Natural photosystems have been extensively studied and the machinery of photosynthesis found to be highly modular, organized on multiple scale levels and compart-mentalized.32 Importantly, all natural photosystems are molecule-based and their function can be understood both at the schematic level and, in many cases, at the molecular-level. Highly specialized components interact in controlled manner to ultimately deliver a product (reduction equivalents) and to effectively deal with waste (oxidation equivalents).
The bacterial photosystem functions without dioxygen production which simplifies the task at hand. Namely, electrons are obtained from more easily oxidized terminal electron donors such as H2S instead of water. Nonetheless, the basic design needed to transform solar energy into stored chemical energy is present. The protein subunits and cofactors that comprise the photosystem in purple bacteria, such as Rhodobacter (Rb.) sphaeroides and Rhodopseudomonas (Rps.) viridis,33 are shown schematically in Fig. 1 which is based on a crystal structure of this assembly.34
The sensitizer in this photosystem, P865, is a symmetric bacteriochlorophyll dimer (labeled Dm and Dl in Fig. 1) which has a strong absorption at 865 nm corresponding to 1.43 eV. In the trans-cellular membrane assembly, the photoexcited P865* initiates charge separation by electron transfer down just one side of the photosynthetic assembly (the L side) as indicated by the arrows in Fig. 1. The reason for this asymmetry in electron transfer is still unclear, however, it is clear that electron transfer through a series of acceptor units: Bl to ^l to Qa and finally Qb, leads of a charge separated complex with very slow (~ 1 sec) back rates. The P865+ cation is a modest oxidant, (Ered = +0.45 V, and is reduced to the starting state by external reductants such as H2S. The reducing potential stored in Qb is utilized in the cell (localized on the cytoplasmic side of the photosynthetic complex) to convert NADP+ to NADPH. Thus, the net chemical reaction is:
The structure and function of this bacterial photosystem reveals important principles for the design of artificial photosystems. First, the sensitizer needs to be positioned close to secondary acceptors and donors which themselves are spatially isolated from each other such that photoexcitation leads to rapid spatial separation of the electron-hole pair. Second, compartmentalization of the photosynthetic assembly is likely to be necessary so as to prevent wasteful back reactions. For water-splitting, a system in which H2 and O2 are generated in separate compartments would have both safety and efficiency advantages.
In green plants and certain algae, the photosynthetic machinery is elaborated over those found in purple bacteria and is now able to reach the high potentials needed to oxidize water to dioxygen. This oxygenic photosystem is comprised of two photosynthetic reaction centers (sensitizer assemblies), photosystem I (PS I) and
photosystem II (PS II) and thus requires more photons to drive the overall reac-tion.While the details have changed upon moving from the bacterial photosystem to PS I, the principle remains that PS I is unable to reach the potentials required to oxidize water. Figure 2 shows the classic Z scheme, first proposed in 1960 by Hill and Bendall35 and subsequently elaborated many times,36-38 which indicates how the two photosystems work together. The two sensitizers or reaction centers for PS I and PS II are again chlorophyll dimers such as found in bacteria, however these chlorophylls absorb at higher energies, 700 and 680 nm, and transiently store more energy. The special pairs for PSI and PSII are denoted P700 and P680, respectively, and excitation of these reaction centers either by direct light absorption or by energy-transfer from an antenna assembly results in charge separation.
A schematic view of the cofactor arrangement in PSII is shown in Fig. 3.39 The reducing potential of the P680* complex (--0.58 V) is used to shuttle an electron down a chain of redox acceptors in the PS II complex (pheotyphytin (phe/phe- at -0.42 V) to quinone A (Qa/ Qa- at -0.08 V) to quinone B (Qb/ Qb-))40 and onto an
external protein acceptor, plastoquinone. Reduced plastoquinone feeds another redox chain in which the reducing potential of these electrons are used to translocate protons across the membrane and thus generate a proton gradient to be used by the cell to generate ATP from ADP.41 The oxidizing potential of the P680+ cation is estimated at +1.25 V40,42 which is highly oxidizing and rapidly oxidizes the nearby tyrosine Z (Yz/Yz+ at +1.21 V). Ten microseconds after excitation, the electron-hole pair is mostly localized as [Yz+/Qa-]. The tyrosine radical cation is positioned near the tetra-nuclear manganese oxygen evolving center (OEC) and possibly even coordinates to the Ca2+ site based on recent X-ray structural data.43 Four sequential excitations (the 'S-state cycle') removes four electrons from the OEC with the last oxidation con-commitent with the evolution of O2 and regeneration of the starting state of the OEC.44 The structure of the OEC in PSII has recently been determined at resolutions as low as 3.2 A43,45,46 which is where the structural 'cubane' model43 shown in Figure 3 originates. The structure must be viewed with caution as there is some criticism of the co-factor structure due to the resolution of the data47 and the possibility of X-ray damage to the OEC cofactor during data collection.48 Nonetheless, this cubane structure incorporates most of the spectroscopic and compositional data known for PSII and serves as a useful model for the active site of oxygen evolution.
Photosystem I forms the second light-absorbing component in the Z scheme for green plants and algae and like PS II, the structure of the protein complexes has been determined by X-ray crystallography.34,49-51 PS I is similar in function to that of the purple bacterial photosystem in that the oxidation potential generated is modest (P700+/P700 at ~ +0.5 V), however, the primary function of this photosystem is to
generate a reducing potential for the generation of NADPH. The electrons for this process come from plastocyanin that is the terminal reduced product from PS II.
Both PSI and PSII are membrane proteins which span the thylakoid membranes in chloroplasts.52 As indicated in Fig. 2, the luminal side of the membrane is where water is oxidized to O2 and protons are generated. The energy dependent translocation of these protons to the stromal side occurs as the electrons flow down the redox gradient indicated in the Z scheme. Ultimately, the protons are either consumed in the production of NADPH on the stromal side or their energy (in the form of a proton gradient) is used to produce ATP.38 The membrane is also the site in which the antenna complex, consisting of hundreds of chlorophylls are organized such that light excitation of any chlorophyll quickly results in energy transfer to the special pair in PS I or PS II for charge-separation.32
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