences 27: 79–87 [11] Hillier W and Babcock GT (2001) Photosynthetic reaction centers Plant Physiology 125: 33–37 [12] Yachandra VK, Sauer K, and Klein MP (1996) Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen Chemical Reviews 96: 2927–2950 [13] Barber J and Archer MD (2001) P680, the primary electron donor of photosystem II Journal of Photochemistry and Photobiology A: Chemistry 142: 97–106 [14] Ishikita H, Loll B, Biesiadka J, et al (2005) Redox potentials of chlorophylls in the photosystem II reaction center Biochemistry 44: 4118–4124 [15] Jordan P, Fromme P, Witt HT, et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution Nature 411: 909–917 [16] Zouni A, Witt HT, Kern J, et al (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 angstrom resolution Nature 409: 739–743 [17] Bahatyrova S, Frese RN, Siebert CA, et al (2004) The native architecture of a photosynthetic membrane Nature 430: 1058–1062 [18] Frank J (2002) Single-particle imaging of macromolecules by cryo-electron microscopy Annual Review of Biophysics and Biomolecular Structure 31: 303–319 [19] Muller DJ and Dufrene YF (2008) Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology Nature Nanotechnology 3: 261–269 [20] Dekker JP and Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants Biochimica et Biophysica Acta—Bioenergetics 1706: 12–39 [21] Sturgis JN and Niederman RA (2008) Atomic force microscopy reveals multiple patterns of antenna organization in purple bacteria: Implications for energy transduction mechanisms and membrane modeling Photosynthesis Research 95: 269–278 [22] Scheuring S and Sturgis JN (2005) Chromatic adaptation of photosynthetic membranes Science 309: 484–487 [23] Kirchhoff H, Haferkamp S, Allen JF, et al (2008) Protein diffusion and macromolecular crowding in thylakoid membranes Plant Physiology 146: 1571–1578 [24] Frese RN, Pamies JC, Olsen JD, et al (2008) Protein shape and crowding drive domain formation and curvature in biological membranes Biophysical Journal 94: 640–647 [25] Frese RN, Siebert CA, Niederman RA, et al (2004) The long-range organization of a native photosynthetic membrane Proceedings of the National Academy of Sciences of the United States of America 101: 17994–17999 [26] Koepke J, Hu XC, Muenke C, et al (1996) The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum Structure 4: 581–597 [27] Papiz MZ, Prince SM, Howard T, et al (2003) The structure and thermal motion of the B800–850 LH2 complex from Rps acidophila at 2.0 (A)over-circle resolution and 100 K: New structural features and functionally relevant motions Journal of Molecular Biology 326: 1523–1538 [28] Sundstrom V, Pullerits T, and van Grondelle R (1999) Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit Journal of Physical Chemistry B 103: 2327–2346 [29] Yang M, Agarwal R, and Fleming GR (2001) The mechanism of energy transfer in the antenna of photosynthetic purple bacteria Journal of Photochemistry and Photobiology 142: 107–119 [30] van Grondelle R and Novoderezhkin V (2001) Dynamics of excitation energy transfer in the LH1 and LH2 light-harvesting complexes of photosynthetic bacteria Biochemistry 40: 15057–15068 [31] Fleming GR and Vangrondelle R (1997) Femtosecond spectroscopy of photosynthetic light-harvesting systems Current Opinion in Structural Biology 7: 738–748 [32] Hu XC, Ritz T, Damjanovic A, et al (2002) Photosynthetic apparatus of purple bacteria Quarterly Reviews of Biophysics 35: 1–62 [33] Noy D, Moser CC, and Dutton PL (2006) Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales Biochimica et Biophysica Acta—Bioenergetics 1757: 