Energy transfer in photosynthesis

The results of recent spectroscopic measurements on chlorophyll a in bilayers and lipid vesicles stimulated a re-examination of energy transfer in photosynthesis. The Förster resonance transfer mechanism is believed to be applicable under reasonable assumptions despite recent criticism. The Förster parameter was newly determined to be R₀ = 65 Å; previous uncertainty due to unknown transition moment orientation can be avoided by assuming the black film dichroic result to be applicable in vivo. The effect due to the still incompletely known thylakoid structure and chlorophyll aggregation is discussed qualitatively. Agreement with experimental fluorescence lifetimes and quantum efficiencies may be obtained with a reasonable choice of parameters.     

Energy transfer in bacterial photosynthesis

Four possible explanations are offered to account for low fluorescence increase observed for purple bacteria under transition from active to inhibited photosynthesis. The increase observed is inconsistent with high (1.0) yield of primary photosynthetic process of P₈₉₀ photooxidation. The dependences of fluorescence yield and lifetime on the portion of active reaction centres have been analysed for each case. Experimental investigation carried out favours the existence of background fluorescence together with fluorescence, whose quantum yield correlates with the reaction centre functional state. The important conclusion is made that lifetime of photosynthetic fluorescence is much lower than 1 nsec and energy is transferred to the reaction centres by a mechanism other than inductive-resonance.     

Energy transfer to the reaction centres in bacterial photosynthesis

From a combined study of (1) bacteriochlorophyll fluorescence lifetimes, (2) relative yields and (3) differential absorption changes corresponding to the reaction centres photooxidation, the absolute values of fluorescence lifetimes and quantum yields for two bacteriochlorophyll fractions have been calculated. The main bacteriochlorophyll fraction (80–90%) serving as a light-gathering antenna for reaction centresP ₈₉₀ is characterized by dark values of fluorescence lifetimes of the order of 10^–11 sec and fluorescence yields of 10^–3. The remaining part of the bulk pigment, not associated withP ₈₉₀ as far as excitation energy transfer is concerned, has an approximately constant fluorescence yield of about 5–8% and lifetime of about 10^–9 sec. Basing on these results, excitation jump times and intermolecular coupling energies were estimated to be 10^–13 sec and 10^–2 ev respectively. The conclusion is made that excitation energy transfer in the main part of bacteriochlorophyll occurs by the exciton mechanism at moderate intermolecular energies.     

Structure-based modeling of energy transfer in photosynthesis

We provide a minimal model for a structure-based simulation of excitation energy transfer in pigment–protein complexes (PPCs). In our treatment, the PPC is assembled from its building blocks. The latter are defined such that electron exchange occurs only within, but not between these units. The variational principle is applied to investigate how the Coulomb interaction between building blocks changes the character of the electronic states of the PPC. In this way, the standard exciton Hamiltonian is obtained from first principles and a hierarchy of calculation schemes for the parameters of this Hamiltonian arises. Possible extensions of this approach are discussed concerning (i) the inclusion of dispersive site energy shifts and (ii) the inclusion of electron exchange between pigments. First results on electron exchange within the special pair of photosystem II of cyanobacteria and higher plants are presented and compared with earlier results on purple bacteria. In the last part of this mini-review, the coupling of electronic and nuclear degrees of freedom is considered. First, the standard exciton–vibrational Hamiltonian is parameterized with the help of a normal mode analysis of the PPC. Second, dynamical theories are discussed that exploit this Hamiltonian in the study of dissipative exciton motion.     

Carboxylate shifts steer interquinone electron transfer in photosynthesis

Understanding the mechanisms of electron transfer (ET) in photosynthetic reaction centers (RCs) may inspire novel catalysts for sunlight-driven fuel production. The electron exit pathway of type II RCs comprises two quinone molecules working in series and in between a non-heme iron atom with a carboxyl ligand (bicarbonate in photosystem II (PSII), glutamate in bacterial RCs). For decades, the functional role of the iron has remained enigmatic. We tracked the iron site using microsecond-resolution x-ray absorption spectroscopy after laser-flash excitation of PSII. After formation of the reduced primary quinone, Q_A⁻, the x-ray spectral changes revealed a transition (t_½ ≈ 150 μs) from a bidentate to a monodentate coordination of the bicarbonate at the Fe(II) (carboxylate shift), which reverted concomitantly with the slower ET to the secondary quinone Q_B. A redox change of the iron during the ET was excluded. Density-functional theory calculations corroborated the carboxylate shift both in PSII and bacterial RCs and disclosed underlying changes in electronic configuration. We propose that the iron-carboxyl complex facilitates the first interquinone ET by optimizing charge distribution and hydrogen bonding within the Q_AFeQ_B triad for high yield Q_B reduction. Formation of a specific priming intermediate by nuclear rearrangements, setting the stage for subsequent ET, may be a common motif in reactions of biological redox cofactors.     

