Pair In Photosynthetic Reaction Center Research Articles

Analysis of the Kinetics of P+HA– Recombination in Membrane-Embedded Wild-Type and Mutant Rhodobacter sphaeroides Reaction Centers between 298 and 77 K Indicates That the Adjacent Negatively Charged QA Ubiquinone Modulates the Free Energy of P+HA– and May Influence the Rate of the Protein Dielectric Response

Time-resolved spectroscopic studies of recombination of the P(+)HA(-) radical pair in photosynthetic reaction centers (RCs) from Rhodobacter sphaeroides give an opportunity to study protein dynamics triggered by light and occurring over the lifetime of P(+)HA(-). The state P(+)HA(-) is formed after the ultrafast light-induced electron transfer from the primary donor pair of bacteriochlorophylls (P) to the acceptor bacteriopheophytin (HA). In order to increase the lifetime of this state, and thus increase the temporal window for the examination of protein dynamics, it is possible to block forward electron transfer from HA(-) to the secondary electron acceptor QA. In this contribution, the dynamics of P(+)HA(-) recombination were compared at a range of temperatures from 77 K to room temperature, electron transfer from HA(-) to QA being blocked either by prereduction of QA or by genetic removal of QA. The observed P(+)HA(-) charge recombination was significantly slower in the QA-deficient RCs, and in both types of complexes, lowering the temperature from RT to 77 K led to a slowing of charge recombination. The effects are explained in the frame of a model in which charge recombination occurs via competing pathways, one of which is thermally activated and includes transient formation of a higher-energy state, P(+)BA(-). An internal electrostatic field supplied by the negative charge on QA increases the free energy levels of the state P(+)HA(-), thus decreasing its energetic distance to the state P(+)BA(-). In addition, the dielectric response of the protein environment to the appearance of the state P(+)HA(-) is accelerated from ∼50-100 ns in the QA-deficient mutant RCs to ∼1-16 ns in WT RCs with a negatively charged QA(-). In both cases, the temperature dependence of the protein dynamics is weak.

Continuum electrostatic investigations of charge transfer processes in biological molecules using a microstate description

Charge transfer through biological macromolecules is essential for many biological processes such as for instance photosynthesis and respiration. In these processes, protons or electrons are transferred between titratable residues or redox-active cofactors, respectively. Often their transfer is tightly coupled. Computational methods based on continuum electrostatics are widely used in theoretical biochemistry to analyze the function of even very complex biochemical systems. These methods allow one to consider the pH and the redox potential of the solution as well as explicitly considering membrane potentials in the calculations. Combining continuum electrostatic calculations with a statistical thermodynamic analysis, it is possible to calculate equilibrium parameters such as protonation or oxidation probabilities. Moreover, it is also possible to simulate reaction kinetics by using parameters calculated from continuum electrostatics. One needs to consider that the transfer rate between two sites depends on the current charge configuration of neighboring sites. We formulate the kinetics of charge transfer systems in a microstate formalism. A unique transfer rate constant can be assigned to the interconversion of microstates. Mutual interactions between sites participating in the transfer reactions are naturally taken into account. This formalism is applied to the kinetics of electron transfer in the tetraheme-subunit and the special pair of the reaction center of Blastochloris viridis. It is shown that continuum electrostatic calculations can be used in combination with an existing rate law to obtain electron transfer rate constants. The relaxation electron transfer kinetics after photo-oxidation of the special pair of photosynthetic reaction center is simulated by a microstate formalism and it is shown to be in good agreement with experimental data. A flux analysis is used to follow the individual electron transfer steps. This method of simulating the complex kinetics of biomolecules based on structural data is a first step on the way from structural biology to systems biology.