90–105 [34] Noy D (2008) Natural photosystems from an engineer’s perspective: Length, time, and energy scales of charge and energy transfer Photosynthesis Research 95: 23–35 [35] Miller JR, Calcaterra LT, and Closs GL (1984) Intramolecular long-distance electron-transfer in radical-anions – The effects of free-energy and solvent on the reaction-rates Journal of the American Chemical Society 106: 3047–3049 [36] Wasielewski MR, Niemczyk MP, Svec WA, and Pewitt EB (1985) Dependence of rate constants for photoinduced charge separation and dark charge recombination on the free-energy of reaction in restricted-distance porphyrin quinone molecules Journal of the American Chemical Society 107: 1080–1082 [37] Markvart T and Landsberg PT (2002) Thermodynamics and reciprocity of solar energy conversion Physica E 14: 71–77 [38] Boeker E and van Grondelle R (1999) Environmental Physics Chichester, NY: Wiley [39] Ross RT and Calvin M (1967) Thermodynamics of light emission and free-energy storage in photosynthesis Biophysical Journal 7: 595–614 [40] Gratzel M (1991) The artificial leaf, molecular photovoltaics achieve efficient generation of electricity from sunlight Coordination Chemistry Reviews 111: 167–174 [41] Mavroidis C, Dubey A, and Yarmush ML (2004) Molecular machines Annual Review of Biomedical Engineering 6: 363–395 [42] Sarikaya M, Tamerler C, Jen AKY, et al (2003) Molecular biomimetics: Nanotechnology through biology Nature Materials 2: 577–585 [43] Defronzo RA, Tobin JD, and Andres R (1979) Glucose clamp technique – Method for quantifying insulin-secretion and resistance American Journal of Physiology 237: E214–E223 [44] Okamura MY, Paddock ML, Graige MS, and Feher G (2000) Proton and electron transfer in bacterial reaction centers Biochimica et Biophysica Acta—Bioenergetics 1458: 148–163 [45] Read EL, Lee H, and Fleming GR (2009) Photon echo studies of photosynthetic light harvesting Photosynthesis Research 101: 233–243 [46] van Grondelle R and Novoderezhkin VI (2006) Energy transfer in photosynthesis: Experimental insights and quantitative models Physical Chemistry Chemical Physics 8: 793–807 676 Technology [47] Schonfeld M, Montal M, and Feher G (1979) Functional reconstitution of photosynthetic reaction centers in planar lipid bilayers Proceedings of the National Academy of Sciences of the United States of America 76: 6351–6355 [48] Janzen AF and Seibert M (1980) Photoelectrochemical conversion using reaction-center electrodes Nature 286: 584–585 [49] Katz E (1994) Application of bifunctional reagents for immobilization of proteins on a carbon electrode surface – Oriented immobilization of photosynthetic reaction centers Journal of Electroanalytical Chemistry 365: 157–164 [50] Trammell SA, Spano A, Price R, and Lebedev N (2006) Effect of protein orientation on electron transfer between photosynthetic reaction centers and carbon electrodes Biosensors and Bioelectronics 21: 1023–1028 [51] Lebedev N, Trammell SA, Spano A, et al (2006) Conductive wiring of immobilized photosynthetic reaction center to electrode by cytochrome c Journal of the American Chemical Society 128: 12044–12045 [52] Lu YD, Xu JJ, Liu BH, and Kong JL (2007) Photosynthetic reaction center functionalized nano-composite films: Effective strategies for probing and exploiting the photo-induced electron transfer of photosensitive membrane protein Biosensors and Bioelectronics 22: 1173–1185 [53] Trammell SA, Griva I, Spano A, et al (2007) Effects of distance and driving force on photoinduced electron transfer between photosynthetic reaction centers and gold electrodes Journal