Energy migration and exciton trapping in green plant photosynthesis

The possible origins of the different fluorescence decay components in green plants are discussed in terms of a random walk and Butler's bipartite model. The interaction of the excitations with the photosystem II reaction centers and, specifically, the regeneration of theses excitations by charge recombination within the reaction centers, are considered. Based on comparisons between fluorescence decay profiles, time-dependent exciton annihilation and photoelectric phenomena, it appears that the fast 200 ps decay component corresponds to primary energy transport from the antenna to the reaction centers and is dominant in filling the photosystem II reaction centers.     

Energy transfer in monomeric phycoerythrocyanin

We describe the involvement of poly(ADP-ribose)polymerase 1 and 2 (PARP-1 and -2) and poly(ADP-ribose)glycohydrolase (PARG) in the response of rat germinal cells to the action of the NO donors, 3-morpholino-sydnonimine (SIN-1) and spermine nonoate (SNO). Primary spermatocytes and round spermatids showed a differential sensitivity to DNA damage induced by acute exposure to SIN-1 and SNO. Spermatocytes were able to repair DNA damage caused by the release of NO from SNO but neither spermatocytes nor spermatids could recover from the release of NO and O2*- from SIN-1. Addition of the PARPs inhibitor, 3-aminobenzamide, and the PARG inhibitor, gallotannin (GT), to germ cell cultures impaired DNA repair significantly. Consistent with the DNA repair seen in primary spermatocytes, both SIN-1 and SNO induced PARPs activation in these cells. In the case of SIN-1, there was an immediate but transient response while SNO induced a delayed but more sustained increase in PARPs activity. Chronic exposure of spermatocytes to SIN-1 and SNO, however, committed the cells to apoptosis, which coincided with proteolysis of PARP-1. The data indicate a dual role for PARPs and PARG in germinal cells as key proteins in processes that sense and repair DNA damage as well as in the commitment to apoptosis following prolonged oxidative stress.     

Energy storage of linear and cyclic electron flows in photosynthesis

The energy storage of photosynthesis in the green alga Chlorella vulgaris was determined by pulsed, time-resolved photoacoustics. The energy storage of the linear electron transfer process in photosynthesis, of cyclic photosystem (PS) I, and possibly of PSII was determined by selection of excitation wavelength and of flash interval. At 695 nm excitation, a rather large cyclic PSI energy storage of 0.68 ± 0.04 eV/quantum of energy at 8 ms after a 1-μs flash was obtained. This energy remained the same at flash intervals of 0.35 to 60 s and was independent of the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. We tentatively assign this energy to the ferredoxin-NADP-reductase-ferredoxin and oxidized cytochrome b₆/f complexes. An efficient distribution of energy between cyclic and linear systems is obtained with the simple assumption that the turnover time of the cyclic system is slower than that of the linear system. The energy storage of linear electron flow was determined by 655 nm excitation of Chlorella with a short flash interval of 0.35 s per flash. It was calculated to be 0.50 ± 0.03 eV/hv, close to that expected for oxygen and NADPH formation. The energy storage of PSII is determined by excitation of Chlorella at 655 nm with a long flash interval of 60 s per flash. It was calculated to be 1.07 ± 0.05 eV/hv, consistent with the energy storage being in S-states and the secondary electron acceptor of PSII with a calculated redox energy of 1.03 eV/hv. In the presence of 1 μm 3-(3,4-dichlorophenyl)-1,1-dimethylurea, the calculated energy storage in PSII is still significant, 0.53 ± 0.04 eV/hv. This probably indicates a significant cyclic electron flow around PSII. These cyclic flows may contribute considerably to energy storage in photosynthesis.     

Coupling of light-induced electron transfer to proton uptake in photosynthesis

Light energy is transformed into chemical energy in photosynthesis by coupling a light-induced electron transfer to proton uptake. The resulting proton gradient drives ATP synthesis. In this study, we monitored the light-induced reactions in a 100-kDa photosynthetic protein from 30 ns to 35 s by FTIR difference spectroscopy. The results provide detailed mechanistic insights into the electron and proton transfer reactions of the QA to QB transition: reduction of QA in picoseconds induces protonation of histidines, probably of His126 and His128 in the H subunit at the entrance of the proton uptake channel, and of Asp210 in the L subunit inside the channel at 12 micros and 150 micros. This seems to be a prerequisite for the reduction of QB, mainly at 150 micros. QA- is reoxidized at 1.1 ms, and a proton is transferred from Asp210 to Glu212 in the L subunit, the proton donor to QB-. Notably, our data indicate that QB is not reduced directly by QA- but presumably through an intermediary electron donor.