Covalently linked zinc chlorophyll dimers as a model of a chlorophyllous pair in photosynthetic reaction centers

A heterodimer, where zinc pyropheophorbide-a was linked with zinc pyropheophorbide-d through ethylene glycol diester, was prepared, as well as the corresponding homodimers. The synthetic dimers were complexed with methanol in benzene to give folded dimers by mutual Zn...O(Me)-H...O=C13(1) bonding. Such complexes had furthest red (Qy) absorption bands at longer wavelengths than the monomeric species. These red-shifts were ascribable to excitonic coupling of the Qy transition states in the chlorin pi-pi stacking conformer. In the heterodimeric system, a minor band was observed at the shorter wavelength side of the main Qy band. This observation can be explained by an additional contribution of Qy vibronic state to the exciton-coupled states. Based on the experimental results, a pair of chlorophyll(Chl)-d with Chl-a as well as a Chl-d homopair were proposed as dimers in reaction centers of Chl-d dominating cyanobacteria.

A phenomenological model of dynamical arrest of electron transfer in solvents in the glass-transition region

A phenomenological model of electron transfer reactions in solvents undergoing glass transition is discussed. The reaction constant cuts off slow polarization modes from the spectrum of nuclear thermal motions active on the observation time scale. The arrest of nuclear solvation in turn affects the reaction activation barrier making it dependent on the rate. The resultant rate constant is sought from a self-consistent equation. The model describes well the sharp change in the solvent Stokes shift of optical lines in the glass-transition region. It is also applied to describe the temperature dependence of primary charge separation and reduction of primary pair in photosynthetic reaction centers. The model shows that a weak dependence of the primary charge separation rate on temperature can be explained by dynamical arrest of nuclear solvation on the picosecond time scale of electron transfer. For reduction of primary pair by cytochrome, the model yields a sharp turnover of the reaction kinetics at the transition temperature when nuclear solvation freezes in.

Wittig reactions on photoprotoporphyrin IX: new synthetic models for the special pair of the photosynthetic reaction center.

A first example of spirochlorin-chlorin dimer with fixed distances and orientations as potential model for the "special pair" of the photosynthetic reaction center is discussed. For the preparation of such a novel structure, the Wittig reagent of the desired "spacer" 5 was reacted with photoprotoporphyrin IX dimethyl ester 3 to produce the intermediate dimer 6, which on intramolecular [4 + 2] Diels-Alder cycloaddition gave an unexpected spirochlorin-chlorin dimer 9. Dehydration of dimer 6 under acid-catalyzed conditions generated the corresponding spirochlorin-porphyrin dimer 16 in quantitative yield. The asymmetry in dimer 6 caused by the biphenyl-type anisotropic effect was confirmed by NMR and model studies. The formation of dihydrobenzoporphyrin 14 by reacting chlorin 3 with the phosphonium salt of p-methylbenzylbromide 10 and isolation of 8-phenanthrenevinylporphyrin 19 from chlorin 7 further confirmed our proposed mechanism for the formation of a spirochlorin-chlorin dimer 9. Following a similar approach, chlorin 3 on reacting with bis-phosphonium salt of 4, 4'-bischloromethylbiphenyl produced conjugated chlorin dimer 25. The spectroscopic data obtained from these dimers suggest that, in these compounds, the individual chromophores are not behaving as an individual molecule, but as a single macrocycle. To examine whether the pi-pi interaction exhibited by dimer 9 resembles the structural arrangement of bacteriochlorophylls in reaction center (RC), we investigated the geometrical parameters used to characterize the pi-pi interactions in tetrapyrrolic macrocycles. Starting from the crystallographic coordinates of 9, the molecular mechanics energy minimization was performed to obtain the model dimer structure. The geometrical parameters that measure the single pyrrole ring overlap were used to compare the model structure with the crystallographic coordinates of the special pair in photosynthetic reaction center. The results indicated that the ring A of spirochlorin and the ring C of chlorin in our model dimer 9 mimic the ring A-ring A interaction found in the crystallographic special pairs, which are strategically placed by the surrounding photosynthetic reaction center protein matrix.

Excited State Energy Transfer Pathways in Photosynthetic Reaction Centers. 2. Heterodimer Special Pair

Ultrafast singlet excited state energy transfer occurs from the monomeric chromophores to the primary electron donor or special pair in photosynthetic reaction centers. The mechanism of this proces...

