Reaction Centers Of Photosynthetic Bacteria Research Articles

Метод функций Грина для расчета нестационарных спектров люминесценции неравновесных молекулярных систем

Interest in ultrafast photochemical processes is due to their role in wildlife and the possibility of using them in solar energy conversion devices. Significant part of experimental research in this area is carried out using different spectroscopic techniques, for example, based on recording the dynamic response of the system to optical excitation by a short laser pulse. This method is basic for photochemistry and is used for studying both small inorganic molecules in liquids or mixtures, and complex biological objects, such as photosynthetic reaction centers of bacteria and plants. Time-resolved luminescence/absorption spectra contain information about the processes of population of the electronic and vibrational states of the system, and therefore make it possible to study the mechanisms of photoreactions. At the same time, the question of the correct interpretation of experimental data in the case of ultrafast reactions at picosecond timescales is still relevant. The traditional approach is based on the decomposition of transient spectra into the dynamic components, associated with different electronic states. This state-associated analysis turns out to be much less accurate in ultrafast nonequilibrium reactions. The spectral dynamics of the system in this case depends not only on chemical transformations (that is, changes in state populations), but also on the evolution of the spectral response for each of the states. Particularly, relaxation of high-frequency intramolecular vibrations in ultrafast reactions was shown to cause not only a shift in the luminescence spectrum, but also significant changes in spectral profiles themselves. An assumption about the invariable shape of individual spectral components cannot be justified here. Relevant analysis of spectral dynamics in such systems thus requires taking into account the nonequilibrium state of intramolecular degrees of freedom and the environment. Development of theoretical models of nonequilibrium processes, as well as software tools for numerical simulation of spectral dynamics and the fitting techniques for experimental results data, allows us to improve the relevance of the analysis. This study is devoted to the development of a mathematical model of spectral dynamics of macromolecular systems, in which photoexcitation triggers a series of ultrafast electron transfer reactions involving several redox centers. The main attention is paid to accounting for nonequilibrium states of the medium and intramolecular degrees of freedom formed both at the stage of photoexcitation and in the course of a multistage reaction. This allows us to expand the range of phenomena under study and apply the model for interpretation of experimental data on multistage charge transfer in biological objects. The model is based on the semiclassical theory of multistage electron transfer in a multicomponent non-Debye solvent, as well as the Green’s function method for the classical (polarization) and quantum (intramolecular) coordinates of the system.

Thermodynamic View of Proton Activated Electron Transfer in the Reaction Center of Photosynthetic Bacteria.

The temperature dependence of the sequential coupling of proton transfer to the second interquinone electron transfer is studied in the reaction center proteins of photosynthetic bacteria modified by different mutations and treatment by divalent cations. The Eyring plots of kinetics were evaluated by the Marcus theory of electron and proton transfer. In mutants of electron transfer limitation (including the wild type), the observed thermodynamic parameters had to be corrected for those of the fast proton pre-equilibrium. The electron transfer is nonadiabatic with transmission coefficient 6 × 10-4, and the reorganization energy amounts to 1.2 eV. If the proton transfer is the rate limiting step, the reorganization energy and the works terms fall in the range of 200-500 meV, depending on the site of damage in the proton transfer chain. The product term is 100-150 meV larger than the reactant term. While the electron transfer mutants have a low free energy of activation (∼200 meV), the proton transfer variants show significantly elevated levels of the free energy barrier (∼500 meV). The second electron transfer in the bacterial reaction center can serve as a model system of coupled electron and proton transfer in other proteins or ion channels.

Role of Coherence in Excitation Transfer Efficiency to the Reaction Center in Photosynthetic Bacteria Chlorobium tepidum

AbstractWe investigate the effect of coherence to the excitation transfer efficiency (ETE) in photosynthetic bacteria Chlorobium tepidum. We have modelled the monomer of Fenna‐Matthews‐Olson (FMO) complex as consisting of eight bacteriochlorophyll‐a sites, while explicitly consider reaction center core complex (RCC) as an additional site. With the use of realistic bath spectrum and several dominant vibronic modes in the non‐Markovian master equation, in an effective 9‐site model, we have compared the ETE for an initial pure state and an initial mixed state. We observe that the initial pure state relaxes efficiently to increase the trapping at the RCC. We further illustrate that the coherence play a competitive role to block the back transfer of excitation from RCC pigment to FMO complex and hence to maximize the ETE.

