Density functional calculations modelling tyrosine oxidation in oxygenic photosynthetic electron transfer

Hybrid density functional calculations are used to model tyrosine oxidation during electron transfer reactions of photosystem II. The predicted frequency values for the 7a and deltaCOH modes of the reduced form and the 7a mode of the oxidised radical form are in excellent agreement with experimental data obtained for Mn and Ca depleted systems by Hienerwadel et al. [Biochemistry 36 (1997) 15447] and Berthomieu et al. [Biochemistry 37 (1998) 10547]. The calculations confirm that the two tyrosines Y(D) and Y(Z) are protonated in the reduced form. On oxidation the larger 7a frequency value observed experimentally for Y(Z*) can be best explained by a greater localisation of the protonic charge released on formation of this tyrosyl free radical.     

Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms

Photosynthesis Research - This minireview is written in honor of Vladimir A. Shuvalov, a pioneer in the area of primary photochemistry of both oxygenic and anoxygenic photosyntheses (See a News...     

Divergent pathways of photosynthetic electron transfer: The autonomous oxygenic and anoxygenic photosystems

The aim of this article is to assemble and integrate, from a personal perspective of a research participant, seldom examined evidence that is incompatible with some basic tenets of photosynthetic electron transport, the cornerstone of which is the Z scheme. The nonconforming evidence pertaining to the mode of ferredoxin reduction and the role of the copper redox protein, plastocyanin, indicates that contrary to the Z scheme ferredoxin is reduced in two experimentally distinguishable ways: oxygenically by PS II (renamed the oxygenic photosystem), without the participation of PS I, and anoxygenically by PS I (renamed the anoxygenic photosystem). It also indicates that plastocyanin is not only, as the Z scheme asserts, the electron donor to the reaction center chlorophyll of PS I (P700) but also to the reaction center chlorophyll of PS II (P680). Other unconventional findings include evidence that the fully functional oxygenic photosystem, when operating separately from the anoxygenic photosystem, reduces plastoquinone to plastoquinol and subsequently oxidizes plastoquinol by two pathways acting in concert: one being the universally recognized DBMIB-sensitive pathway via the Rieske iron-sulfur center of the cytochrome bf complex and the other, a hitherto unrecognized, DBMIB-insensitive electron transport pathway around P680 that centers on cytochrome b-559. These nonconforming findings form the basis of an alternate hypothesis of photosynthetic electron transport that modifies and complements the Z scheme.Abbreviations PS photosystem - PQ oxidized plastoquinone - PQH₂ reduced plastoquinone (plastoquinol) - Q_A and Q_B specialized membrane-bound forms of PQ - PC plastocyanin - Fd ferredoxin - BISC F_AF_B, membrane-bound iron-sulfur centers of PS I - DBM1B 2,5-dibromo-3-methyl-6-isopropyl-n-benzoquinone (dibromothymoquinone) - DNP-INT dinitrophenol ether of iodonitrothymol - NADP⁺ NADPH, oxidized and reduced forms of nicotinamide adenine dinucleotide phosphate - FCCP carbonylcyanide-p-trifluoromethoxyphenyl-hydrazone - CCCP carbonyl cyanide-3-chlorophenylhydrazone - SF 6847 2,6,-di-(t-butyl)-4-(2,2-dicyanovinyl) phenol - diuron (DCMU) 3-(3,4-dichlorophenyl)-1,1-dimethylurea - EPR electron paramagnetic resonance - DCIP 2,6-dichloro-phenolindophenol - UHDBT 5-(n-undecyl)-6-hydroxy-4-7-dioxobenzothiazole; cytochrome b-559_HP-cytochrome b-559_LP, high- and low potential states of cytochrome b-559 - oxygenic reductions reductions in which water is the electron donor - BBY PS II preparation made according to Berthold et al. (1981) Dedicated to Professor Achim Trebst on his 65th birthday.Based in part on lecture in Advanced Course on Trends in Photosynthesis Research, Palma de Mallorca, Spain, September 18, 1990.     

Uphill energy transfer in a chlorophyll d-dominating oxygenic photosynthetic prokaryote, Acaryochloris marina

The steady-state fluorescence properties and uphill energy transfer were analyzed on intact cells of a chlorophyll (Chl) d-dominating photosynthetic prokaryote, Acaryochloris marina. Observed spectra revealed clear differences, depending on the cell pigments that had been sensitized; using these properties, it was possible to assign fluorescence components to specific Chl pigments. At 22 degrees C, the main emission at 724 nm came from photosystem (PS) II Chl d, which was also the source of one additional band at 704 nm. Chl a emissions were observed at 681 nm and 671 nm. This emission pattern essentially matched that observed at -196 degrees C, as the main emission of Chl d was located at 735 nm, and three minor bands were observed at 704 nm, 683 nm, and 667 nm, originating from Chl d, Chl a, and Chl a, respectively. These three minor bands, however, had not been sensitized by carotenoids, suggesting specific localization in PS II. At 22 degrees C, excitation of the red edge of the absorption band (which, at 736 nm, was 20 nm longer than the absorption maximum), resulted in fluorescence bands of Chl d at 724 nm and of Chl a at 682 nm, directly demonstrating an uphill energy transfer in this alga. This transfer is a critical factor for in vivo activity, due to an inversion of energy levels between antenna Chl d and the primary electron donor of Chl a in PS II.     