of Physical Chemistry C 111: 17122–17130 [54] Suemori Y, Nagata M, Nakamura Y, et al (2006) Self-assembled monolayer of light-harvesting core complexes of photosynthetic bacteria on an amino-terminated ITO electrode Photosynthesis Research 90: 17–21 [55] Kondo M, Nakamura Y, Fujii K, et al (2007) Self-assembled monolayer of light-harvesting core complexes from photosynthetic bacteria on a gold electrode modified with alkanethiols Biomacromolecules 8: 2457–2463 [56] Magis GJ, den Hollander MJ, Onderwaater WG, et al (2010) Light harvesting, energy transfer and electron cycling of a native photosynthetic membrane adsorbed onto a gold surface Biochimica et Biophysica Acta—Biomembranes 1798: 637–645 [57] Maly J, Masojidek J, Masci A, et al (2005) Direct mediatorless electron transport between the monolayer of photosystem II and poly (mercapto-p-benzoquinone) modified gold electrode-new design of biosensor for herbicide detection Biosensors and Bioelectronics 21: 923–932 [58] Badura A, Esper B, Ataka K, et al (2006) Light-driven water splitting for (bio-)hydrogen production: Photosystem as the central part of a bioelectrochemical device Photochemistry and Photobiology 82: 1385–1390 [59] Ciobanu M, Kincaid HA, Lo V, et al (2007) Electrochemistry and photoelectrochemistry of photosystem I adsorbed on hydroxyl-terminated monolayers Journal of Electroanalytical Chemistry 599: 72–78 [60] Terasaki N, Yamamoto N, Tamada K, et al (2007) Bio-photo sensor: Cyanobacterial photosystem I coupled with transistor via molecular wire Biochimica et Biophysica Acta—Bioenergetics 1767: 653–659 [61] Das R, Kiley PJ, Segal M, et al (2004) Integration of photosynthetic protein molecular complexes in solid-state electronic devices Nano Letters 4: 1079–1083 [62] Sauvage F, Chen DH, Comte P, et al (2010) Dye-sensitized solar cells employing a single film of mesoporous TiO2 beads achieve power conversion efficiencies over 10% ACS Nano 4: 4420–4425 [63] Park C, Yoon J, and Thomas EL (2003) Enabling nanotechnology with self assembled block copolymer patterns Polymer 44: 6725–6760 [64] Ho SP and Degrado WF (1987) Design of a 4-helix bundle protein – Synthesis of peptides which self-associate into a helical protein Journal of the American Chemical Society 109: 6751–6758 [65] Choma CT, Lear JD, Nelson MJ, et al (1994) Design of a heme-binding 4-helix bundle Journal of the American Chemical Society 116: 856–865 [66] Ye SX, Discher BM, Strzalka J, et al (2005) Amphiphilic four-helix bundle peptides designed for light-induced electron transfer across a soft interface Nano Letters 5: 1658–1667 [67] Pandit A, Ma HR, van Stokkum IHM, et al (2002) Time-resolved dissociation of the light-harvesting complex of Rhodospirillum rubrum, studied by infrared laser temperature jump Biochemistry 41: 15115–15120 [68] Pandit A, Visschers RW, van Stokkum IHM, et al (2001) Oligomerization of light-harvesting I antenna peptides of Rhodospirillum rubrum Biochemistry 40: 12913–12924 [69] Pandit A, van Stokkum IHM, Georgakopoulou S, et al (2003) Investigations of intermediates appearing in the reassociation of the light-harvesting complex of Rhodospirillum rubrum Photosynthesis Research 75: 235–248 [70] Todd JB, Recchia PA, Parkes-Loach PS, et al (1999) Minimal requirements for in vitro reconstitution of the structural subunit of light-harvesting complexes of photosynthetic bacteria Photosynthesis Research 62: 85–98 [71] Loach PA, Parkesloach PS, Davis CM, and Heller BA (1994) Probing protein structural requirements for formation of the core light-harvesting complex of photosynthetic bacteria using