William W. Parson

Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement

Comparing photosynthetic and photovoltaic efficiencies is not a simple issue. Although both processes harvest the energy in sunlight, they operate in distinctly different ways and produce different types of products: biomass or chemical fuels in the case of natural photosynthesis and nonstored electrical current in the case of photovoltaics. In order to find common ground for evaluating energy-conversion efficiency, we compare natural photosynthesis with present technologies for photovoltaic-driven electrolysis of water to produce hydrogen. Photovoltaic-driven electrolysis is the more efficient process when measured on an annual basis, yet short-term yields for photosynthetic conversion under optimal conditions come within a factor of 2 or 3 of the photovoltaic benchmark. We consider opportunities in which the frontiers of synthetic biology might be used to enhance natural photosynthesis for improved solar energy conversion efficiency.

Light-harvesting antennas in photosynthesis

Editorial. Preface. Color Plates. I: Introduction to Light-Harvesting. 1. Photosynthetic Membranes and Their Light-Harvesting Antennas B.R. Green, J.M. Anderson, W.W. Parson. 2. The Pigments H. Scheer. 3. Optical Spectroscopy in Photosynthetic Antennas W.W. Parson, V. Nagarajan. 4. The Evolution of Light-Harvesting Antennas B.R. Green. II: Structure and Function in Light-Harvesting. 5. The Light-Harvesting System of Purple Bacteria B. Robert, R.J. Cogdell, R. van Grondelle. 6. Antenna Complexes from Green Photosynthetic Bacteria R.E. Blankenship, K. Matsuura. 7. Light-Harvesting in Photosystem II H. van Amerongen, J.P. Dekker. 8. Structure and Function of the Antenna System in Photsystem I P. Fromme, E. Schlodder, S. Jansson. 9. Antenna Systems and Energy Transfer in Cyanophyta and Rhodophyta M. Mimuro, H. Kikuchi. 10. Antenna Systems of Red Algae: Phycobilisomes with Photosystem II and Chlorophyll Complexes with Photosystem I E. Gantt, B. Grabowski, F.X. Cunningham Jr. 11. Light-Harvesting Systems in Chlorophyll c-Containing Algae A.N. Macpherson, R.G. Hiller. III: Biogenesis, Regulation and Adaptation. 12. Biogenesis of Green Plant Thylakoid Membranes K. Cline. 13. Pulse Amplitude Modulated Chlorophyll Fluorometry and its Application in Plant Science G.H. Krause, P. Jahns. 14. Photostasis in Plants, Green Algae and Cyanobacteria: The Role of Light-Harvesting Antenna Complexes N.P.A. Huner, G. Oquist, A. Melis. 15. Photoacclimation of Light-Harvesting Systems in EukaryoticAlgae P.G. Falkowski, Yi-Bu Chen. 16. Multi-level Regulation of Purple Bacterial Light-Harvesting Complexes C.S. Young, J.T. Beatty. 17. Environmental Regulation of Phycobilisome Biosynthesis A.R. Grossman, L.G. van Waasbergen, D. Kehoe. Index.

Pigment content and molar extinction coefficients of photochemical reaction centers from Rhodopseudomonas spheroides

Reaction center particles isolated from carotenoidless mutant Rhodopseudomonas spheroides were studied with the aim of determining the pigment composition and the molar extinction coefficients. Two independent sets of measurements using a variety of methods show that a sample with A800 nm = 1.00 contains 20.8 ± 0.8 μM tetrapyrrole and that the ratio of bacteriochlorophyll to bacteriopheophytin is 2:1. Measurements were made of the absorption changes attending the oxidation of cytochrome c coupled to reduction of the photooxidized primary electron donor in reaction centers, using laser flash excitation. The ratio of the absorption change at 865 nm (due to the bleaching of P870) to that at 550 nm (oxidation of cytochrome) was found to be 5.77. These results, combined with other data, yield a pigment composition of 4 bacteriochlorophyll and 2 bacteriopheophytin molecules in a reaction center. Based on this choice, extinction coefficients are determined for the 802- and 865-nm bands: e802 nm = 288 (± 14) mM−1 · cm−1 and e865 nm = 128 (± 6) mM−1 · cm−1. For reversible bleaching of the 865-nm band, Δered - ox865nm = 112 (± 6) mM−1 · cm−1 (referred to the molarity of reaction centers). Earlier reported values of photochemical quantum efficiency are recomputed, and the revised values are shown to be compatible with those obtained from measurements of fluorescence transients.