Chemical rescue of H+ delivery in proton transfer mutants of reaction center of photosynthetic bacteria

In the native and most mutant reaction centers of bacterial photosynthesis, the electron transfer is coupled to proton transfer and is rate limiting for the second reduction of QB− → QBH2. In the presence of divalent metal ions (e.g. Cd2+) or in some (“proton transfer”) mutants (L210DN/M17DN or L213DN), the proton delivery to QB− is made rate limiting and the properties of the proton pathway can be directly examined. We found that small weak acids and buffers in large concentrations (up to 1 M) were able to rescue the severely impaired proton transfer capability differently depending on the location of the defects: lesions at the protein surface (proton gate H126H/H128H + Cd2+), beneath the surface (M17DN + Cd2+, L210DN/M17DN) or deep inside the protein (L213DN) could be completely, partially or to very small extent recovered, respectively. Small zwitterionic acids (azide/hydrazoic acid) and buffers (tricine) proved to be highly effective rescuers consistent with their enhanced binding affinity and access to any of the proton acceptors (including QB− itself) in the pathway. As a consequence, back titration of the protons at L212Glu could be observed as a pH-dependence of the rate constant of the charge recombination in the presence of azide or formate. Model calculations support the collective influence of the acid cluster on the change of the protonation states upon extension of the cluster with the bound small acid. In proton transfer mutants, the rescuing agents decreased the free energy of activation together with their enthalpic and entropic components. This is in agreement with the hypothesis that they function as protein-penetrating protonophores delivering protons into the chain and select dominating paths out of many alternate routes. We estimate that the proton delivery will be accelerated in one pathway out of 100–200 alternate pathways. The implications for design of the chemical recovery of impaired intra-protein proton transfer pathways in proton transfer mutants are discussed.

Characterization of mercury(II)-induced inhibition of photochemistry in the reaction center of photosynthetic bacteria.

Mercuric contamination of aqueous cultures results in impairment of viability of photosynthetic bacteria primarily by inhibition of the photochemistry of the reaction center (RC) protein. Isolated reaction centers (RCs) from Rhodobacter sphaeroides were exposed to Hg2+ ions up to saturation concentration (~ 103 [Hg2+]/[RC]) and the gradual time- and concentration-dependent loss of the photochemical activity was monitored. The vast majority of Hg2+ ions (about 500 [Hg2+]/[RC]) had low affinity for the RC [binding constant Kb ~ 5mM-1] and only a few (~ 1 [Hg2+]/[RC]) exhibited strong binding (Kb ~ 50μM-1). Neither type of binding site had specific and harmful effects on the photochemistry of the RC. The primary charge separation was preserved even at saturation mercury(II) concentration, but essential further steps of stabilization and utilization were blocked already in the 5 < [Hg2+]/[RC] < 50 range whose locations were revealed. (1) The proton gate at the cytoplasmic site had the highest affinity for Hg2+ binding (Kb ~ 0.2μM-1) and blocked the proton uptake. (2) Reduced affinity (Kb ~ 0.05μM-1) was measured for the mercury(II)-binding site close to the secondary quinone that resulted in inhibition of the interquinone electron transfer. (3) A similar affinity was observed close to the bacteriochlorophyll dimer causing slight energetic changes as evidenced by a ~ 30nm blue shift of the red absorption band, a 47meV increase in the redox midpoint potential, and a ~ 20meV drop in free energy gap of the primary charge pair. The primary quinone was not perturbed upon mercury(II) treatment. Although the Hg2+ ions attack the RC in large number, the exertion of the harmful effect on photochemistry is not through mass action but rather a couple of well-defined targets. Bound to these sites, the Hg2+ ions can destroy H-bond structures, inhibit protein dynamics, block conformational gating mechanisms, and modify electrostatic profiles essential for electron and proton transfer.

