Energy Conversion in Photosynthesis: A Paradigm for Solar Fuel Production Gary F. Moore and Gary W. Brudvig Department of Chemistry, Yale University, New Haven, Connecticut, 06520; email:
[email protected],
[email protected]
Annu. Rev. Condens. Matter Phys. 2010. 2:2.1–2.25
Key Words
The Annual Review of Condensed Matter Physics is online at conmatphys.annualreviews.org
energy transfer, electron transfer, catalysis, photosystem II, solar cells
This article’s doi: 10.1146/annurev-conmatphys-062910-140503 Copyright © 2010 by Annual Reviews. All rights reserved 1947-5454/10/0810-0001$20.00
Abstract Solar energy has the capacity to fulfill global human energy demands in an environmentally and socially responsible manner, provided efficient, low-cost systems can be developed for its capture, conversion, and storage. Toward these ends, a molecular-based understanding of the fundamental principles and mechanistic details of energy conversion in photosynthesis is indispensable. This review addresses aspects of photosynthesis that may prove auspicious to emerging technologies. Conversely, areas in which human ingenuity may offer innovative solutions, resulting in enhanced energy storage efficiencies in artificial photosynthetic constructs, are considered. Emphasis is placed on photoelectrochemical systems that utilize water as a source of electrons for the production of solar fuels.
2.1
1. PERSPECTIVES AND OVERVIEW During the winter months of 1855, Benjamin Silliman, Jr., professor of general and applied chemistry at Yale, conducted a series of pioneering experiments on the properties and uses of petroleum gathered from springs near Titusville, Pennsylvania. His detailed and optimistic report, completed April 16, 1855, led to the drilling of the first successful oil well by Edwin L. Drake at Titusville in 1859, and the founding of the modern petroleum industry. -The American Petroleum Institute, 19551 The drilling of the Drake well indeed marked the beginning of the international search for oil and in many ways changed the way we live. Currently, the energy economy of nearly all countries is based on the use of stored energy, primarily fossil fuels (the ancient products of photosynthesis) in the form of coal, oil, and natural gas, as well as nuclear energy in the form of uranium isotopes. Increases in world population and the rise of emerging economies are correlated with a projected increase in the rate of world-marketed energy consumption by 44% over the 2006 to 2030 period (from 15.8 TW in 2006 to 22.7 TW in 2030) (1–3). In the near term, current global market downturns dampen world demand for energy as manufacturing and consumer demand for goods and services abate. With anticipated economic recovery after 2010, most nations will return to trend growth in energy demand. Although oil supplies will dwindle, coal is abundant! Likewise, estimated fossil energy resources are capable of supporting a 30-TW burn rate for several centuries (3, 4). The more significant global concern is an alteration of Earth’s atmospheric chemistry in the form of increasing anthropogenic CO2 levels stemming from the combustion of fossil fuels (5, 6). Such issues dictate an imperative for transition to alternative carbon-neutral sources of energy (7). Of the available carbon-neutral energy sources, solar is quite promising, as it is abundant (striking the Earth’s surface at a rate of !120,000 TW) but unfortunately diffuse (!100 mW/cm2 ¼ 1.3 horsepower per square meter and diurnal. Thus, devising cost-effective methods for efficiently capturing and storing this energy for human use is among the grand challenges of science (8). Nature offers inspiration for designing devices capable of such processes and assurance that solar energy conversion can be performed on vast scales. Globally, photosynthesis stores solar energy in reduced carbon at a rate of !120 TW (9). As structural and mechanistic details of this process are elucidated, it should be possible to extract the principles involved and incorporate them into synthetic constructs. We must understand the limitations of biological systems imposed by their evolutionary history; such inefficiencies provide opportunities for human ingenuity to develop innovations. In this review, we discuss fundamental principles and parameters of solar energy conversion while drawing on examples from natural and artificial photosynthetic systems. Maximum efficiencies and theoretical limitations of such constructs are addressed as are potential strategies for improving current efficiencies.
1
These words appear on the plaque presented to the Yale University in 1955 from The American Petroleum Institute in recognition of the 100th anniversary of the Silliman report. The plaque is currently displayed near the main entrance of the Yale Chemistry Department.
2.2
Moore
#
Brudvig
2. INSPIRATION FROM NATURE Photosynthesis is the process by which a wide array of organisms, including archaea, bacteria, algae, and plants capture solar energy and ultimately convert it to chemical energy for storage purposes. In most cases, the process of photosynthesis involves five distinct phases: 1. the initial absorption of photonic energy (light), 2. the transfer of electronic excitation energy by antenna pigments (conduits) to a reaction center, 3. a charge separation event at a reaction center that converts electronic excitation energy to chemical redox energy, 4. stabilization of the charge separation by secondary processes often involving migration of holes and electrons to spatially separate electron donors and acceptors, and 5. synthesis of stable chemical products that store a portion of the initially absorbed photonic energy. Although there are variations in the overall processes of the many photosynthetic organisms, the fundamental principles and physics involved are similar. In this section, we briefly discuss key components involved in the capture, conversion, and storage of solar energy. We then review the photosynthetic process as it occurs in bacterial and oxygenic photosynthesis.
2.1. Capture and Conversion For light energy to be stored by photosynthetic organisms, it must first be captured and converted to a more readily usable form. The absorption of light, the transfer of its energy, the generation of charge-separated states, and subsequent further spatial separation of electrons and holes (charge stabilization) are fundamental steps of this overall process. 2.1.1. The Absorption of Light by Photoactive Pigments. The sun, as with all stars, is a nearly perfect black-body radiator incandescently emitting radiation that produces a characteristic broad spectrum of light. Figure 1 shows the solar irradiance spectra outside the Earth’s atmosphere [Air Mass (AM)0] and at sea level (AM1.5). As solar radiation passes through the atmosphere, incident energy is reduced by various absorption and scattering processes. High-energy ultraviolet (UV) light is effectively screened out by the ozone layer. Consequently, wavelengths less than 400 nm contribute only !8% to the total solar irradiance. The spectral region from 400 to 700 nm (visible light) makes up !45% of the solar irradiance whereas wavelengths longer than 700 nm (infrared light) account for !47%. The electric field of an incoming photon of light can induce an oscillating electric dipole in one of the chromophores associated with the photosynthetic apparatus, inducing a transition to a higher electronic energy state. Promoting an electron from the highest occupied molecular orbital to the lowest unoccupied molecular orbital gives a simple illustrative description of an electronic configuration constituting the lower energy ground state (S) and the higher energy excited state (S*) of a chromophore following the absorption of light (hn): S þ hn ! S* www.annualreviews.org
1:
#
Energy Conversion in Photosynthesis
2.3
Irradiance (W m–2 nm–1)
2.0
a
AM0
b
1.5
1.0 AM1.5
0.5
0.0
1,000
500
1,500
Wavelength (nm)
2,000
2,500
4
3
2
1
Energy (eV)
Figure 1 (a) Solar irradiance spectra outside the Earth’s atmosphere [denoted by AM0 (green line)] and at sea level [denoted by AM1.5 (blue line)] displayed as a function of wavelength and (b) the same spectra plotted as a function of energy.