Excited states of photosynthetic reaction centers at low redox potentials

In preparations of photochemical reaction centers from Rhodopseudomonas spheroides R-26, lowering the recox potential so as to reduce the primary electron acceptor prevents the photochemical transfer of an electron from bacteriochlorophyll to the acceptor. Measuring absorbance changes under these conditions, we found that a 20-ns actinic flash converts the reaction center to a new state, P-F, which then decays with a half-time that is between 1 and 10 ns at 295 degrees K. At 25 degrees K, the decay half-time is approx. 20 ns. The quantum yield of state P-F appears to be near 1.0, both at 295 and at 15 degrees K. State P-F could be an intermediate in the photochemical electron-transfer reaction which occurs when the acceptor is in the oxidized form. Following the decay of state P-F, we detected another state, P-R, with a decay half-time of 6 mus at 295 degrees K and 120 mus at 15 degrees K. The quantum yield of state P-R is approx. 0.1 at 295 degrees K, but rises to a value nearer 1.0 at 15 degrees K. The kinetics and quantum yields are consistent with the view that state P-R forms from P-F. State P-R seems likely to be a side-product, rather than an intermediate in the electron-transfer process. The decay kinetics indicate that state P-F cannot be identical with the lowest excited singlet state of the reaction center. One of the two states, P-F or P-R, probably is the lowest excited triplet state of the reaction center, but it remains unclear which one.

Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides

The time-course of fluorescence from reaction centers isolated from Rhodopseudomonas sphaeroides was measured using single-photon counting techniques. When electron transfer is blocked by the reduction of the electron-accepting quinones, reaction centers exhibit a relatively long-lived (delayed) fluorescence due to back reactions that regenerate the excited state (P*) from the transient radical-pair state, PF. The delayed fluorescence can be resolved into three components, with lifetimes of 0.7, 3.2 and 11 ns at 295 K. The slowest component decays with the same time-constant as the absorbance changes due to PF, and it depends on both temperature and magnetic fields in the same way that the absorbance changes do. The time-constants for the two faster components of delayed fluorescence are essentially independent of temperature and magnetic fields. The fluorescence also includes a very fast (prompt) component that is similar in amplitude to that obtained from unreduced reaction centers. The prompt fluorescence presumably is emitted mainly during the period before the initial charge-transfer reaction creates PF from P*. From the amplitudes of the prompt and delayed fluorescence, we calculate an initial standard free-energy difference between P* and PF of about 0.16 eV at 295 K, and 0.05 eV at 80 K, depending somewhat on the properties of the solvent. The multiphasic decay of the delayed fluorescence is interpreted in terms of relaxations in the free energy of PF with time, totalling about 0.05 eV at 295 K, possibly resulting from nuclear movements in the electron-carriers or the protein.

Temperature and detection-wavelength dependence of the picosecond electron-transfer kinetics measured in Rhodopseudomonas sphaeroides reaction centers. Resolution of new spectral and kinetic components in the primary charge-separation process

Abstract We have examined the temperature dependence of the rate of electron transfer to ubiquinone from the bacteriopheophytin (BPh) that serves as an initial electron acceptor (I) in reaction centers of Rhodopseudomonas sphaeroides . The kinetics were measured from the decay of the 665-nm absorption band of the reduced BPh (BPh − or I − ) and from the recovery of the BPh band at 545 nm, following excitation of reaction centers in polyvinyl alcohol films with 30-ps flashes. The measured time constant decreases from 229 ± 25 ps at 295 K to 97 ± 8 ps near 100 K and then remains constant down to 5 K. The temperature dependence of the kinetics can be rationalized on the assumption that the reaction results in changes in the frequencies of numerous low-energy nuclear (vibrational) modes of the electron carriers and/or the protein. The kinetics measured in the absorption bands near 765 and 795 nm show essentially the same temperature dependence as those measured at 545 or 665 nm, but the time constants vary with detection wavelength. The time constant measured in the 795-nm region (70 ± 10 ps at 5 and 76 K) is shorter than that seen in the absorption bands of the BPh; the time constant measured at 758 nm is longer. Time constants measured with reaction centers in solution at 288 K also vary with the detection wavelength. These results can be explained on the assumption that the absorption changes measured at some wavelengths reflect nuclear relaxations rather than electron transfer. The absorption changes at 795 nm probably reflect a relaxation of the bacteriochlorophyll molecules that are near neighbors of the BPh and the primary electron donor (P). Those near 530 and 755 nm probably are due to the second BPh molecule, which does not appear to undergo oxidation or reduction.

Singlet-triplet fusion in Rhodopseudomonas sphaeroides chromatophores. A probe of the organization of the photosynthetic apparatus.

Chromatophores from various strains of Rhodopseudomonas sphaeroides were excited with laser flashes lasting about 20 ns. Fluorescence from the antenna bacteriochlorophyll of the photosynthetic apparatus was measured both during the laser flash, and during a weak Xe flash following the laser flash. Strong laser flashes caused severe quenching of the fluorescence, which could be correlated with the formation of triplet states of the antenna pigments. Triplet states of both BChl and carotenoids acted as quenchers, but bacteriochlorophyll triplets were the more effective of the two. In the double-flash experiments, the reciprocal of the fluorescence yield was proportional to the concentration of triplet quenchers remaining at the time of the second flash. This relationship indicates that singlet excitations can migrate over large domains in the antenna, rather than being restricted by boundaries separating individual reaction centers. Comparisons of chromatophores from different strains and from cells grown under different conditions showed that excitations are concentrated rapidly in the antenna complexes with the longest wavelength absorption bands (B870), and that the migration of excitations to trapping sites is relatively insensitive to the amount of antenna bacteriochlorophyll absorbing at shorter wavelengths (B800–B850). This suggests that the B870 complexes are organized in the membrane so as to interconnect many reaction centers, and that the B800–B850 complexes are arranged peripherally.