Density functional theory calculations for resveratrol

The calculations based on the density functional theory (DFT) have been used to study the structure-activity of resveratrol in the chain reaction of autooxidation. According to the geometry obtained by using a B3LYP/6-31G**, the HOMO, LUMO of resveratrol and the spin density, the single electron distribution of the 4'- and 5-radical of resveratrol were calculated, it was found that resveratrol is a potential antioxidant. The 4'-hydroxyl group of resveratrol is more reactive than 3- and 5-positions because of the resonance effects. The dominant structure of the resveratrol radicals is a semiquinone structure which determines the stability of radicals, and the unpaired electron is mainly distributed to the O-atom and its ortho and para positions. The antioxidant activity of resveratrol is related to the spin density and the unpaired electron distribution of the O-atom.     

Electron transport and transmembrane proton transfer in photosynthetic systems of oxygenic type in Silico

Using a mathematical model of light-induced stages of photosynthesis, which takes into account the key stages of pH-dependent regulation on the acceptor and donor sides of PS I, we analyzed electron and proton transport in chloroplasts of higher plants and in cyanobacterial cells. A comparison of computer simulations with experimental data showed that our model adequately described the complex nonmonotonic kinetics of the light-induced redox transients of P₇₀₀. Effects of atmospheric gases (CO₂ and O₂) on the kinetics of photooxidation of P₇₀₀ and generation of the transmembrane pH difference were studied. We also analyzed how cyclic electron transport influenced the kinetics of electron transfer, intrathylakoid pH, and ATP production. Within the framework of our model, we described the time courses of electron flow through PS II and distribution of electron fluxes on the acceptor side of PS I in chloroplasts and in cyanobacteria. It was demonstrated that contributions of cyclic electron transport and electron flow to O₂ (the Mehler reaction) were significant during the initial phase of the induction period, but diminished upon activation of the Calvin-Benson cycle.     

Virtual intermediates in photosynthetic electron transfer.

We explore the possibility of virtual transfer in the primary charge separation of photosynthetic bacteria within the context of several types of experimental data. We show that the peak that might be expected in the virtual rate as electric fields vary the intermediate state energy is severely broadened by coupling to high-frequency modes. The Stark absorption kinetics data are thus consistent with virtual transfer in the primary charge separation. High-frequency coupling also makes the temperature dependence weak over a wide range of parameters. We demonstrate that Stark fluorescence anisotropy data, usually taken as evidence of virtual transfer, can in fact be consistent with two-step transfer. We suggest a two-pulse excitation experiment to quantify the contributions from two-step and virtual transfer. We show that virtual absorption into a charge transfer state can make a substantial contribution to the Stark absorption spectrum in a way that is not related to any derivative of the absorption spectrum.     

Electrostatics and proton transfer in photosynthetic water oxidation

Photosystem II (PSII) oxidizes two water molecules to yield dioxygen plus four protons. Dioxygen is released during the last out of four sequential oxidation steps of the catalytic centre (S(0) --> S(1), S(1) --> S(2), S(2) --> S(3), S(3) --> S(4) --> S(0)). The release of the chemically produced protons is blurred by transient, highly variable and electrostatically triggered proton transfer at the periphery (Bohr effect). The extent of the latter transiently amounts to more than one H(+)/e(-) under certain conditions and this is understood in terms of electrostatics. By kinetic analyses of electron-proton transfer and electrochromism, we discriminated between Bohr-effect and chemically produced protons and arrived at a distribution of the latter over the oxidation steps of 1 : 0 : 1 : 2. During the oxidation of tyr-161 on subunit D1 (Y(Z)), its phenolic proton is not normally released into the bulk. Instead, it is shared with and confined in a hydrogen-bonded cluster. This notion is difficult to reconcile with proposed mechanisms where Y(Z) acts as a hydrogen acceptor for bound water. Only in manganese (Mn) depleted PSII is the proton released into the bulk and this changes the rate of electron transfer between Y(Z) and the primary donor of PSII P(+)(680) from electron to proton controlled. D1-His190, the proposed centre of the hydrogen-bonded cluster around Y(Z), is probably further remote from Y(Z) than previously thought, because substitution of D1-Glu189, its direct neighbour, by Gln, Arg or Lys is without effect on the electron transfer from Y(Z) to P(+)(680) (in nanoseconds) and from the Mn cluster to Y(ox)(Z).     