hybrid reconstitution methodology Photosynthesis Research 40: 231–245 [72] Todd JB, Parkes-Loach PS, Leykam JF, and Loach PA (1998) In vitro reconstitution of the core and peripheral light-harvesting complexes of Rhodospirillum molischianum from separately isolated components Biochemistry 37: 17458–17468 [73] Parkes-Loach PS, Majeed AP, Law CJ, and Loach PA (2004) Interactions stabilizing the structure of the core light-harvesting complex (LHL) of photosynthetic bacteria and its subunit (B820) Biochemistry 43: 7003–7016 [74] Noy D and Dutton PL (2006) Design of a minimal polypeptide unit for bacteriochlorophyll binding and self-assembly based on photosynthetic bacterial light-harvesting proteins Biochemistry 45: 2103–2113 [75] Nagata M, Nango M, Kashiwada A, et al (2003) Construction of photosynthetic antenna complex using light-harvesting polypeptide-alpha from photosynthetic bacteria, R rubrum with zinc substituted bacteriochlorophyll alpha Chemistry Letters 32: 216–217 [76] Ochiai T, Nagata M, Shimoyama K, et al (1441) Immobilization of porphyrin derivatives with a defined distance and orientation onto a gold electrode using synthetic light-harvesting alpha-helix hydrophobic polypeptides Langmuir 26: 14419–14422 [77] Pandit A, Buda F, van Gammeren AJ, et al (2010) Selective chemical shift assignment of bacteriochlorophyll a in uniformly [C-13-N-15]-labeled light-harvesting complexes by solid-state NMR in ultrahigh magnetic field Journal of Physical Chemistry B 114: 6207–6215 [78] Pandit A, Wawrzyniak PK, van Gammeren AJ, et al Nuclear magnetic resonance secondary shifts of a light-harvesting complex reveal local backbone perturbations induced by its higher-order interactions Biochemistry 49: 478–486 [79] Alia A, Wawrzyniak PK, Janssen GJ, et al (2009) Differential charge polarization of axial histidines in bacterial reaction centers balances the asymmetry of the special pair Journal of the American Chemical Society 131: 9626–9627 [80] Wawrzyniak PK, Alia A, Schaap RG, et al (2008) Protein-induced geometric constraints and charge transfer in bacteriochlorophyll–histidine complexes in LH2 Physical Chemistry Chemical Physics 10: 6971–6978 [81] Hay S, Wallace BB, Smith TA, et al (2004) Protein engineering of cytochrome b(562) for quinone binding and light-induced electrons transfer Proceedings of the National Academy of Sciences of the United States of America 101: 17675–17680 [82] Conlan B, Cox N, Su J-H, et al (2009) Photo-catalytic oxidation of a di-nuclear manganese centre in an engineered bacterioferritin ‘reaction centre’ Biochimica et Biophysica Acta 1787: 1112–1121 [83] Chu CC and Bassani DM (2008) Challenges and opportunities for photochemists on the verge of solar energy conversion Photochemical & Photobiological Sciences 7: 521–530 [84] Balzani V, Credi A, and Venturi M (2008) Molecular machines working on surfaces and at interfaces ChemPhysChem 9: 202–220 [85] Bauer RE, Grimsdale AC, and Mullen K (2005) Functionalised polyphenylene dendrimers and their applications Functional Molecular Nanostructures, pp 253–286 Berlin, Germany: Springer [86] Li WS and Aida T (2009) Dendrimer porphyrins and phthalocyanines Chemical Reviews 109: 6047–6076 Artificial Leaves: Towards Bio-Inspired Solar Energy Converters 677 [87] Nakamura Y, Aratani N, and Osuka A (2007) Cyclic porphyrin arrays as artificial photosynthetic antenna: Synthesis and excitation energy transfer Chemical Society Reviews 36: 831–845 [88] Aratani N, Kim D, and Osuka A (2009) Discrete cyclic porphyrin arrays as artificial light-harvesting antenna Accounts of Chemical Research 