Dynamics of biochemical and biophysical reactions: insight from computer simulations.

1. Introduction 5632. Obtaining rate constants from molecular-dynamics simulations 5642.1 General relationships between quantum electronic structures and reaction rates 5642.2 The transition-state theory (TST) 5692.3 The transmission coefficient 5723. Simulating biological electron-transfer reactions 5753.1 Semi-classical surface-hopping and the Marcus equation 5753.2 Treating quantum mechanical nuclear tunneling by the dispersed-polaron/spin-boson method 5803.3 Density-matrix treatments 5833.4 Charge separation in photosynthetic bacterial reaction centers 5844. Light-induced photoisomerizations in rhodopsin and bacteriorhodopsin 5965. Energetics and dynamics of enzyme reactions 6145.1 The empirical-valence-bond treatment and free-energy perturbation methods 6145.2 Activation energies are decreased in enzymes relative to solution, often by electrostatic effects that stabilize the transition state 6205.3 Entropic effects in enzyme catalysis 6275.4 What is meant by dynamical contributions to catalysis? 6345.5 Transmission coefficients are similar for corresponding reactions in enzymes and water 6365.6 Non-equilibrium solvation effects contribute to catalysis mainly through Δg[Dagger], not the transmission coefficient 6415.7 Vibrationally assisted nuclear tunneling in enzyme catalysis 6485.8 Diffusive processes in enzyme reactions and transmembrane channels 6516. Concluding remarks 6587. Acknowledgements 6588. References 658Obtaining a detailed understanding of the dynamics of a biochemical reaction is a formidable challenge. Indeed, it might appear at first sight that reactions in proteins are too complex to analyze microscopically. At room temperature, even a relatively small protein can have as many as 1034 accessible conformational states (Dill, 1985). In many cases, however, we have detailed structural information about the active site of an enzyme, whereas such information is missing for corresponding chemical systems in solution. The atomic coordinates of the chromophore in bacteriorhodopsin, for example, are known to a resolution of 1–2 A. In addition, experimental studies of biological processes such as photoisomerization and electron transfer have provided a wealth of detailed information that eventually may make some of these processes classical problems in chemical physics as well as biology.

Primary photochemical processes in isolated reaction centers of Rhodopseudomonas viridis

Picosecond and nanosecond spectroscopic techniques have been used to study the primary electron transfer processes in reaction centers isolated from the photosynthetic bacterium Rhodopseudomonas viridis. Following flash excitation, the first excited singlet state (P*) of the bacteriochlorophyll complex (P) transfers an electron to an intermediate acceptor (I) in less than 20 ps. The radical pair state P+I-) subsequently transfers an electron to another acceptor (X) in about 230 ps. There is an additional step of unknown significance exhibiting 35 ps kinetics. P+ subsequently extracts an electron from a cytochrome, with a time constant of about 270 ns. At low redox potential (X reduced before the flash), the state P+I- (or PF) lives approx. 15 ns. It decays, in part, into a longer lived state (PR), which appears to be a triplet state. State PR decays with an exponential time of approx. 55 microseconds. After continuous illumination at low redox potential (I and X both reduced), excitation with an 8-ps flash produces absorption changes reflecting the formation of the first excited singlet state, P*. Most of P* then decays with a time constant of 20 ps. The spectra of the absorbance changes associated with the conversion of P to P* or P+ support the view that P involves two or more interacting bacteriochlorophylls. The absorbance changes associated with the reduction of I to I- suggest that I is a bacteriopheophytin interacting strongly with one or more bacteriochlorophylls in the reaction center.

Radical-pair decay kinetics, triplet yields and delayed fluorescence from bacterial reaction centers

Abstract Purified reaction centers from Rhodopseudomonas sphaeroides and Rhodospirillum rubrum were excited with short flashes of light, under conditions that blocked electron transfer to the first quinone (Q). The radical-pair state (P F ) generated by the excitation decays by several different back-reactions. One back-reaction repopulates an excited singlet state (P∗) and results in delayed fluorescence; another produces a triplet state (P R ). We measured the decay kinetics of P F , the quantum yield of P R , and the intensity and decay kinetics of the delayed fluorescence under a variety of conditions, including cryogenic temperatures, magnetic fields, depletion of Q and Fe, and isotopic replacement of 1 H by 2 H. The delayed fluorescence decays about twice as rapidly as P F , and has an unusual temperature dependence. It increases in amplitude with decreasing temperature from 260 to 215 K, and then decreases. From the amplitude of the delayed fluorescence, we estimate the standard free energy and enthalpy differences between P F and P∗, and an effective rate constant for the repopulation of P∗, as functions of temperature. Regeneration of P∗ accounts for only a small fraction of the decay of P F . Contrary to expectation, the quantum yield of P R is not decreased by deuteration of the reaction centers, or by depletion of Q or Fe. The known decay paths of P F cannot fully account for the dependence of the P R yield and the decay kinetics of P F on temperature and magnetic fields, nor for the decay kinetics and temperature dependence of the delayed fluorescence. Possible solutions to some of these problems are suggested.