Relationship between the oxidation potential of the bacteriochlorophyll dimer and electron transfer in photosynthetic reaction centers

The primary electron donor in the photosynthetic reaction center from purple bacteria is a bacteriochlorophyll dimer containing four conjugated carbonyl groups that may form hydrogen bonds with amino acid residues. Spectroscopic analyses of a set of mutant reaction centers confirm that hydrogen bonds can be formed between each of these carbonyl groups and histidine residues in the reaction center subunits. The addition of each hydrogen bond is correlated with an increase in the oxidation potential of the dimer, resulting in a 355-mV range in the midpoint potential. The resulting changes in the free-energy differences for several reactions involving the dimer are related to the electron transfer rates using the Marcus theory. These reactions include electron transfer from cytochrome c₂ to the oxidized dimer, charge recombination from the primary electron acceptor quinone, and the initial forward electron transfer.     

Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: a pulsed photoacoustic study of electron transfer in photosystem I reveals a similarity to bacterial reaction centers in both volume change and entropy

The thermodynamic properties of electron transfer in biological systems are far less known in comparison with that of their kinetics. In this paper the enthalpy and entropy of electron transfer in the purified photosystem I trimer complexes from Synechocystis sp. PCC 6803 have been studied, using pulsed time-resolved photoacoustics on the 1 micros time scale. The volume contraction of reaction centers of photosystem I, which results directly from the light-induced charge separation forming P(700+F(A)/F(B-) from the excited-state P700*, is determined to be -26 +/- 2 A3. The enthalpy of the above electron-transfer reaction is found to be -0.39 +/- 0.1 eV. Photoacoustic estimation of the quantum yield of photochemistry in the purified photosystem I trimer complex showed it to be close to unity. Taking the free energy of the above reaction as the difference of their redox potentials in situ allows us to calculate an apparent entropy change (TDeltaS) of +0.35 +/- 0.1 eV. These values of DeltaV and TDeltaS are similar to those of bacterial reaction centers. The unexpected sign of entropy of electron transfer is tentatively assigned, as in the bacterial case, to the escape of counterions from the surface of the particles. The apparent entropy change of electron transfer in biological system is significant and cannot be neglected.     

Density functional calculations on model tyrosyl radicals.

A gradient-corrected density functional theory approach (PWP86) has been applied, together with large basis sets (IGLO-III), to investigate the structure and hyperfine properties of model tyrosyl free radicals. In nature, these radicals are observed in, e.g., the charge transfer pathways in photosystem II (PSII) and in ribonucleotide reductases (RNRs). By comparing spin density distributions and proton hyperfine couplings with experimental data, it is confirmed that the tyrosyl radicals present in the proteins are neutral. It is shown that hydrogen bonding to the phenoxyl oxygen atom, when present, causes a reduction in spin density on O and a corresponding increase on C4. Calculated proton hyperfine coupling constants for the beta-protons show that the alpha-carbon is rotated 75-80 degrees out of the plane of the ring in PSII and Salmonella typhimurium RNR, but only 20-30 degrees in, e.g., Escherichia coli, mouse, herpes simplex, and bacteriophage T4-induced RNRs. Furthermore, based on the present calculations, we have revised the empirical parameters used in the experimental determination of the oxygen spin density in the tyrosyl radical in E. coli RNR and of the ring carbon spin densities, from measured hyperfine coupling constants.     

Inhibition of photosynthetic electron transfer by amphotericin B

The polyene antibiotic amphotericin B inhibits photosynthetic electron transfer by Class II maize mesophyll chloroplasts, from water to FeCN, DCIP and diquat but not to plastocyanin. Photosystem 1 activity is also inhibited by amphotericin B, but ferredoxin-NADP reductase activity is not affected. The activity of all the photosynthetic electron transfer systems inhibited by amphotericin B can be restored by the addition of carrier amounts of plastocyanin. The results suggest that amphotericin B inhibits photosynthetic electron transfer by acting only at the plastocyanin site in the chain, and that the primary site of reduction of FeCN and DCIP from water by Class II chloroplasts lies on the reducing side of photosystem 1.     