Nature makes use of a wide array of pigments, including chlorophylls, bacteriochlorophyll (BChl), carotenoids, and phycobilins, for effectively capturing a wide range of photons. No known organism, however, is capable of utilizing light of wavelengths longer than 1,030 nm for photosynthesis. Although this spectral region accounts for !30% of the total solar irradiance, the photons that compose it have relatively low energy content. 2.1.2. Energy Transfer via Antenna Systems. The majority of pigments involved in photosynthesis function as antennas, harvesting the relatively diffuse source of photons arriving from the sun and delivering their energy to reaction centers. This function allows reaction centers to turn over at optimal rates and permits organisms to utilize photons over a large spectral range, including wavelengths for which the extinction coefficient of the reaction center pigments may be comparatively low. Most antenna systems incorporate a spatial and energetic organizational scheme, allowing excitation energy to pass from lower wavelength-absorbing pigments, located at the more distal sections of the antenna complex, to longer wavelength-absorbing chromophores that are proximal to reaction centers. Loss of photonic energy as heat (DH), during migration from excited-state donor pigments (D*) to ground-state acceptor pigments (A), provides a degree of irreversibility to the overall process, promoting effective funneling of excitation energy to reaction centers: D* þ A ! D þ A* þ DH
2:
The fundamental equation for energy (10, 11), and electron (12), transfer is the Fermi Golden Rule, which accounts for transitions between states due to weak perturbations. The formalism is expressed in Equation 3, 2p Ti!f ¼ % jhci jVjcf ij2 r, 3: h where Ti!f is the transition probability; % h is the Dirac constant (the reduced Plank constant); ci and cf are wave functions for the initial and final states, respectively; V is the operator that couples the initial and final states; and r is the density of states. Conventional 2.4
Moore
#
Brudvig
Fo¨rster Theory uses the Golden Rule expression in the context of a dipole-dipole approximation with the assumption that the donor and acceptor pigments are weakly coupled (13). This mechanism involves a nonradiative resonant process (neither photon emission nor absorbance is involved) resulting from coulombic coupling of transition dipoles among corresponding energy donors and acceptors. Singlet-singlet energy transfer between chlorophyll pigments is well described by the Fo¨rster model. As expressed in Equation 4, kD!A ¼ a
k2 k0D J(eA ), R6DA
4:
the energy transfer between pigments is dependent upon their mutual orientation and is proportional to interchromophore distance to the inverse sixth power, where kD!A is the transfer rate constant, a is a constant, k is an orientation factor, k0D is the radiative relaxation rate constant of the donor, RDA is the distance (in centimeters) between donor (D) and acceptor (A), and J(eA) is the spectral overlap (in coherent units cm6 mol%1) between the absorption spectrum of the acceptor and the fluorescence spectrum of the donor. Such parameters allow for separation of pigments that are large (up to !100 A˚) in comparison to chromophore dimensions. In this mechanism, efficient transfer is facilitated by a) favorable spectral overlap of donor emission and acceptor absorption, b) a high fluorescence quantum yield of the isolated donor pigment, and c) a large extinction coefficient for the acceptor. Evolutionary processes have likely fine-tuned these parameters to favor efficient transfer of energy between pigments in antenna complexes while preventing electron-transfer processes which, as discussed in the following section, demand a much closer spatial overlap of the orbitals involved. The increase in overall light-harvesting efficiency provided by antenna systems can in some cases (high-light or stressed conditions) lead to photodamage of the organism. For this reason, nature has developed elaborate regulation, protection, and repair mechanisms (14–18). Such processes include photoprotection from singlet oxygen damage provided by rapid quenching of chlorophyll triplet states by energy transfer to carotenoid pigments. Unlike singlet-singlet energy transfer, triplet-triplet transfer is forbidden from proceeding via a dipole-dipole mechanism and likely occurs by an electron exchange process requiring ˚ ), as accounted for in the Dexter self-exchange mechaclose orbital contact (within !10 A nism of energy transfer (19). In the Dexter mechanism, exchange rates fall off exponentially with increasing donor acceptor separation, as expressed in Equation 5, kD!A ¼ KJe(%2RDA =L) ,
5:
where kD!A is the transfer rate constant, K is the orbital overlap factor, J is the spectral overlap integral, RDA is the distance between donor (D) and acceptor (A), and L is a constant. Although the conventional Fo¨rster and Dexter mechanisms differ in formalism, they essentially represent two ends of a continuum, and it is not always clear which mechanism is operating during a given energy-transfer process or if such a distinction is even relevant (20). This is especially true for many of the highly organized yet complex photosynthetic antenna systems. 2.1.3. Electron Transfer at Reaction Centers. The final step in an antenna system is transfer of energy to a reaction center. Here, the energy of an excited state is transformed www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.5
to chemical potential in the form of a charge-separated state. The reaction center is a multisubunit pigment-protein complex embedded in the photosynthetic membrane. It contains chlorophylls and other redox-active cofactors such as quinones (Qs) or iron sulfur centers. In most photosynthetic organisms, the reaction center contains a special pair of chlorophyll pigments (P) that are promoted to an electronically excited dimer (P*) by energy transfer from the antenna system (or by direct photon absorption). The excited state (P*) is a powerful reducing agent that rapidly donates an electron to a nearby electron acceptor molecule (A), generating the charge-separated state PþA–: P* þ A ! Pþ þ A%
6:
This initial photo-induced electron transfer is followed by a series of stabilizing, rapid, secondary charge-transfer events that prevent undesirable charge-recombination reactions by spatially separating holes and electrons. Within less than a nanosecond, the corresponding charges are separated by nearly the thickness of the biological membrane (!0.3 nm). Although each electron transfer comes at the expense of some fraction of the initially absorbed photonic energy, the physical separation reduces geminant recombination rates by orders of magnitude, allowing slower enzymatic processes to take over and make use of the photogenerated chemical redox energy by converting it to forms more easily utilized by the organism. Electron-transfer reactions in biological systems have received a great deal of experimental and theoretical analysis (12, 21, 22). Equation 7 describes the electron-transfer rate constant (kET) in the adiabatic regime (where the electronic transmission factor is close to unity): qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi " # 2 %2 lkB T)jVj2 e %(DGo þl) =4lkB T ) kET ¼ (p=h 7: The pre-exponential factor includes the electronic matrix element V describing coupling between reactant and product states (a function of the overlap of donor and acceptor orbitals, which depends on spatial, energetic, geometric, and symmetry factors) in addition to the reduced Planck constant, the Boltzmann constant kB, and the reorganizational energy for the reaction l. The reorganizational energy is associated with nuclear motions involved in transforming from the reactant to product states. It includes a solventindependent term li accounting for molecular structural differences between reactants and products and a solvent-dependent term ls, which represents the solvent reorganizational energy. The exponential term in Equation 7 is the Franck-Condon factor, which includes the standard free-energy change for the reaction (DGo), as well as l. As described by Equation 7, electron transfer can occur in three regimes. In the normal region, where –DGo < l, the rate of electron transfer increases as a function of a progressively negative standard Gibbs free energy (DGo). When –DGo equals l, the Franck-Condon factor is at a maximum; thus, electron transfer is activationless and the rate is maximized as a function of thermodynamic driving force. For considerably exergonic reactions, where –DGo > l, the system is in the inverted region. Here, the rate of electron transfer decreases with an increasingly negative standard Gibbs free energy. Such inverted region kinetics are often invoked as an explanation for the observed relatively slow charge-recombination reactions in photosynthetic reaction centers; yet other factors may be responsible (12). Electron-transfer reactions involving electrodes and semiconductor surfaces (a topic discussed later) do not display inverted region behavior. Here, a high density of states 2.6
Moore
#
Brudvig
assures there is always a product state to which electron transfer is essentially activationless. In this case, the rate constant is summed over all density of states and the relative contribution from each state is weighted according to Fermi-Dirac statistics regarding the probability of electron occupancy (23). For systems in which –DGo & l, the Butler-Volmer equation for reactions at an electrode provides a sufficient mathematical description of the electron-transfer kinetics (24).
2.2. Cyclic Electron Transport in Purple Photosynthetic Bacteria Photosynthetic bacteria use light energy to power a cyclic electron-transport system that is coupled to the formation of a proton gradient across a biological membrane. The resulting proton-motive force (PMF) is used for production of adenosine triphosphate (ATP) by the enzyme ATP synthase (25). During this process, photons are initially absorbed by an extensive antenna system, and excitation energy is transferred to a reaction center. Isolated purple bacterial reaction centers have been probed, utilizing a variety of techniques, resulting in a wealth of information regarding structure and kinetic/thermodynamic parameters of the various redox-active species involved (26). Structures of reaction center complexes from the photosynthetic bacteria Rhodopseudomonas viridis and Rhodobacter sphaeroides have been extensively studied, and crystal structures at better than 2.3 A˚ resolution are available. The complex contains three protein subunits designated L, M, and H. The L-M-H terminology, although widely used, is erroneously based on apparent molecular masses as determined by mobility on sodium dodecyl sulfate polyacrylamide gel, where L ¼ light, M ¼ medium, and H ¼ heavy. The true masses (L ¼ 31 kDa, M ¼ 34 kDa, and H ¼ 28 kDa), as later determined by DNA sequencing, are significantly different from those suggested by their names. In some species (such as Rhodopseudomonas viridis), a fourth subunit, C (cytochrome), is present. The reaction center protein forms a scaffold on which the various redox cofactors are arranged along transmembrane a helices of the L and M proteins, forming two branches (denoted A and B) with a pseudo-twofold axis of symmetry. Purple bacterial reaction centers contain four BChls, two bacteriopheophytins (BPheos), one carotenoid, two Qs, and one metal ion (in most cases a nonheme Fe2þ). Despite the apparent pseudo-twofold symmetry of the overall structure, the electron-transfer pathway is asymmetric. At the reaction center, excitation of the primary electron donor, a BChl dimer (P870, named for its lowest energy absorption band at 870 nm), generates a very strong reducing agent (the excited-state BChl dimer, P870*) with an estimated redox potential of –940 mV versus a normal hydrogen electrode (NHE) (Figure 2). Transient absorption measurements indicate this excited-state species is rapidly oxidized (!3 ps) and that an electron is donated to the nearby BPheo, located on the A branch, via a monomeric BChl (27). This ion pair state (P870þ-BPhA–) decays via subsequent electron transfer to a Q acceptor (QA located on the A branch) in 200–300 ps. QA– then transfers the electron to the B branch Q (QB) forming the semi-Q species QB– in 100–200 ps. QB– is a relatively stable species; lasting long enough for a second photon to activate the reaction center complex. Concomitant with oxidation of QA–, the oxidized primary donor (P870þ) is reduced by a cytochrome [either a bound cytochrome subunit that donates electrons via a heme cofactor or a soluble cytochrome c species (in most cases cytochrome c2)] that regenerates P870 for subsequent rounds of photochemistry (28). Following a second photoinitiated turnover of the reaction center, reduction of QB– is accompanied by proton uptake from the aqueous www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.7
–1.0
P870* 3 ps BChl
1 ps
E (V versus NHE)
BPheo
200 ps
–0.5
hν (1.4 eV) 0.0
0.5
QA 10 ns
200 µs
QB
100 ms
P870
Figure 2 Energy-kinetic diagram for the photochemistry and electron-transfer processes in reaction centers prepared from Rhodobacter sphaeroides. In this diagram, bacteriochlorophyll (BChl) a is indicated as potential redox intermediate energetically poised between the excited-state BChl dimer (P870*) and bacteriopheophytin (BPheo). Abbreviations: V, volts; NHE, normal hydrogen electrode.
cytoplasmic compartment and subsequent release of the hydro-Q species from the QB binding site (29). The released hydro-Q diffuses to the cytochrome bc1 complex (a large, multisubunit, integral membrane protein complex located within the intracytoplasmic membrane), where it is oxidized to Q, in a two-electron/two-proton process. The resulting protons are expelled into the periplasmic side of the lipid membrane (30, 31). One of the electrons donated to the cytochrome bc1 complex is used to restore the oxidized cytochrome c to its reduced state, thereby completing the cyclic electron-transport chain. The other electron is involved in reduction of Q in a process known as the modified Q cycle (32). Together, the reaction center and the cytochrome bc1 complex use photonic energy to pump two protons from the cytoplasm into the periplasm per electron transferred through the chain. The resulting free energy, stored in the proton gradient, is ultimately used to power conversion of adenosine diphosphate (ADP) and inorganic phosphate (Pi) to ATP by the enzyme ATP synthase, converting PMF to chemical energy in the form of phosphodiester bonds (25).