42: 1922–1934 [89] Holzwarth AR, Griebenow K, and Schaffner K (1992) Chlorosomes, photosynthetic antennae with novel self-organized pigment structures Journal of Photochemistry and Photobiology A: Chemistry 65: 61–71 [90] Tamiaki H (1996) Supramolecular structure in extramembranous antennae of green photosynthetic bacteria Coordination Chemistry Reviews 148: 183–197 [91] Balaban TS, Holzwarth AR, Schaffner K, et al (1995) CP-MAS C-13-NMR dipolar correlation spectroscopy of C-13-enriched chlorosomes and isolated bacteriochlorophyll-c aggregates of Chlorobium tepidum – The self-organization of pigments is the main structural feature of chlorosomes Biochemistry 34: 15259–15266 [92] Miyatake T and Tamiaki H (2005) Self-aggregates of bacteriochlorophylls-c, d and e in a light-harvesting antenna system of green photosynthetic bacteria: Effect of stereochemistry at the chiral 3-(1-hydroxyethyl) group on the supramolecular arrangement of chlorophyllous pigments Journal of Photochemistry and Photobiology C: Photochemistry Reviews 6: 89–107 [93] Balaban TS, Tamiaki H, and Holzwarth AR (2005) Chlorins programmed for self-assembly Supermolecular Dye Chemistry, pp 1–38 Berlin, Germany: Springer [94] Psencik J, Polivka T, Nemec P, et al (1998) Fast energy transfer and exciton dynamics in chlorosomes of the green sulfur bacterium Chlorobium tepidum The Journal of Physical Chemistry A 102: 4392–4398 [95] Steensgaard DB, van Walree CA, Permentier H, et al (2000) Fast energy transfer between BChl d and BChl c in chlorosomes of the green sulfur bacterium Chlorobium limicola Biochimica et Biophysica Acta – Bioenergetics 1457: 71–80 [96] Prokhorenko VI, Steensgaard DB, and Holzwarth AF (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum Biophysical Journal 79: 2105–2120 [97] Prokhorenko VI, Holzwarth AR, Muller MG, et al (2002) Energy transfer in supramolecular artificial antennae units of synthetic zinc chlorins and co-aggregated energy traps A time-resolved fluorescence study Journal of Physical Chemistry B 106: 5761–5768 [98] Prokhorenko VI, Steensgaard DB, and Holzwarth AR (2003) Exciton theory for supramolecular chlorosomal aggregates: Aggregate size dependence of the linear spectra Biophysical Journal 85: 3173–3186 [99] Jochum T, Reddy CM, Eichhofer A, et al (2008) The supramolecular organization of self-assembling chlorosomal bacteriochlorophyll c, d, or e mimics Proceedings of the National Academy of Sciences of the United States of America 105: 12736–12741 [100] Ganapathy S, Oostergetel GT, Wawrzyniak PK, et al (2009) Alternating syn–anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes Proceedings of the National Academy of Sciences of the United States of America 106: 8525–8530 [101] Ganapathy S, Sengupta S, Wawrzyniak PK, et al (2009) Zinc chlorins for artificial light-harvesting self-assemble into antiparallel stacks forming a microcrystalline solid-state material Proceedings of the National Academy of Sciences of the United States of America 106: 11472–11477 [102] Huijser A, Marek PL, Savenije TJ, et al (2007) Photosensitization of TiO2 and SnO2 by artificial self-assembling mimics of the natural chlorosomal bacteriochlorophylls Journal of Physical Chemistry C 111: 11726–11733 [103] Siebbeles LDA, Huijser A, and Savenije TJ (2009) Effects of molecular organization on exciton diffusion in thin films of bioinspired light-harvesting molecules Journal of Materials Chemistry 19: 6067–6072 [104] Wurthner F (2004) Perylene bisimide dyes as versatile building blocks for functional supramolecular architectures Chemical Communications (14): 1564–1579 [105] Chen ZJ, Stepanenko V, Dehm V, et al (2007) Photoluminescence and conductivity of self-assembled pi–pi stacks of perylene bisimide dyes Chemistry – A European Journal 13: 436–449 [106] Gust D and Moore TA (1989) Mimicking photosynthesis Science 244: 35–41 [107] Moore TA, Gust D, Mathis P, et al (1984) Photodriven charge separation in a carotenoporphyrin quinone triad Nature 307: 630–632 [108] Gust D, Moore TA, and Moore AL (2009) Solar fuels via artificial photosynthesis Accounts of Chemical Research 42: 1890–1898 [109] Imahori H (2007) Creation of fullerene-based artificial photosynthetic systems Bulletin of the Chemical Society of Japan 80: 621–636 [110] Gust D (2001) Mimicking photosynthetic solar energy transduction Accounts of Chemical Research 34: 40–48 [111] Moore GF, Hambourger M, Gervaldo M, et al (2008) A bioinspired construct that mimics the proton coupled electron transfer between P680(center dot)+ and the Tyr(z)–His190 pair of photosystem II Journal of the American Chemical Society 130: 10466–10467 [112] Fukuzumi S (2008) Development of bioinspired artificial photosynthetic systems Physical Chemistry Chemical Physics 10: 2283–2297 [113] Wasielewski MR (2009) Self-assembly strategies for integrating light harvesting and charge separation in artificial photosynthetic systems Accounts of Chemical Research 42: 1910–1921 [114] Bullock JE, Carmieli R, Mickley SM, et al (2009) Photoinitiated charge transport through pi-stacked electron conduits in supramolecular ordered assemblies of donor–acceptor triads Journal of the American Chemical Society 131: 11919–11929 [115] Bhosale R, Misek J, Sakai N, and Matile S Supramolecular n/p-heterojunction photosystems with oriented multicolored antiparallel redox gradients (OMARG-SHJs) Chemical Society Reviews 39: 138–149 [116] Sakai N, Bhosale R, Emery D, et al Supramolecular n/p-heterojunction photosystems with antiparallel redox gradients in electron- and hole-transporting pathways Journal of the American Chemical Society 132: 6923 [117] Bhosale R, Bhosale S, Bollot G, et al (2007) Synthetic multifunctional nanoarchitecture in lipid bilayers: Ion channels, sensors, and photosystems Bulletin of the Chemical Society of Japan 80: 1044–1057 Further reading Blankenship RE, Tiede DM, Barber J, et al (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement Science 332: 805, DOI: 10.1126/science.1200165 Regalado A (2010) Reinventing the leaf: Artificial photosynthesis to create clean fuel Scientific American Magazine (2010) Blankenship RE (2002) Molecular Mechanisms of Photosynthesis Oxford, UK: Blackwell Science Ltd Collings AF and Critchley C (2006) Artificial Photosynthesis: From Basic Biology to Industrial Application Weinheim, Germany: Wiley–VCH Verlag GmbH & Co KGaA, ISBN: 9783527606740, DOI: 10.1002/3527606742 Pandit A, de Groot HJM, and Holzwarth A (2006) Harnessing Solar Energy for the Production of Clean Fuels Leiden, The Netherlands: Leiden University, ISBN 978-90-9023907-1  ... Figure 14 ) [10 8, 10 9] 672 Technology H N C N O N N H H N N CH3 2.0 C-1P-C60 C-P-1C60 + – Energy (eV) C-P -C60 1[ C+-P-C– ] 60 1. 0 3[C+-P-C– ] 60 C-P-C60 10 0.0 C-P-C60 Figure 14 High -energy states... Biochemistry 41: 15 115 15 120 [68] Pandit A, Visschers RW, van Stokkum IHM, et al (20 01) Oligomerization of light-harvesting I antenna peptides of Rhodospirillum rubrum Biochemistry 40: 12 913 12 924 [69]... Acta 17 87: 11 12 11 21 [83] Chu CC and Bassani DM (2008) Challenges and opportunities for photochemists on the verge of solar energy conversion Photochemical & Photobiological Sciences 7: 5 21 530