Synthesis of a cofacial chlorin dimer of defined symmetry

Special pair chlorophylls arranged in a cofacial dimeric structure play an important role in the initial step of light induced electron transfer of photosynthetic reaction centers of bacteria and plants. For mimicking the natural photosynthetic reaction center we aimed on synthesis of an artificial special pair 13 constructed from two chlorin subunits 5a, b and a rigid biphenylene spacer moiety 11. Due to the reduced C2h symmetry of the chlorin units compared with so far used D4h porphyrins and due to the rigid spacer a cofacial dimer of defined symmetry and distance was obtained.

Mechanism and Reaction Coordinate of Directional Charge Separation in Bacterial Reaction Centers.

Using first-principles molecular dynamics, we predict the reaction coordinate and mechanism of the first charge-separation step in the reaction center of photosynthetic bacteria in a model including the special pair (P) and closest relevant residues. In the ground state, a dynamical localization of the highest occupied orbital is found to be a defining characteristic of P. This feature is linked to the tuning of the orbital energy levels by the coupling with two collective low-frequency vibrational modes. After electronic excitation, we demonstrate one specific mode that couples to P*, representing the reaction coordinate along which the excited state develops. The characteristic vibrational coordinate we predict to be the rotation of an axial histidine (HisM202), which selectively lowers the energy of one (PM) of the two bacteriochlorophylls in P. This leads to a unidirectional displacement of electron density to establish PL(+)PM(-) charge-transfer character, a hypothesis well-supported by an extensive framework of experimental evidence.

Kinetics of reduction of bacteriochlorophyll dimer in reaction centers of photosynthetic bacteria

Kinetic curves of reduction of the oxidized bacteriochlorophyll dimer by the proximal heme of cytochrome in seven mutated reaction centers from Rps. viridis was measured in the temperature range of 295-10 K under an ambient potential when two high-potential hemes were reduced. The data are analyzed in frames of a model which accounts for slow medium dynamics (the diffusion-reaction equation) and the quantum effect in the modes responsible for reorganization of the cofactors and the medium. The model reproduces the observed nonexponential kinetics down to the lowest temperature where the fast kinetic component still survives. The modeling results in determination of an average characteristic time for re-orientation of dipoles of the protein matrix as a function of temperature. At temperatures above the glass-transition temperature, this function shows Arrhenius behavior with the activation energy varying between the values of 0.5 eV for wild type Rps. viridis and 0 eV for Rps. sulfoviridis found previously. Possible reasons for disappearance of the fast kinetic component in some reaction centers under study at low temperatures are discussed.

Kinetic bacteriochlorophyll fluorometer

A pump and probe fluorometer with a laser diode as single light source has been constructed for measurement of fast induction and relaxation of the fluorescence yield in intact cells, chromatophores and isolated reaction centers of photosynthetic bacteria. The time resolution of the fluorometer is limited by the repetition time of the probing flashes to 20 micros. The apparatus offers high sensitivity, excellent performance and can become a versatile device for a range of demanding applications. Some of them are demonstrated here including fast and easy investigation of the (1) organization and redox state of the photosynthetic apparatus of the intact cells of different bacterial strains and mutants and (2) electron transfer reactions on donor and acceptor sides of isolated reaction centers. The compact design of the mechanics, optics, electronics, and data processing makes the device easy to use as outdoor instrument or to integrate into larger measuring systems.

Proton-Transfer Reactions in Reaction Center of Photosynthetic BacteriaRhodobacter sphaeroides