2.3. Linear Electron Transport in Oxygenic Photosynthetic Organisms Oxygenic photosynthetic organisms, including plants, algae, and cyanobacteria, use a linear electron-transport system in which water is the source of electrons (oxidizing H2O to O2) for the conversion of nicotinamide adenine dinucleoide phosphate (NADPþ) to its reduced form (NADPH). To generate the photovoltages necessary for matching the relatively large redox span of these half reactions (the oxidation and reduction component of the overall redox reaction in which O2/H2O is 0.82 V and NADPþ/NADPH is –0.32 V versus NHE at pH ¼ 7), such organisms use dual photochemical systems [photosystems II and I (PSII and PSI)] connected in series via the cytochrome b6f complex (33). Both photosystems are located in thylakoid membranes with their associated antenna complexes and the cytochrome b6f complex. In this scheme, two photons are required for linear transport of one electron from PSII through the cytochrome b6f complex and then through PSI. Electrons are supplied to PSII 2.8
Moore
#
Brudvig
from water via the oxygen-evolving complex (OEC), a tetranuclear manganese cluster associated with calcium (Mn4Ca), which after accumulating four oxidizing equivalents, catalyzes the oxidation of water to oxygen. The electrons liberated from water are ultimately transferred to NADPþ, producing NADPH, at the terminal side of PSI. In a manner analogous to processes of the cytochrome bc1 complex of purple photosynthetic bacteria, electron movement is coupled to formation of a proton gradient at the cytochrome b6f complex. Thus, a portion of the absorbed photonic energy is stored as reducing potential in NADPH and a portion as PMF (used for subsequent conversion of ADP to ATP). Both forms of these transient energy carriers are utilized in the Calvin-Benson-Basham cycle (34), where CO2 is converted to sugar (a reduced fuel). In this overall Z scheme (35–37), a minimum total of eight photons is required (four photo-induced reactions of PSII and PSI) for the consumption of two molecules of water and the production of one O2, two NADPH, and three ATP molecules (38). PSII is the only known biochemical system capable of oxidizing water to molecular oxygen (39–46); therefore, it has been extensively studied in the context of artificial energy transduction systems and is reviewed in the following section.
2.4. Photosystem II PSII is an !650 kDa dimeric membrane-spanning complex composed of more than 20 polypeptide subunits and numerous redox cofactors. Water is oxidized to molecular oxygen at one side of the membrane (the luminal side), and plasto-Q is reduced to plastoquinol at the other (the stromal side). Nearly all of the electron-transfer cofactors are coordinated by two nearly symmetrical chlorophyll-binding protein subunits (D1 and D2). The entire PSII dimer is surrounded by chlorophyll and carotenoid containing lightharvesting proteins (or in the case of cyanobacteria and some algae, phycobilisomes), which absorb photonic energy and transfer it to the reaction-center primary electron donor (P680). The reaction center is comprised of four chlorophyll a pigments located in the D1 core. Although the reaction centers of oxygenic photosynthetic organisms are considerably more complex than those found in bacterial photosynthetic organisms, the similarities are striking. The D1 and D2 proteins are functionally, and to some degree structurally, analogous to the L and M subunits in purple photosynthetic bacteria (47–49). Likewise, these two sets of proteins exhibit weak, but definite, sequence homology (50). Photonic energy is trapped, predominately by the outer antenna systems, and is transferred to photochemically activated reaction centers via the chlorophyll-binding proteins CP47 and CP43 (Figure 3). Excitation of P680 initiates a cascade of electron-transfer events beginning with transfer of an electron to a primary pheophytin (Pheo), forming the P680þ-Pheo– state in 2–21 picoseconds (40). This is followed by a second charge-stabilizing electron transfer from Pheo– to plasto-Q QA, occurring within a few hundred picoseconds. Despite the !26 A˚ separation in charges, this state (P680þ-PQA–) is unstable with respect to charge recombination (t ' 100 ms) (51). However, a redox-active tyrosine residue, YZ (D1Tyr161) prevents electron transfer from QA– to P680þ by reducing the oxidized primary donor (42, 51, 52). On the acceptor side, QA– transfers the electron to plasto-Q (QB) forming the semiplasto-Q species QB–. Following a second photoinitiated turnover of the reaction center, reduction of QB– is accompanied by proton uptake from the stroma. The www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.9
a
2PQ + 4e– + 4H+
ST R OM A
2PQH2 hν
hν Fe 2+
QA
QB
hν Pheo
Thylakoid membrane CP43
ChlZ P680
e–
D1
TyrD
TyrZ
D2
Cl –
Mn4Ca
23 kDa
OEC
Cyt b559 CP47
33 kDa 17 kDa
L UM EN
2H2O
O2 + 4H+ + 4e–
b P680* 2 ps BPheo
– 0.5
170–210 ps
E (V versus NHE)
11 ns 0.0
hν (1.8 eV)
QA 100–200 µs PQ QB PQH2 100 ms
900 µs
Cyt yt b559
0.5
2H2O 1.0
4H+ + O2
Fast
S0 30 µs S1 100 µs S2 350 µs S3 1.0 ms
ChlZ
500 ms
YZ
YD
1s
23–260 ns P680
Figure 3 (a) A schematic representation of the PSII complex and its antenna system, consisting of more than 20 protein subunits. The larger subunits are indicated by either name or molecular mass. Photonic energy is trapped predominantly by the outer antenna and transferred to the photochemically activated reaction centers via chlorophyll-binding proteins CP47 and CP43. Excitation of P680 initiates a cascade of electron-transfer events, proceeding from P680* to pheophytin (Pheo), QA, and onto QB; the ET pathway is marked by the solid arrows. Dashed arrows indicate secondary ET pathways, which may play a photoprotective role. On the donor side, electrons extracted from water at the luminally located Mn4Ca cluster are used to regenerate P680 via the redox mediator Tyrz. (b) Energy-kinetic diagram illustrating the redox chemistry of PSII.