Excited State Energy Transfer Pathways in Photosynthetic Reaction Centers. 1. Structural Symmetry Effects

Ultrafast excited state energy transfer to the primary electron donor or special pair in photosynthetic reaction centers has been measured following excitation of the lowest electronic state of the other chromophores. This was achieved by observing the rise time and induced anisotropy in the spontaneous fluorescence from the special pair using fluorescence up-conversion at 85 K. Very fast energy transfer is observed when exciting either of the bacteriochlorophyll monomers. Energy transfer from the bacteriopheophytins, which are considerably further from the special pair than the bacteriochlorophyll monomers, is about 50% slower. The rate, distance, and temperature dependence of energy transfer in both cases are very different from what is predicted by conventional Förster dipole−dipole theory. By working at low temperature and with the reaction center mutant (M)L214H (the beta mutant), which assembles with a bacteriochlorophyll monomer in place of a bacteriopheophytin in the HL binding site (the location of the primary electron acceptor), it is possible to selectively initiate the energy transfer process on the functional and nonfunctional sides of the reaction center. The observed rates of energy transfer to the special pair are found to be similar. Thus energy transfer rates are comparable on the functional and nonfunctional sides, while electron transfer rates differ by at least 2 orders of magnitude. This suggests that the dominant source of functional asymmetry for electron transfer involves differences in the association of the functional-side chromophores with their environment (e.g. free and reorganization energy differences), rather than differences in electronic coupling.

Observation of Ultrafast Energy Transfer from the Accessory Bacteriochlorophylls to the Special Pair in Photosynthetic Reaction Centers

The energy transfer from accessory bacteriochlorophyll molecules (B) to the special pair (P) in the reaction center of Rb. capsulatus and Rb. sphaeroides R26 has been time-resolved using 23 fs pulses. In both reaction centers, the B* transient bleaching decays biexponentially, with a fast component of approximately 100 fs which gives a characteristic time scale for excitation energy transfer from B* to P. In Rb. capsulatus, the amplitudes for this component and a 360 {+-} 40 fs decay of uncertain origin reported in previous experiments are approximately equal. Several models for the two components are discussed. 33 refs., 2 figs.

Hole localization and spin coupling in .pi.-mono- and .pi.-dications of .mu.-oxoporphyrin dimers. Relevance to structure of oxidized special pair in photosynthetic reaction centers

The antiferromagnetically coupled cofacial [mu]-oxoiron(III) dimers of octaethylporphyrin (OEP) and [alpha],[beta],[gamma],[Delta]-tetraphenylporphyrin (TPP) can be oxidized in two one-electron steps to yield [pi]-monocations and [pi]-dications. Hitherto unreported absorption bands are observed in the mid-infrared region in the spectra of the monocations. These are identified as intervalence transitions of dynamically trapped holes. The electron-phonon coupling energies (CH[sub 2]Cl[sub 2] solution, 295 K) are 0.31 [+-] 0.04 eV, and the inter-ring, predominantly through-space, electronic coupling constants J are 0.07 and 0.03 eV, respectively. The small values of J are a consequence of the large mean plane separation of the porphyrin rings (4.53 A). Since it is impossible that the electron-phonon coupling energies will vary greatly between cofacial porphyrin dimers, it is suggested that absorption hands around 1 eV in the [pi]-monocations of [open quotes]sandwich[close quotes] compounds such as M[sup III]P[sub 2] or M[sup IV]P[sub 2][sup +], where P is a porphyrin and M are lanthanide, actinide, or transition metals (3-12) observed under similar conditions will have electronic ground states that are delocalized on at least the vibrational time scale, with frequency maxima equal to 2J in the tight-binding approximation. The thermal inter-ring hole-transfer times in the [mu]-oxo dimer monocations are estimated to bemore » approximately 1 ps. The relevance of these results to the problem of the structure of the oxidized [open quotes]special pair[close quotes] in the photosynthetic reaction center is briefly discussed. 52 refs., 4 figs., 5 tabs.« less