The mechanism of proton uptakes by the secondary ubiquinone (Q(B)) in the reaction center of the photosynthetic bacteria Rhodobacter sphaeroides is investigated theoretically. Two protons are transferred to the secondary ubiquinone (Q(B)) upon two electron transfers to it. The pathways of the proton transfers are explored through molecular dynamics and free-energy calculations by a molecular mechanical method and potential energy surface calculations by a hybrid ab initio quantum mechanical/molecular mechanical method. Initial locations of donor protons are identified at Glu-L212 and at Asp-L210. It is shown that the first proton transfer takes place from Glu-L212 to Q(B) through their direct hydrogen bond only when the second electron is transferred to Q(B). The second proton transfer from Asp-L210 to Q(B) proceeds through long-range hydrogen-bond network bridges connecting them. The hydrogen-bond network bridges are occasionally formed with several water molecules in the water molecular structural fluctuation dynamics of the "proton channel". The activation energy barrier along the second proton-transfer path thus formed is consistent with the experimental rate. It is also found that there exist very strong interactions among water molecules and a protonated carboxyl group of Asp-L210, suggesting formation of a hydronium ion in the surroundings of negatively charged acidic groups in the proton channel.

Nanophotobiocatalysts based on mesoporous titanium dioxide films conjugated with enzymes and photosynthetic reaction centers of bacteria

Nanophotobiocatalysts based on mesoporous titanium dioxide films conjugated with enzymes and photosynthetic reaction centers of bacteria

A Discrete Supramolecular Conglomerate Composed of Two Saddle‐Distorted Zinc(II)‐Phthalocyanine Complexes and a Doubly Protonated Porphyrin with Saddle Distortion Undergoing Efficient Photoinduced Electron Transfer

Porphyrins (Por) and phthalocyanines (Pc) exhibit lightharvesting efficiency for producing charge-separated states as models of the reaction center in photosynthetic bacteria and photovoltaic cells for energy conversion. The use of supramolecular assemblies to model the functionality of the reaction center is an attractive and fruitful strategy to develop photofunctional materials and devices. Porphyrins exhibit strong Soret bands around 400 to 450 nm, whereas phthalocyanines show strong Q bands around 700 to 800 nm. Thus, the combination of those two p systems can cover nearly the whole range of the visible region and can be a useful strategy for development of photofunctional materials for efficient light-energy conversion. Attempts have so far been made to synthesize covalently linked Por–Pc heterodyad molecules and construct Por–Pc heterosupramolecules. Recently, ZnPor and ZnPc have been reported to form two-dimensional arrays on gold surfaces, and the formation of a cofacial ZnPor–ZnPc coordination tetrad has also been reported. However, a crystal structure determination of a discrete supramolecular assembly composed of both Por and Pc has yet to be reported. In addition, since the Q-band absorption of Pc usually overlaps the wavelength of fluorescence of Por, energy transfer is favored over electron transfer in most heterodyads. We have developed supramolecular assemblies based on a saddle-distorted nonplanar porphyrin, dodecaphenylporphyrin (H2DPP), and its metal complexes. [11–13] The saddle distortion facilitates protonation of pyrrole nitrogen atoms to allow access to a stable diprotonated porphyrin, which can act as an electron acceptor. In addition, the saddle distortion affords higher Lewis acidity at the metal center to maintain axial coordination of ligands, as a result of poor overlap of the pyrrole nitrogen lone pair orbitals with d orbitals of the metal center. In contrast, the Zn complex of the saddle-distorted phthalocyanine 1,4,8,11,15,18,22,25-octaphenylphthalocyanine (H2OPPc) exhibits a lower oxidation potential relative to the corresponding porphyrin complex. To construct supramolecular conglomerates composed of both porphyrin and phthalocyanine in a well-defined manner, we have taken advantage of saddle distortion of both components. Herein, we report formation of a discrete supramolecular assembly composed of H4DPP 2+ and [Zn(OPPc)] connected by 4-pyridinecarboxylate (4-PyCOO ) with coordination and hydrogen bonding (Figure 1). The supramolecular conglomerate [(H4DPP){Zn(OPPc)(k-N-4-PyCOO)}2] (1) was synthesized by reaction of [H4DPP](4-PyCOO)2 (2) and Zn(OPPc) (3) in toluene. We crystallized and isolated 1 in pure form by vapor diffusion of hexanes into solution of the mixture in toluene. X-ray crystallography of 1 unambiguously established its structure (Figure 2a).