plastoquinol species (QBH2) is released from the D1 binding site and replaced by another plasto-Q from the Q pool. The released plastoquinol diffuses to the cytochrome b6f complex, where electrons are transferred from plastoquinol to the plastocyanin (PC) protein. The mobile PC protein donates electrons to the oxidized primary donor of PSI (P700þ). Oxidation equivalents at the donor side of PSII are transferred via YZ to the OEC. 2.10
Moore
#
Brudvig
2.5. Storage and Catalysis During the process of photosynthetic energy conversion, light energy is ultimately stored in the form of chemical bonds (solar fuels). Catalysis, lowering of the activation energy requirements, is imperative for driving such reactions with visible light energy at near thermodynamic potentials. 2.5.1. Thermodynamic Considerations. The oxidation of water to molecular oxygen and hydrogen (2H2O ! O2 þ 2H2) is a thermodynamically demanding reaction (DGo ¼ 474 kJ mol–1 ¼ 4.92 eV) (Figure 4a). From an energetic perspective, hydrogen production (2Hþ þ 2e– ! H2) is approximately equivalent to other biochemical half reactions, such as the reduction of NADPþ or CO2. Hence, it is discussed here as a proxy for the various half reactions found in biology. At pH 7, a more biologically relevant pH, the formal potential (Eo0 ) for oxygen production (O2 þ 4e– þ 4Hþ ! 2H2O) is 0.81 V versus NHE (Figure 4b). Therefore, the theoretical minimum energy pathway for water oxidation requires four oxidation events, each occurring with an average energy of 0.81 eV (Figure 4c). The actual pathway can, however, have large variations in energy demand depending on the reaction
a
b
O2
–2
–1
0.70 V
H2O2
1.76 V
E (V versus NHE)
0
H 2O
1.23 V +1
H+
3 H2O2 + 2H+
4
pH
8
12
2H˙
4
O2 + 4H+
H+ + H˙
2
H– + H+
Minimum energy path 0.81 eV/electron
2H2O 0
H2
d
H2O + OH˙ + H+
1 0
0
H2O + O + 2H+ O2– + 4H+
2
2H+ + 2e – –1
Energy (eV)
Energy (eV)
H2
0.00 V
2H2O
0
0
c
4
O2 + 4H+ + 4e –
1
1
2
3
Electrons removed
H2 0
4
2H+ 0
1
Electrons added
2
Figure 4 (a) The Latimer diagrams for oxygen and hydrogen show the standard reduction potentials (in V versus NHE at pH ¼ 0; see panel b) connecting the various oxidation states. (b) The Pourbaix diagrams for the oxygen and hydrogen production half reactions illustrate the pH dependence of the formal potentials. (c–d) A modified version of the Frost diagram for (c) oxygen (45, 53) and (d) hydrogen illustrate the energy dependence (shown here in eV) of the individual electron-transfer steps for the oxygen and hydrogen production half reactions at pH 7 with a normal hydrogen electrode reference. www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.11
coordinate. For example, as illustrated in Figure 4c, the redox potentials of the individual oxidation events proceeding via H2O2 or an oxygen atom vary widely. For the H2O2 route (Figure 4c), redox potentials vary from %0.45 to 2.33 V versus NHE. The estimated redox potential of P680þ (!1.25 V versus NHE) implies that photosynthetic water oxidation proceeds by a mechanism involving highly optimized redox events. For comparison, the thermodynamics of hydrogen production (54, 55) are illustrated in Figure 4. Energy requirements for individual steps are dependent on the mechanism and source of electrons. Again, the chosen reference is the normal hydrogen electrode. Thus, at pH 7 hydrogen production requires a minimum of 0.83 eV, if provided the appropriate mechanism. The homolytic pathway (Figure 4d), proceeding with formation of two H# radicals, is most energetically demanding when the radicals are unstabilized. The heterolytic pathway, (Figure 4d) requiring the formation of hydride, occurs at a milder reduction potential. Although a platinum surface stabilizes homolytic intermediates, these examples (in water at pH 7) illustrate potential advantages of homogenous catalysis involving metalcenter-bound hydrides. Nature has developed efficient catalysts, hydrogenase enzymes found in many bacteria and some algae, for the reduction of protons to hydrogen. Likewise, these enzymes have been targets for chemical mimicry (56–65) and sought for direct use in solar energy conversion applications (66–69). Reviews of hydrogenases and their associated chemistry are available (70–72). 2.5.2. The Oxygen-Evolving Complex. P680þ is the most oxidizing redox cofactor known in biology. With a reduction potential of !1.25V versus NHE, it provides the thermodynamic driving force necessary for water oxidation. Though the oxidation of water to molecular oxygen requires removal of four electrons, electron-transfer reactions induced by the absorption of a photon provide only one oxidizing equivalent. In this regard, the OEC acts as a capacitor that is electrically connected to P680 via YZ, storing oxidation equivalents through four photoinduced one-electron-transfer events. Each oxidation state in the catalytic cycle is known as an S state, with S0 being the most reduced state and S4 the most oxidized. The S1 state is the dark-stable state, and the S4 to S0 transition is spontaneous and light independent (73, 74). In contrast to chemical and electrochemical water splitting, photosynthetic water oxidation proceeds with modest driving force as the OEC operates at near 0 overpotential with turnovers up to 50 molecules of O2 released per second. In addition to managing the flow of electrons and the release of molecular oxygen, proton movement away from the OEC (to the lumen) must be tightly controlled. Given the large difference in mass between electrons and protons, as well as the coupled nature of their transfer at the OEC, protons can only tunnel over limited distances of a few angstroms, whereas electrons are capable of tunneling over tens of angstroms (75–79). Hence, proton release at the OEC is likely rate limiting. Given these restraints, it is probable the OEC and its environment have been finely tuned to rapidly transfer protons away from the active site to the luminal surface of the protein. A detailed understanding of the structural and mechanistic details of the OEC is critical, as the reaction it catalyzes provides the paradigm for engineering direct solar fuel production systems based on inexpensive and earth-abundant materials. Current understanding of the OEC structure is based mainly on electron paramagnetic resonance (EPR) (80–85), X-ray crystallography (86–88), extended X-ray absorption fine structure (EXAFS) measurements (89–94), Fourier transform infrared spectroscopy (95, 96), and quantum mechanics/ molecular mechanics modeling (97). A number of thorough reviews regarding structural 2.12
Moore
#
Brudvig
details, as well as possible mechanisms of water oxidation at the OEC are available (45, 72, 98–102). EPR experiments have set the number of manganese atoms in the OEC at four (80, 81, 85), and a calcium atom has also been indicated as part of the OEC through biochemical (103, 104), EPR (81), EXAFS (94), and X-ray diffraction experiments (86). Crystal structures of PSII have resolved the electron density of the OEC and suggest an arrangement composed of a trimanganese cluster with a single dangler manganese at slightly longer distances from the core cluster. In the work of Ferreira et al. (86) (based on a 3.5 A˚ structure of PSII from the cyanobacterium Thermosynechococcus elongatus), X-ray anomalous difference maps, at the Mn adsorption edge and at wavelengths where Ca2þ has an anomalous difference, were used to model the OEC as a cuboidal Mn3Ca cluster bridged by oxo-atoms connected to a fourth Mn via a m-oxo-bridge. In addition, a bicarbonate ion was used to account for additional electron density at the active site. In the work of Loll ˚ structure of PSII also from the cyanobacterium Thermosyneet al. (87) (based on a 3.0 A chococcus elongatus), the OEC was modeled without oxo-bridges, and a slightly different positioning of the metals and ligands was used to fit the electron density. Interestingly, no electron density was observed at the position corresponding to the bicarbonate ion as in the work of Ferreira et al. More recently, Guskov et al. have reported on a 2.9 A˚ structure of PSII (again from the cyanobacterium Thermosynechococcus elongatus) (88). In this work, ˚ is a chloride, bound through a putative water molecule to the Mn4Ca cluster at 6.5 A suggested to serve a role in proton-transfer reactions, as it is close to two possible proton channels. In an effort to address concerns regarding X-ray-induced damage to the OEC structure during data collection (105), oriented EXAFS measurements (which involve a lower X-ray exposure), have been used to obtain information regarding the geometry of the metal atoms at the active site (89). Although the EXAFS technique allows precise measurement of metal-to-metal distances, such measurements cannot determine a unique structure, but rather narrows the selection of possible geometries. Thus, theoretical calculations have aided in developing chemically sensible models of the OEC by explicitly considering the perturbational influence of the surrounding protein environment according to state-ofthe-art quantum mechanics/molecular mechanics hybrid methods, in conjunction with the X-ray diffraction structure of PSII. The resulting models can be validated through direct comparisons with high-resolution EXAFS spectroscopic data (97, 106).
3. ARTIFICIAL PHOTOSYNTHETIC SYSTEMS Photosynthetic organisms operate at near 100% internal quantum efficiency (i.e., the percentage of absorbed photons that are converted to collected carriers) (107). However, energy storage efficiency (i.e., the fraction of power that is converted by the cell to a form with the potential to do work) is much lower. Values range from as high as !27% [when measured in plants under optimal conditions with little or no work being extracted (opencircuit) and photon flux expressed in terms of photons absorbed] to as low as > 1%–5% (when measured at steady state with the photon flux expressed in terms of available photons at intensities incident to the Earth’s surface) (41, 108, 109). By comparison, commercial single-junction silicon photovoltaic cells operate with an !15% electricitygeneration efficiency (based on incident solar radiation) and efficiencies over 40% can be obtained utilizing tandem multiband gap cells (110). These systems, however, do not www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.13
produce reduced fuels. Instead, electrical power is the product. Nevertheless, electrolysis systems, operating at !1 Amp/cm2, with a potential requirement of 1.75 V and an energy storage efficiency of !73% (53.5 kWh kg%1), are commercially available (111). Thus, three silicon photovoltaic cells, connected in series, can power a commercial electrolyzer, converting solar energy to hydrogen (a proxy for NADPH), with a total energy-storage efficiency of !11%. Currently, such applications are cost prohibitive for implementation at a global scale; hence the need for new materials and fundamental science. Designing low-cost artificial photosynthetic systems, capable of using sunlight to split water into its elements, has long been envisioned as a promising strategy for meeting human energy demands (112). Application of these concepts will require effective coupling of light capture, photochemical charge separation, and efficient catalysts (72, 66, 113– 114). A large body of work involving synthesis and characterization of molecular-based donor-acceptor systems, mimicking charge separation and energy transfer in natural photosynthesis (115–124), has contributed to and advanced the field of artificial photosynthesis. Likewise, water oxidation photocatalysts using a variety of metal oxides (125–130), (oxy)nitrides and oxysulfides (131), as well as catalysts that mimic aspects of the active sites in natural enzymes (65, 132–141), have been actively pursued in developing methods for solar energy storage. In this section, we review and compare selected examples of direct approaches to overall solar energy transduction that utilize components of the examples given above. In 1972, Fujishima and Honda reported the first example of photo-assisted water oxidation coupled to hydrogen production utilizing semiconducting n-type TiO2 electrodes under illumination with UV light (142). As initially reported, the system consists of an electrochemical cell in which a single-crystal rutile TiO2 electrode is connected to a platinum black electrode through an external load (diagrammed schematically in Figure 5). Anodic currents begin to flow upon illumination of the anode with wavelengths shorter 5
a
b
V
–0.5
TiO2 CB
H+/H2
1
2 3
TiO2 + 4 hν 4e – + 4p+ (excitation of TiO2 by light) 4p+
4H+
+ 2H2O O2 + (at the TiO2 electrode)
4e – + 4H+ 2H2 (at the platinum electrode)
hν
E (V versus NHE)
4
0.5 H2O/O2
hν (3.2 eV)
1.5
2.5
TiO2 VB
Figure 5 (a) Schematic of the Fujishima and Honda cell as reported in 1972. [Reprinted by permission from Macmillian Publishers Ltd (142).] Direct band gap excitation of TiO2 (3.2 eV) with ultraviolet (UV) light is coupled to the oxidation of water, producing oxygen, at the TiO2 electrode (1) and the formation of hydrogen at the cathode (2). The overall reaction is 2H2O ! O2 þ 2H2. The cathode and anode are separated by a glass frit (3) and provisions are made to measure the current (4) and voltage (5) of the device. (b) Energy level diagram for the photochemistry and relevant redox reactions occurring in the Fujishima and Honda cell. 2.14
Moore
#
Brudvig
than 415 nm (3.0 eV), corresponding to the bandgap of TiO2 (!3.0–3.2 eV). Likewise, the direction of the current suggests oxidation reactions (oxygen evolution) occur at the TiO2 anode, and reduction reactions (hydrogen evolution) occur at the platinum black cathode. Oxygen evolution was confirmed by analytical measurements and currents of a few milliamps were produced upon illumination with a 500 W xenon lamp. Quantum efficiency of the device was estimated to be !10% and a minimum energy storage efficiency of !1% can be achieved by production of H2 (143). Although the photo-assisted reaction seems to require a small applied voltage (as low as 0.25 V) when using single-crystal rutile TiO2, later work, employing wider band gap semiconductor materials (such as SrTiO3 and anatase TiO2), demonstrated photoinduced hydrogen production at zero applied potential (144, 145). Because these reactions require high-energy UV radiation, they are of limited use for solar fuel generation. In 1991, O’Regan and Gra¨tzel described a low-cost solar cell (Figure 6) based on dyesensitized semiconductor films (146). The working electrode is composed of a mesoporous TiO2 film deposited on a conductive glass substrate (typically fluorine-doped tin oxide or indium-doped tin oxide). The high surface area of the semiconductor material allows a monolayer of charge transfer dye (usually a ruthenium polypyridyl complex) to absorb a large portion of incident solar energy flux (!46%). The counter electrode is composed of conductive glass activated with a platinum catalyst. Unlike the Fujishima and Honda cell, the Gra¨tzel cell does not produce fuel or use water as a source of electrons. It is a singlethreshold device, involving a cyclic electron-transport system coupled to electricity generation. An electrolyte containing a redox mediator (typically triiodide/iodide dissolved in an organic solvent) is used to interface the photoanode with the cathode and complete the circuit. In this regard, the cyclic nature of the electron pathway is somewhat analogous to electron flow in bacterial photosynthesis (149).