Picosecond laser photolysis studies on dimer model systems in relation to photosynthetic charge separation processes

In relation to the photoinduced charge separation in the special pair of photosynthetic reaction center, solvation induced intramolecular electron transfer in the excited state of composite system with identical halves have been investigated with picosecond spectroscopy in the case of 1,2-dienthrylethanes. The energy gap dependences of charge separation and charge recombination in these systems are demonstrated and compared with those of hybrid dimer model of metal porphyrins, porphyrin-quinone systems and various aromatic donor-acceptor systems. The significance of these results in the understanding of efficient charge separation in biological reaction center is discussed.

Solvent Polarity Dependent Photophysics of a Fixed‐Distance, Symmetric Chlorophyll Dimer. A Model of the Special Pair in Photosynthetic Reaction Centers

AbstractThe synthesis and properties of a fixed‐distance symmetric bis‐pyrochlorophyllide‐a molecule are described. The molecule, 1, consists of two methyl pyrochlorophyllide‐a (MePChlide‐a) moieties which share a common vinyl group at the 2‐position of each macrocycle. The two chlorophylls are trans to one another across the vinyl linkage. The dihedral angle between the plane of each macrocycle and the vinyl linkage is about 50°. The Qy absorption band of this dimer occurs at 689 nm and is essentially independent of solvent. The band is red‐shifted by about 27 run relative to that of MePChlide‐a. The fluorescence maximum of 1 occurs at 722 nm. This is a red‐shift of 49 nm relative to methyl MePChlide‐a. The circular dichroism spectrum of 1 shows strong, nonconservative bands in the red region. The fluorescence quantum yield, fluorescence lifetimes, and picosecond transient absorbance kinetics all exhibit a very strong dependence on solvent polarity. The fluorescence quantum yields of 1 in toluene, butyronitrile, and N, N‐dimethyl formamide (DMF) are 0.18, 0.008, and 0.002, respectively. The bleach of the 689 nm band (following excitation with a 1.5‐ps, 610‐nm laser pulse) recovers with single exponential time constants of 2.51 ns, 100 ps, and 64 ps in toluene, butyronitrile, and DMF, respectively. Possible mechanisms for the polarity‐dependent increase of the nonradiative decay rate of 1 are considered.

ChemInform Abstract: A Twisted and Partially Overlapping Porphyrin Dimer as a New Model of Special Pair in Photosynthetic Reaction Center.

ChemInformVolume 18, Issue 50 Organic Dyes ChemInform Abstract: A Twisted and Partially Overlapping Porphyrin Dimer as a New Model of Special Pair in Photosynthetic Reaction Center. A. OSUKA, A. OSUKA Chem. Lab., Agric. Univ. Athens, 118 55 Athens, GreeceSearch for more papers by this authorK. MARUYAMA, K. MARUYAMA Chem. Lab., Agric. Univ. Athens, 118 55 Athens, GreeceSearch for more papers by this author A. OSUKA, A. OSUKA Chem. Lab., Agric. Univ. Athens, 118 55 Athens, GreeceSearch for more papers by this authorK. MARUYAMA, K. MARUYAMA Chem. Lab., Agric. Univ. Athens, 118 55 Athens, GreeceSearch for more papers by this author First published: December 15, 1987 https://doi.org/10.1002/chin.198750314AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat No abstract is available for this article. Volume18, Issue50December 15, 1987 RelatedInformation

A Twisted and Partially Overlapping Porphyrin Dimer as a New Model of Special Pair in Photosynthetic Reaction Center

Abstract A twisted and partially overlapping porphyrin dimer bridged by a 1,1′-spirobiindane spacer was synthesized. Its biszinc complex and bismagnesium complex showed a split Soret band, indicating the exciton interaction of the two porphyrin ring. Bismagnesium complex underwent reversible one-electron oxidation 40 mV more easily than the corresponding monomeric porphyrin.