Mechanism of Quinol Oxidation by Ferricenium Produced by Light Excitation in Reaction Centers of Photosynthetic Bacteria

The kinetics and thermodynamics of cyclic electron transfer through the isolated reaction center protein of photosynthetic bacterium Rhodobacter sphaeroides were determined in detergent (Triton X-100) solution. The redox reactions between the reducing (ubiquinol-0 or ubiquinol-10) and oxidizing species (ferricenium, ferricytochrome, or ferricyanide) produced chemically or by light excitation of the protein were monitored by absorption changes of the reactants and by acidification of the solution accompanied with the disappearance of the quinol. The bimolecular rate constants of reactions of anionic ubiquinol-0 with different oxidizing agents showed large variation: 5 x 10(8) M(-1) s(-1) for ferricenium, 3.5 x 10(5) M(-1) s(-1) for ferricyanide, and 1.5 x 10(5) M(-1) s(-1) for ferricytochrome. Although the redox partners were created in pairs by the same protein promptly after light excitation, their bimolecular redox reaction was not observed even in the case of the fastest reacting partners of ferricenium and ubiquinol-0. Instead, they equilibrate with the corresponding (donor and acceptor) pools before the electron is transferred. The (logarithms of the) observed rate constants of quinol oxidation showed steep pH-dependence for water soluble ubiquinol-0 (slope +1) and mild pH-dependence for hydrophobic ubiquinol-10 (slope approximately 0.25). Combined with studies of the ionic strength dependence of the rate, it was concluded that the electron-transfer pathways of ubiquinol-0 and ubiquinol-10 oxidation started from their anionic and neutral forms, respectively. The mild pH-dependence of the rate of ubiquinol-10 oxidation came from the electrostatic interactions between ferricenium and the pH-dependent surface charges of the reaction center. The results help to understand, monitor, and design (cyclic) electron flow in bioenergetic proteins.

Ultrafast Electron Transfer in Photosynthesis: Reduced Pheophytin and Quinone Interaction Mediated by Conical Intersections

The mechanism of electron transfer (ET) from reduced pheophytin (Pheo(-)) to the primary stable photosynthetic acceptor, a quinone (Q) molecule, is addressed by using high-level ab initio computations and realistic molecular models. The results reveal that the ET process involving the (Pheo(-) + Q) and (Pheo + Q(-)) oxidation states can be essentially seen as an ultrafast radiationless transition between the two hypersurfaces taking place via conical intersections (CIs). According to the present findings, an efficient ultrafast ET implies that the Pheo- and Q move toward each other in a given preferential parallel orientation, reaching the most effective arrangement for ET at intermolecular distances (R) around 5-3 Angstrom, where the lowest CIs are predicted. Favored donor/acceptor interactions are related to orientations with some overlap between the lowest occupied molecular orbitals (LUMO) of the two systems, and they lead to state-crossings at an earlier stage of the movement (larger R). Furthermore, when the topology of the interacting moieties does not make possible the LUMOs overlap, the corresponding diabatic potential energy curves do not intersect. Thus, it is anticipated that large scale motions, which are difficult to monitor experimentally, are actually occurring in the photosynthetic reaction centers of bacteria, algae, and higher plants, to fulfill the observed ultrafast ET processes.

Artificial Photosynthetic Reaction Centers: Mimicking Sequential Electron and Triplet‐Energy Transfer