a Semiconductor e–
Electrolyte
S+/S*
(S+/S* ) 2
e
–
(R/R–) 5
(S+/S– )
1–100 ps TiO2 CB
–0.25
∆V 1 hν
e–
–0.75
E (V versus NHE)
3
Dye
b
Conducting glass counter electrode
4 e– e–
Load
1 ms –1 s
1 μs 0.25
hν (1.6 eV)
0.75
I3–/ I – 10 ns
S+/S e–
e–
1.25
Figure 6 (a) Schematic of the dye-sensitized solar cell reported by, O’Regan and Gra¨tzel. [Reprinted by permission from Macmillian Publishers Ltd (146).] (b) Energy-kinetic diagram for the photochemistry and electron-transfer processes described in a previously reported dye-sensitized solar cell (147, 148). These lifetimes represent an estimate for general comparison. The time scales are dependent on the specific sensitizer and electrolyte conditions used. Also, experimental values obtained in the absence of some components of an operational cell may not reflect actual rates. www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.15
For dye-sensitized solar cells, the external and internal quantum efficiencies are typically reported in terms of incident photon-to-current efficiency (IPCE) and absorbed photon-to-current efficiency (APCE), respectively. IPCE is the product of the lightharvesting efficiency (LHE) of the dye at a given wavelength, the electron injection efficiency (Finj), and the charge collection efficiency (!C): IPCE ¼ LHE ( finj ( !c ¼ LHE ( APCE:
8:
APCE is simply the product of Finj and !c. Energy storage efficiency, typically reported as overall energy conversion efficiency (!), is a product of the short-circuit current density (JSC), the open-circuit voltage (VOC), and the fill factor (FF) according to Equation 9: !¼
power out Voc ( Jsc ( FF ¼ , power in Pin
9:
where Pin is the total solar incident on the cell (100 mW/cm2 for AM 1.5). As originally reported, the device operated with an IPCE > 80% and current densities > 12 mA/cm2. The overall energy conversion efficiency (!) was measured at 7.1%–7.9% under simulated solar light conditions and 12% in diffuse daylight. Following optimization of various system parameters, internal quantum efficiencies near unity and confirmed energy conversion efficiencies in excess of 10% have been reported (128, 150, 151). In 2008, Youngblood and colleagues designed a photo-assisted, water-splitting, dyesensitized solar cell (Figure 7) utilizing a heteroleptic (having more than one type of ligand) ruthenium polypyridyl dye that serves both as a sensitizer to TiO2 and a molecular bridging unit to a nanoparticulate iridium oxide water oxidation catalyst (IrO2)nH2O, !2-nm diameter) (152–154). One of the bipyridine moieties coordinating the ruthenium is functionalized with phosphonate groups, selective for binding the TiO2 anode, whereas another is functionalized with a malonate group, selective for binding to the IrO2)nH2O catalyst. The overall cell configuration consists of a three-electrode setup employing an H configuration.
a
b –0.5
Bias voltage e–
S+/S*
TiO2 TS
hν TiO2
e– O O
O N
P N N
O P O O
Ru2+
H2
H2O
O
N
O
N O
O
IrO2 · nH2O
O2
hν (1.8 eV)
0.5
370 µs
4H+ + O2 1.0
2H2O IrO2 · nH2O 2.2 ms
S+/S
1.5
TiO2
Dye-sensitized TiO2 film
H2O
e–
N
Pt
0.0
E (V versus NHE)
TiO2
2H+ H2
TiO2 CB
Pt
Figure 7 (a) Schematic of the water-splitting dye-sensitized solar cell reported by Youngblood et al. in 2009. (Adapted from Reference 153, figure 2, with permission from the American Chemical Society.) (b) An illustrative energy-kinetic diagram for the photochemistry and electron-transfer processes occurring in the water-splitting dye-sensitized solar cell displayed above. 2.16
Moore
#
Brudvig
In a typical experiment, the photoanode was irradiated with a 300 W xenon arc lamp (using a 410-nm long-pass filter) at potentials positive of %325 mV versus an Ag/AgCl, reference cell producing a measurable steady photocurrent (typically 10–30 mA). In addition, hydrogen and oxygen were detected at the cathode and anode, respectively, by gas chromatography. An external quantum yield of 4.5 ( 10%3 was estimated from the measured current density of 12.7 mA/cm2 when illuminated with a 450-nm light source at an intensity of 7.8 mW/cm2. A turnover number of 16 per dye molecule was determined from the total current produced over a 4 h period, at which point the photocurrent had decayed to a value commensurate with bare TiO2. Time-resolved spectroscopic studies indicate charge recombination between TiO2 and oxidized sensitizer is approximately an order of magnitude more rapid than charge shift from oxidized sensitizer to IrO2)nH2O; hence, the observed low quantum efficiencies and need for a bias potential. The system does illustrate the photo-assisted production of a reduced fuel (hydrogen) utilizing a dye-sensitized Fujishima-Honda cell incorporating principles of natural photosynthesis. In recent efforts to further advance the concepts referenced above, Brimblecomb and coauthors coupled a manganese-containing catalyst [(Mn4O4L6)þ, cubium] imbedded in a proton-conducting membrane (Nafion) to a dye-sensitized TiO2 photoanode (155). A schematic diagram of the device is illustrated in Figure 8. Unlike the cell reported by Youngblood and coworkers, both UV and visible photons are required for operation of the cell. UV light is presumably needed to induce the release of oxygen from cubium by activating a Mn O charge-transfer band [peaking at 350 nm (3.5 eV)] within the complex (156). Nonetheless, the device functions without the necessity of an external bias potential and the catalyst is composed of an Earth-abundant metal; both are desirable features of a practical photoelectrochemical cell. The overall cell configuration consists of a two-electrode setup (with the counter electrode used as reference). Illumination of the photoanode with a 100-mW/cm2 xenon-lamp white light source at wavelengths > 290 nm gives rise to a transient current. The authors interpret the presence of an initial sharp photocurrent spike as arising from injection of electrons from the excited-state ruthenium polypyridal dye into the TiO2 conduction band. This is followed by a second photocurrent peak that develops on a slower time scale. The secondary rise in photocurrent is consistent with regeneration of oxidized ruthenium dye, presumably via donation of an electron from the catalyst. The slow rise (seconds) of this
Conductive glass
e–
Dye
Nafion
Electrolyte
e – Ru*
Cathode
b
2H2 hν 2H2O
hν
e– Ru''/Ru'''
[Mn4O4L6]+
e–
O2
4 × 1 e– O C O
4e –
Dye
TiO2
O
C
Nafion
4 × 1e –
N
Ru N
4e –
hν
SO3–
N N
O
4H+
4 hν
N N
Mn
SO3–
O 2H2O Mn O Mn O2 H+ Diffusion Mn O SO3H SO H SO3– SO3H 3 SO3– SO3–
O
Electrolyte
a
FTO-coated glass
TiO2
Figure 8 (a) Cross-sectional arrangement of the photoelectrochemical cell reported by Brimblecomb and coauthors. (b) A schematic diagram of the same cell showing the proposed operation of the device. (Adapted from Reference 155, figure 1, with permission from the American Chemical Society.) Abbreviation: FTO, fluorine-doped tin oxide. www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.17
secondary photocurrent suggests charge transfer between the catalyst and oxidized ruthenium dye is rate limiting. A turnover frequency of 47 * 10 O2 molecules per cluster per hour and 41 * 9 electrons per dye per hour was estimated from the peak photocurrent generated (31 * 7 mA). Charge collected over 2 h equates to 13 O2 molecules per Mn cluster and 11 electrons per dye molecule. Production of O2 was confirmed using a Clarke electrode and measured O2 yields were within 10% of the yield calculated from collected charge. IPCE measurements yield a peak external quantum yield of 1.7% upon excitation at wavelengths corresponding to the maximum in the absorption band of the ruthenium polypyridal metal-to-ligand charge-transfer band.
4. MAXIMUM EFFICIENCIES AND THEORETICAL LIMITS In accordance with the Shockley-Queisser efficiency limit, single-junction photovoltaic systems have a theoretical maximum energy conversion efficiency of !33% (157). Such limitations arise from four unavoidable loss mechanisms: 1. incomplete absorption of the available incident solar energy, given that photons with energy lower than the absorption threshold (Eg) of the reaction center are not absorbed; 2. photons with energy greater than Eg are thermalized to energies matching the absorption threshold (carrier cooling); 3. the photovoltage is always less than Eg, given thermodynamic losses; and 4. a fraction of the excited-states radiatively recombines with the ground states. On the basis of these considerations, the ideal bandgap for a single-threshold device is !1.3 eV (925 nm). For tandem cells, using dual absorbers, the Shockley-Queisser efficiency limit is extended to !46% energy conversion efficiency, with absorption thresholds of !1.63 eV (761 nm) and !0.95 eV (1,305 nm) (110). These calculations exemplify that for oxygenic photosynthetic organisms, threshold energies of the reaction-center pigments (680 and 700 nm) allow for only !1/2 the available incident photons to be absorbed. Although the use of tandem photochemical systems allows for the generation of relatively large photovoltages capable of using water as a source of electrons to reduce NADPþ, similarities in effective band gaps, result in !1/2 the energy efficiency that could be obtained in a single-threshold system. The correspondence in absorption thresholds of PSII and PSI reaction centers is likely due to evolutionary constraints.
5. CONCLUSIONS AND CLOSING REMARKS Advancements in the field of artificial photosynthesis illustrate the potential to design and build human constructs employing the fundamental principles of photosynthetic energy conversion. In general, these systems will require drastic improvement in efficiency and stability before consideration for practical applications. With regard to the artificial systems reviewed here, low quantum and energy storage efficiencies are serious issues. These yields, in large part, reflect slow electron-transfer kinetics between the catalyst and photoxidized sensitizer, as well as fast back electron transfer from TiO2. Incorporation of a catalyst to accomplish water oxidation by PSII likely did not occur without intermediate stages. These include 2.18
Moore
#
Brudvig
1. the need for a more oxidizing reaction center capable of meeting the thermodynamic requirements necessary for water oxidation; 2. the progressive shifting of the reaction-center pigment from absorption thresholds in the near infrared to the red, thereby increasing the effective bandgap (i.e., the conversion of BChl a and BChl b to chlorophyll a and chlorophyll b; and 3. the incorporation of protection mechanisms to avoid oxidative damage including nonphotochemical quenching (14–17) and frequent replacement (approximately once every 30 min) of the entire D1 complex (158). Similar strategies may prove useful in developing artificial systems, most notably the need for new dyes with higher potentials that maximize forward rates of electron transfer, with respect to the exponential factor in Equation 7. This is in contrast to an approach used to increase the energy conversion efficiency of Gra¨tzel-type dye-sensitized solar cells, where the aim is to lower the ground state potential (Sþ/S) of the dye while keeping the excitedstate potential (Sþ/S*) constant and poised negative of the TiO2 conduction band. Here, the desired effect is to shift the optical band gap (the E0–0 transition) of the sensitizer to longer wavelengths, thereby absorbing a greater fraction of incident light and increasing the associated current density (JSC). The use of high-potential pigments provides an additional issue to contend with. Namely, excited-state potentials are tied to ground state potentials via the E0–0 transition in accordance with the Rehm-Weller Equation (159, 160). Thus, shifting the ground state potential to more positive potentials, without altering the optical properties of the dye, will also shift the excited-state potential in the same direction, by the same magnitude, adversely affecting electron-transfer dynamics between the excited-state dye and the TiO2 conduction band. Shifting the absorption spectrum of the dye to shorter wavelengths (an approach taken by nature) avoids this issue; yet, this comes at the expense of further decreasing the match to the solar spectrum. A second solution would be to change the semiconductor to one with a more positive conduction band. This, however, still raises additional issues, as the semiconductor conduction band in TiO2 is only slightly negative of the proton/hydrogen couple. Therefore, any shifting of the conduction band to more positive values is likely to make hydrogen production at the counter electrode thermodynamically unfavorable. Taking inspiration from nature, the use of tandem cells wired in electrical series, with one photosystem handling the oxidative chemistry (at more positive potentials) and another the reductive chemistry (at more negative potentials), avoids the issues mentioned above. In addition, the tandem cell could absorb photons over a larger spectral range if the photosystems were stacked in optical series. In accordance with the Shockley-Queisser efficiency limit, ideal absorption thresholds of the two photosystems should be near 761 and 1,305 nm (110). Unlike the natural photosynthetic apparatus, such an artificial Z scheme would provide a superior match to the solar spectrum. The incorporation of artificial antenna systems, with the ability to effectively shuttle excitation energy to reaction centers, is another approach to extending spectral coverage, albeit only to frequencies higher than that of the reaction center’s threshold. This approach does, however, provide a mechanism for maximizing turnover at reaction centers and preventing undesirable charge-recombination reactions, as a relatively large number of dyes could potentially service one catalytic site. For photosynthetic active light (400– 700 nm), at full sun, the photon flux (1,800 mEm%2s%2) is such that a chlorophyll pigment www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.19
absorbs light at a rate of approximately one photon every 100 ms (41). These factors, coupled with the relative instability of photochemical intermediates, demand that photosynthetic organisms efficiently collect and transfer photonic energy to reaction centers. Similar approaches may prove necessary in artificial systems seeking to interface multielectron catalytic chemistry with the inherently single-electron nature of photochemistry. Covalently linked arrays of light-harvesting pigments, that funnel excitation energy to a central site capable of inducing charge separation, have been demonstrated in artificial systems; however, the preparation of such arrays requires considerable effort (117, 122). More ambitious goals include the incorporation of self-assembly and repair mechanisms. This is perhaps the most intriguing aspect of biological organisms and is essential to the natural photosynthetic process. There are few examples of human-made constructs possessing the dynamic ability to sense and repair damage occurring during operation. Kanan and Nocera have described an electrodeposited water oxidation catalyst composed of cobalt and phosphate that forms in the presence of an applied potential (operating at 1 mA/cm2, with an overpotential of 0.41 V to oxidize water at pH 7) (141, 161–164). Details of the catalyst structure remain unknown; still, the use of earth-abundant materials, operation in water at neutral pH, and in situ assembly captures several enticing features of the OEC. Although the system is capable of turnover when the potential is applied by an electrode surface, where there is a high density of states and delocalized metallic orbitals, it is not yet clear if such a system will be capable of interfacing with the discrete and localized orbitals provided by molecular-based charge-separating networks composed of organic or inorganic constituents. Recent results, however, have demonstrated formation of the catalyst on mesostructured hematite (a-Fe2O3) photoanodes resulting in a > 350 mV cathodic shift of the onset potential for photoelectrochemical water oxidation and a significantly increased IPCE (18% at 450 nm with a 1 V versus RHE bias) in comparison with native a-Fe2O3 photoanodes (165, 166). The development of cost-effective alternative energy sources to meet human energy demands in an environmentally responsible manner is critical to mitigating anthropogenic climate change and achieving energy security. Solar energy provides a resource that is abundant yet virtually untapped. Although the fundamental technology for carrying out solar-induced conversion of water to hydrogen is commercially available (silicon photovoltaics coupled with water electrolyzers), the cost of these systems in comparison with fossil fuels remains a significant barrier to their implementation. Natural photosynthesis offers many desirable features; yet, only the most efficient components of photosynthesis should be a direct target for chemical mimicry (167). Many aspects of photosynthesis, including a poor match of the solar spectrum (!400–700 nm for oxygen-evolving photosynthetic organisms versus !400–1,000 nm of solar irradiance), are rather inefficient. To date, the study of artificial photosynthetic systems has allowed for rigorous analyses of the thermodynamic and kinetic properties of electron and energy transfer as a function of donor/acceptor distance, orientation, driving force, orbital overlap, and symmetry properties of the system, thus providing the fundamental rules for their design, construction, and operation (115–124). In most cases, the preparation of such constructs requires considerable effort and leaves much to be desired in terms of stability and scalability. The challenges presented here are indeed great, requiring technological, economic, and policydriven considerations. The need for innovative solutions, however, should not be understated nor postponed, as the environmental and energy-related issues involved are crucial to the long-term well-being of all future generations. 2.20
Moore
#
Brudvig
DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS This work was supported by the Office of Basic Energy Sciences of the U.S. Department of Energy (DE-FG02-07ER15909) for funding work on artificial photosynthesis, the National Institutes of Health Grant GM32715 for funding work on natural photosynthesis, and the Camille & Henry Dreyfus Foundation. G.F.M. is grateful to the Yale Green Energy Consortium for many fruitful discussions.