An artificial photosynthetic reaction center consisting of a carotenoid (C), a dimesitylporphyrin (P), and a bis(heptafluoropropyl)porphyrin (P(F)), C-P-P(F) , and the related triad in which the central porphyrin has been metalated to give C-P(Zn)-P(F) have been synthesized and characterized by transient spectroscopy. These triads are models for amphipathic triads having a carboxylate group attached to the P(F) moiety; they are designed to carry out redox processes across lipid bilayers. Triad C-P-P(F) undergoes rapid singlet-singlet energy transfer between the porphyrin moieties, so that their excited states are in equilibrium. In benzonitrile, photoinduced electron transfer from the first excited singlet state of P and hole transfer from the first excited singlet state of P(F) yield the initial charge-separated state C-P(.) (+)-P(F) (.) (-). Subsequent hole transfer to the carotenoid moiety generates the final charge-separated state C(.) (+)-P-P(F) (.) (-), which has a lifetime of 1.1 mus and is formed with a quantum yield of 0.24. In triad C-P(Zn)-P(F) energy transfer from the P(Zn) excited singlet to the P(F) moiety yields C-P(Zn)-(1)P(F) . A series of electron-transfer reactions analogous to those observed in C-P-P(F) generates C(.) (+)-P(Zn)-P(F) (.) (-), which has a lifetime of 750 ns and is formed with a quantum yield of 0.25. Flash photolysis experiments in liposomes containing an amphipathic version of C-P(Zn)-P(F) demonstrate that the added driving force for photoinduced electron transfer in the metalated triad is useful for promoting electron transfer in the low-dielectric environment of artificial biological membranes. In argon-saturated toluene solutions of C-P-P(F) and C-P(Zn)-P(F) , charge separation is not observed and a considerable yield of triplet species is generated upon excitation of the porphyrin moieties. In both triads triplet energy localized in the P(F) moiety is channeled to the carotenoid chromophore by a triplet energy-transfer relay mechanism. Certain photophysical characteristics of these triads, including the sequential electron transfer and the triplet energy-transfer relay mechanism, are reminiscent of those observed in natural reaction centers of photosynthetic bacteria.

Analysis of Kinetics of Electron Transfer in the Reaction Centers of Photosynthetic Bacteria Using the Rips—Jortner Model

Analysis of Kinetics of Electron Transfer in the Reaction Centers of Photosynthetic Bacteria Using the Rips—Jortner Model

Construction of Light‐Harvesting Materials

AbstractFor Abstract see ChemInform Abstract in Full Text.

光捕集機能体の構築

ImidazolylporphyrinatoZn gave a complementary coordination dimer of extraordinary stability. It exhibited excellent properties as a mimic of the structure and the function of the special pair of the reaction center in photosynthetic bacteria. Coupling of imidazolylporphyrinatoZn at the meso position afforded an array of a few hundreds nanometer to a micrometer scale. The linear array could be regarded as a unit of energy/electron transfer since no fluorescence quenching was observed by the array formation. When imidazolylporphyrinatoZn's were linked by a meta-phenylene grouping, macrocyclic porphyrin rings composed of 10 and 12 porphyrin units were obtained to represent the the light harvesting complex B 850 of photosynthetic bacteria. The linear array was attached on gold surface by thiolate extended from porphyrin. The assembled porphyrins have demonstrated significant improvement of the efficiency of photocurrent generation.

Inter- and Intraspecific Variation in Excited-state Triplet Energy Transfer Rates in Reaction Centers of Photosynthetic Bacteria¶

Inter- and Intraspecific Variation in Excited-state Triplet Energy Transfer Rates in Reaction Centers of Photosynthetic Bacteria¶

Self-Regulation Phenomena in Bacterial Reaction Centers. I. General Theory

A model for light-induced charge separation in a donor-acceptor system of the reaction center of photosynthetic bacteria is described. This description is predicated on a self-regulation of the flow of photo-activated electrons due to self-consistent, slow structural rearrangements of the macromolecule. Effects of the interaction between the separated charges and the slow structural modes of the biomolecule may accumulate during multiple, sequential charge transfer events. This accumulation produces non-linear dynamic effects on system function, providing a regulation of the charge separation efficiency. For a biomolecule with a finite number of different charge-transfer states, the quasi-stationary populations of these states with a localized electron on different cofactors may deviate from a Lagmuir law dependence with actinic light intensity. Such deviations are predicted by the model to be due to light-induced structural changes. The theory of self-regulation developed here assumes that light-induced changes in the effective adiabatic potential occur along a slow structural coordinate. In this model, a “light-adapted” conformational state appears when bifurcation produces a new minimum in the adiabatic potential. In this state, the lifetime of the charge-separated state may be quite different from that of the “dark-adapted” conformation. The results predicted by this theory agree with previously obtained experimental results on photosynthetic reaction centers.