LITERATURE CITED 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29.
Int. Energy Outlook. 2009. May, Rep., Washington, D.C.: U.S. Dep. Energy Hoffert MI, Caldeira K, Jain AK, Haites EF, Harvey LDD, et al. 1998. Nature 395:881–84 Lewis NS, Nocera DG. 2006. Proc. Natl. Acad. Sci. USA 103:15729–35 U.S. Dep. Energy. 2007. Basic Research Needs: Catalysis for Energy. Rep. Aug. Washington, D.C.: U.S. Dep. Energy IPCC. 2007. Summary for policy makers. Rep. Cambridge, UK/New York: Cambridge Univ. Press Arrhenius S. 1896. Phil. Mag. J. S. 41:239–76 U.S. Dep. Energy. 2008. New sciences for a secure and sustainable energy future. Rep. Dec. Washington, D.C.: U.S. Dep. Energy U.S. Dep. Energy. 2007. Directing Matter and Energy: Five Challenges for Science and the Imagination. Rep. Dec. Washington, D.C.: U.S. Dep. Energy Archer MD, Barber J, eds. 2004. Molecular to Global Photosynthesis. London: Imperial Coll. Press. Pearlstein RM. 1996. Photosynth. Res. 48:75–82 Bernhardt K, Trissl H-W. 1999. Biochim. Biophys. Acta-Bioenergetics 1409:125–42 Marcus RA, Sutin N. 1985. Biochim. Biophys. Acta-Bioenergetics 811:265–322 Forster T. 1948. Ann. Physik [6 Folge] 2:55–75 Krieger-Liszkay A, Fufezan C, Trebst A. 2008. Photosynth. Res. 98:551–64 Barber J, Andersson B. 1992. Trends Biochem. Sci. 17:61–66 Holt NE, Fleming GR, Niyogi KK. 2004. Biochemistry 43:8281–89 Dreuw A, Fleming GR, Head-Gordon M. 2005. Biochem. Soc. Trans. 33:858–62 Niyogi KK. 1999. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:333–59 Dexter DL. 1953. J. Chem. Phys. 21:836–50 Scholes GD, Jordanides XJ, Fleming GR. 2001. J. Phys. Chem. B 105:1640–51 Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL. 1992. Nature 355:796–802 Gray HB, Winkler JR. 1996. Annu. Rev. Biochem. 65:537–61 Chidsey CED. 1991. Science 251:919–22 Bard AJ, Faulkner LR. 2001. Electrochemical Methods: Fundamentals and Applications. New York: Wiley. 856 pp. 2nd ed. Futai M, Noumi T, Maeda M. 1989. Annu. Rev. Biochem. 58:111–36 Hoff AJ, Deisenhofer J. 1997. Phys. Rep. 287:1–247 Woodbury NW, Allen JP. 1995. Adv. Photosynth. 2:527–57 Ortega JM, Drepper F, Mathis P. 1999. Photosynth. Res. 59:147–57 Okamura MY, Paddock ML, Graige MS, Feher G. 2000. Biochim. Biophys. Acta-Bioenergetics 1458:148–63 www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.21
30. 31. 32. 33. 34. 35. 36. 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 48. 49. 50. 51. 52. 53. 54. 55. 56. 57. 58. 59. 60. 61. 62. 63. 64. 65. 66. 67. 68. 69. 70. 71. 72. 73. 2.22
Crofts AR, Berry EA. 1998. Curr. Opin. Struct. Biol. 8:501–9 Berry EA, Guergova-Kuras M, Huang L-S, Crofts AR. 2000. Annu. Rev. Biochem. 69:1005–75 Mitchell P. 1976. J. Theor. Biol. 62:327–67 Bolton JR, Hall DO. 1979. Annu. Rev. Energy 4:353–401 Gontero B, Lebreton S, Graciet E. 2002. Annu. Plant Rev. 7:120–50 Hill R, Bendall F. 1960. Nature 186:136–7 Duysens LNM, Amesz J, Kamp BM. 1961. Nature 190:510–1 Duysens LNM. 1989. Photosynth. Res. 21:61, 64–79 Kramer DM, Sacksteder CA, Cruz JA. 1999. Photosynth. Res. 60:151–63 Deisenhofer J, Norris JG. 1993. The Photosynthetic Reaction Center. San Diego: Acad. Press. 574 pp. Ort D, Yocum C. 1996. Oxygenic Photosynthesis: The Light Reactions. Dordrecht: Kluwer Acad. Blankenship RE. 2002. Molecular Mechanisms of Photosynthesis. Oxford, UK: Blackwell Sci. Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, et al. 1989. Biochemistry 28:9557–65 Barber J. 1998. Biochim. Biophys. Acta-Bioenergetics 1365:269–77 Rutherford AW, Faller P. 2003. Ser. B 358:245–53 McEvoy JP, Brudvig GW. 2006. Chem. Rev. 106:4455–83 Radmer R, Kok B. 1975. Annu. Rev. Biochem. 44:409–33 Michel H, Deisenhofer J. 1988. Biochemistry 27:1–7 Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, et al. 2001. Nature 409:739–43 Diner BA, Rappaport F. 2002. Annu. Rev. Plant Biol. 53:551–80 Michel H, Deisenhofer J. 1990. Quantum Chem. Biochem. 22:1–9 de Wijn R, van Gorkom HJ. 2002. Biochim. Biophys. Acta-Bioenergetics 1553:302–8 Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA, Lavergne J. 2002. Biochemistry 41: 8518–27 Radmer R, Cheniae G. 1977. Topics in Photosynthesis. Vol. 2. Amsterdam: Elsevier Parker VD. 1992. J. Am. Chem. Soc. 114:7458–62 Wayner DDM, Parker VD. 1993. Acc. Chem. Res. 26:287–94 Liu X, Ibrahim SK, Tard C, Pickett CJ. 2005. Coord. Chem. Rev. 249:1641–52 Mealli C, Rauchfuss TB. 2007. Angew. Chem. Int. Ed. 46:8942–4 Tard C, Liu X, Ibrahim SK, Bruschi M, De Gioia L, et al. 2005. Nature 433:610–13 Li Z, Ohki Y, Tatsumi K. 2005. J. Am. Chem. Soc. 127:8950–51 Ogo S, Kabe R, Uehara K, Kure B, Nishimura T, et al. 2007. Science 316:585–87 Jones AK, Lichtenstein BR, Dutta A, Gordon G, Dutton PL. 2007. J. Am. Chem. Soc. 129: 14844–45 Rakowski DuBois M, DuBois DL. 2009. Chem. Soc. Rev. 38:62–72 Tard C, Pickett CJ. 2009. Chem. Rev. 109:2245–74 Gloaguen F, Rauchfuss TB. 2009. Chem. Soc. Rev. 38:100–8 Le Goff A, Artero V, Jousselme B, Tran PD, Guillet N, et al. 2009. Science 326:1384–87 Hambourger M, Moore GF, Kramer DM, Gust D, Moore AL, Moore TA. 2009. Chem. Soc. Rev. 38:25–35 Woolerton TW, Sheard S, Reisner E, Pierce E, Ragsdale SW, Armstrong FA. 2010. J. Am. Chem. Soc. 132:2132–33 Ghirardi ML, Dubini A, Yu J, Maness P-C. 2009. Chem. Soc. Rev. 38:52–61 Lubner CE, Grimme R, Bryant DA, Golbeck JH. 2010. Biochemistry 49:404–14 Evans DJ, Pickett CJ. 2003. Chem. Soc. Rev. 32:268–75 Vincent KA, Parkin A, Armstrong FA. 2007. Chem. Rev. 107:4366–413 Lubitz W, Reijerse EJ, Messinger J. 2008. Environ. Sci. 1:15–31 Kok B, Forbush B, McGloin M. 1970. Photochem. Photobiol. 11:457–75
Moore
#
Brudvig
74. 75. 76. 77. 78. 79. 80. 81. 82. 83. 84. 85. 86. 87. 88. 89. 90. 91. 92. 93. 94. 95. 96. 97. 98. 99. 100. 101. 102. 103. 104. 105. 106. 107. 108. 109. 110. 111. 112. 113. 114. 115.
Joliot P, Barbieri G, Chabaud R. 1969. Photochem. Photobiol. 10:309–29 Cukier RI, Nocera DG. 1998. Annu. Rev. Phys. Chem. 49:337–69 Hammes-Schiffer S. 2001. Acc. Chem. Res. 34:273–81 Mayer JM. 2004. Annu. Rev. Phys. Chem. 55:363–90 Meyer TJ, Huynh MHV, Thorp HH. 2007. Angew. Chem. Int. Ed. 46:5284–304 Chang CJ, Chang MCY, Damrauer NH, Nocera DG. 2004. Biochim. Biophys. Acta-Bioenergetics 1655:13–28 Dismukes GC, Siderer Y. 1981. Proc. Natl. Acad. Sci. USA 78:274–78 De Paula JC, Beck WF, Brudvig GW. 1986. J. Am. Chem. Soc. 108:4002–9 Kim SH, Gregor W, Peloquin JM, Brynda M, Britt RD. 2004. J. Am. Chem. Soc. 126:7228–37 Miller AF, Brudvig GW. 1991. Biochim. Biophys. Acta-Bioenergetics 1056:1–18 Koulougliotis D, Shen J-R, Ioannidis N, Petrouleas V. 2003. Biochemistry 42:3045–53 Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, et al. 2000. J. Am. Chem. Soc. 122:10926–42 Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Science 303:1831–38 Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. 2005. Nature 438:1040–44 Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. 2009. Nat. Struct. Mol. Biol. 16:334–42 Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, et al. 2006. Science 314:821–25 Haumann M, Mueller C, Liebisch P, Iuzzolino L, Dittmer J, et al. 2005. Biochemistry 44: 1894–908 Haumann M, Liebisch P, Mueller C, Barra M, Grabolle M, Dau H. 2005. Science 310:1019–21 Robblee JH, Cinco RM, Yachandra VK. 2001. Biochim. Biophys. Acta-Bioenergetics 1503:7–23 Yachandra VK, Sauer K, Klein MP. 1996. Chem. Rev. 96:2927–50 Cinco RM, McFarlane HKL, Robblee JH, Yano J, Pizarro SA, et al. 2002. Biochemistry 41:12928–33 Debus RJ, Strickler MA, Walker LM, Hillier W. 2005. Biochemistry 44:1367–74 Noguchi T. 2008. Coord. Chem. Rev. 252:336–46 Sproviero EM, Gasco´n JA, McEvoy JP, Brudvig GW, Batista VS. 2008. J. Am. Chem. Soc. 130:3428–42 Brudvig GW. 2008. Phil. Trans. R. Soc. B 363:1211–19 Siegbahn PEM. 2009. Acc. Chem. Res. 42:1871–80 Dau H, Zaharieva I. 2009. Acc. Chem. Res. 42:1861–70 Barber J. 2009. Chem. Soc. Rev. 38:185–96 Tommos C, Babcock GT. 1998. Acc. Chem. Res. 31:18–25 Vrettos JS, Stone DA, Brudvig GW. 2001. Biochemistry 40:7937–45 Ghanotakis DF, Babcock GT, Yocum CF. 1984. FEBS Lett. 167:127–30 Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, et al. 2005. Proc. Natl. Acad. Sci. USA 102:12047–52 Sproviero EM, Gasco´n JA, McEvoy JP, Brudvig GW, Batista VS. 2008. J. Am. Chem. Soc. 130:6728–30 Wraight CA, Clayton RK. 1974. Biochim. Biophys. Acta-Bioenergetics 333:246–60 Zhu X-G, Long SP, Ort DR. 2008. Curr. Opin. Biotechnol. 19:153–59 Gust D, Kramer D, Moore A, Moore TA, Vermaas W. 2008. MRS Bull. 33:383–87 Hanna MC, Nozik AJ. 2006. J. Appl. Phys. 100:074510 Ivy J. 2004. Summary of electrolytic hydrogen production: milestone completion report. September, 2004. Rep., Natl. Renewable Energy Lab., Golden, Colo. Ciamician G. 1912. Science 36:385–94 Kamat PV. 2007. J. Phys. Chem. C 111:2834–60 Meyer GJ. 2005. Inorg. Chem. 44:6852–64 Meyer TJ. 1989. Acc. Chem. Res. 22:163–70 www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.23
116. 117. 118. 119. 120. 121. 122. 123. 124. 125. 126. 127. 128. 129. 130. 131. 132. 133. 134. 135. 136. 137. 138. 139. 140. 141. 142. 143. 144. 145. 146. 147. 148. 149. 150. 151. 152. 153. 154. 155. 156. 157. 2.24
Gust D, Moore TA, Moore AL. 2001. Acc. Chem. Res. 34:40–48 Gust D, Moore TA, Moore AL. 1993. Acc. Chem. Res. 26:198–205 Wasielewski MR. 1992. Chem. Rev. 92:435–61 Lomoth R, Magnuson A, Sjo¨din M, Huang P, Styring S, Hammarstro¨m L. 2006. Photosynth. Res. 87:25–40 Sun L, Hammarstrom L, Akermark B, Styring S. 2001. Chem. Soc. Rev. 30:36–49 Balzani V, Moggi L, Scandola F. 1987. NATO ASI Ser. C 214:1–28 Holten D, Bocian DF, Lindsey JS. 2002. Acc. Chem. Res. 35:57–69 Fukuzumi S. 2008. Phys. Chem. Chem. Phys. 10:2283–97 Flamigni L, Collin J-P, Sauvage J-P. 2008. Acc. Chem. Res. 41:857–71 Harriman A, Pickering IJ, Thomas JM, Christensen PA. 1988. J. Chem. Soc., Faraday Trans. I 84:2795–806 Jiao F, Frei H. 2009. Angew. Chem. Int. Ed. 48:1841–44 Gra¨tzel M. 2005. Chem. Lett. 34:8–13 Gra¨tzel M. 2001. Nature 414:338–44 Osterloh FE. 2008. Chem. Mater. 20:35–54 van de Krol R, Liang Y, Schoonman J. 2008. J. Mater. Chem. 18:2311–20 Maeda K, Domen K. 2007. J. Phys. Chem. C 111:7851–61 Breslow R. 1995. Acc. Chem. Res. 28:146–53 Ru¨ttinger W, Dismukes GC. 1997. Chem. Rev. 97:1–24 Cady CW, Crabtree RH, Brudvig GW. 2008. Coord. Chem. Rev. 252:444–55 Yagi M, Kaneko M. 2001. Chem. Rev. 101:21–35 Mukhopadhyay S, Mandal SK, Bhaduri S, Armstrong WH. 2004. Chem. Rev. 104:3981–4026 Manchanda R, Brudvig GW, Crabtree RH. 1995. Coord. Chem. Rev. 144:1–38 Rakowski Dubois M, Dubois DL. 2009. Acc. Chem. Res. 42:1974–82 Dempsey JL, Brunschwig BS, Winkler JR, Gray HB. 2009. Acc. Chem. Res. 42:1995–2004 Morris AJ, Meyer GJ, Fujita E. 2009. Acc. Chem. Res. 42:1983–94 Kanan MW, Nocera DG. 2008. Science 321:1072–75 Fujishima A, Honda K. 1972. Nature 238:37–38 Wrighton MS, Ginley DS, Wolczanski PT, Ellis AB, Morse DL, Linz A. 1975. Proc. Natl. Acad. Sci. USA 72:1518–22 Wrighton MS, Ellis AB, Wolczanski PT, Morse DL, Abrahamson HB, Ginley DS. 1976. J. Am. Chem. Soc. 98:2774–79 Rao MV, Rajeshwar K, Verneker VRP, DuBow J. 1980. J. Phys. Chem. 84:1987–91 O’Regan B, Gra¨tzel M. 1991. Nature 353:737–40 Nazeeruddin MK, Kay A, Rodicio I, Humphry-Baker R, Mueller E, et al. 1993. J. Am. Chem. Soc. 115:6382–90 Hagfeldt A, Graetzel M. 1995. Chem. Rev. 95:49–68 McConnell I, Li G, Brudvig GW. 2010. Chem. Biol. 17:434–47 Nazeeruddin MK, Pe´chy P, Renouard T, Zakeeruddin SM, Humphry-Baker R, et al. 2001. J. Am. Chem. Soc. 123:1613–24 Gra¨tzel M. 2005. MRS Bull. 30:23–27 Youngblood WJ, Lee S-HA, Kobayashi Y, Hernandez-Pagan EA, Hoertz PG, et al. 2009. J. Am. Chem. Soc. 131:926–27 Youngblood WJ, Lee S-HA, Maeda K, Mallouk TE. 2009. Acc. Chem. Res. 42:1966–73 Gust D, Moore TA, Moore AL. 2009. Acc. Chem. Res. 42:1890–98 Brimblecombe R, Koo A, Dismukes GC, Swiegers GF, Spiccia L. 2010. J. Am. Chem. Soc. 132:2892–94 Brimblecombe R, Swiegers GF, Dismukes GC, Spiccia L. 2008. Angew. Chem. Int. Ed. 47: 7335–38 Shockley W, Queisser HJ. 1961. J. Appl. Phys. 32:510–19
Moore
#
Brudvig
158. 159. 160. 161. 162. 163. 164. 165. 166. 167.
Murray JW, Barber J. 2007. J. Struct. Biol. 159:228–37 Rehm D, Weller A. 1969. Ber. Bunsenges. Phys. Chem 73:834–39 Rehm D, Weller A. 1970. Isr. J. Chem. 8:259–71 Surendranath Y, Dinca M, Nocera DG. 2009. J. Am. Chem. Soc. 131:2615–20 Lutterman DA, Surendranath Y, Nocera DG. 2009. J. Am. Chem. Soc. 131:3838–39 Kanan MW, Surendranath Y, Nocera DG. 2009. Chem. Soc. Rev. 38:109–14 Nocera DG. 2009. Inorg. Chem. 48:10001–17 Zhong DK, Sun J, Inumaru H, Gamelin DR. 2009. J. Am. Chem. Soc. 131:6086–87 Zhong DK, Gamelin DR. 2010. J. Am. Chem. Soc. 132:4202–7 Rutherford AW, Moore TA. 2008. Nature 453:449
www.annualreviews.org
#
Energy Conversion in Photosynthesis
2.25