Thermodynamics of electron transfer in oxygenic photosynthetic reaction centers: volume change, enthalpy, and entropy of electron-transfer reactions in manganese-depleted photosystem II core complexes

We have previously reported the thermodynamic data of electron transfer in photosystem I using pulsed time-resolved photoacoustics [Hou et al. (2001) Biochemistry 40, 7109-7116]. In the present work, using preparations of purified manganese-depleted photosystem II (PS II) core complexes from Synechocystis sp. PCC 6803, we have measured the DeltaV, DeltaH, and estimated TDeltaS of electron transfer on the time scale of 1 micros. At pH 6.0, the volume contraction of PS II was determined to be -9 +/- 1 A3. The thermal efficiency was found to be 52 +/- 5%, which corresponds to an enthalpy change of -0.9 +/- 0.1 eV for the formation of the state P680+Q(A-) from P680*. An unexpected volume expansion on pulse saturation of PS II was observed, which is reversible in the dark. At pH 9.0, the volume contraction, the thermal efficiency, and the enthalpy change were -3.4 +/- 0.5 A3, 37 +/- 7%, and -1.15 +/- 0.13 eV, respectively. The DeltaV of PS II, smaller than that of PS I and bacterial centers, is assigned to electrostriction and analyzed using the Drude-Nernst equation. To explain the small DeltaV for the formation of P680+Q(A-) or Y(Z*)Q(A-), we propose that fast proton transfer into a polar region is involved in this reaction. Taking the free energy of charge separation of PS II as the difference between the energy of the excited-state P680* and the difference in the redox potentials of the donor and acceptor, the apparent entropy change (TDeltaS) for charge separation of PS II is calculated to be negative, -0.1 +/- 0.1 eV at pH 6.0 (P680+Q(A-)) and -0.2 +/- 0.15 eV at pH 9.0 (Y(Z*)Q(A-)). The thermodynamic properties of electron transfer in PS II core reaction centers thus differ considerably from those of bacterial and PS I reaction centers, which have DeltaV of approximately -27 A3, DeltaH of approximately -0.4 eV, and TDeltaS of approximately +0.4 eV.     

Structural aspects of vectorial electron transfer in photosynthetic reaction centers

Structural aspects of photosynthetic reaction centers in bacteria and plants are discussed in relation with the ability of these structures to perform a photoinduced electron transfer from one side of the membrane to the other. A comparison is made with recently synthesized artificial models. Functional similarities between the acceptor sides of bacterial and of Photosystem-II centers are utilized to hypothesize on their structure.This review corresponds to a lecture delivered at the 3rd European Bioenergetics Conference, Hannover, September 1984.     

Density functional calculations of 15N chemical shifts in solvated dipeptides

We performed density functional calculations to examine the effects of solvation, hydrogen bonding, backbone conformation, and the side chain on 15N chemical shielding in proteins. We used N-methylacetamide (NMA) and N-formyl-alanyl-X (with X being one of the 19 naturally occurring amino acids excluding proline) as model systems. In addition, calculations were performed for selected fragments from protein GB3. The conducting polarizable continuum model was employed to include the effect of solvent in the density functional calculations. Our calculations for NMA show that the augmentation of the polarizable continuum model with the explicit water molecules in the first solvation shell has a significant influence on isotropic 15N chemical shift but not as much on the chemical shift anisotropy. The difference in the isotropic chemical shift between the standard beta-sheet and alpha-helical conformations ranges from 0.8 to 6.2 ppm depending on the residue type, with the mean of 2.7 ppm. This is in good agreement with the experimental chemical shifts averaged over a database of 36 proteins containing >6100 amino acid residues. The orientation of the 15N chemical shielding tensor as well as its anisotropy and asymmetry are also in the range of values experimentally observed for peptides and proteins.     

Periplasmic electron carriers and photo-induced electron transfer in the photosynthetic bacterium Ectothiorhodospira sp.

A detailed analysis of the periplasmic electron carriers of the photosynthetic bacterium Ectothiorhodospira sp. has been performed. Two low mid-point redox potential electron carriers, cytochrome c′ and cytochrome c, are detected. A high potential iron–sulfur protein is the only high mid-point redox potential electron transfer component present in the periplasm. Analysis of light-induced absorption changes shows that this high potential iron–sulfur protein acts in vivo as efficient electron donor to the photo-oxidized high potential heme of the Ectothiorhodospira sp. reaction center. This revised version was published online in June 2006 with corrections to the Cover Date.     

Contrasting modes of photosynthetic enzyme regulation in oxygenic and anoxygenic prokaryotes

Enzymes that are regulated by the ferredoxin/thioredoxin system in chloroplasts — fructose-1,6-bisphosphatase (FBPase), sedoheptulose-1,7-bisphosphatase purified from two different types of photosynthetic prokaryotes (cyanobacteria, purple sulfur bacteria) and tested for a response to thioredoxins. Each of the enzymes from the cyanobacterium Nostoc muscorum, an oxygenic organism known to contain the ferredoxin/thioredoxin system, was activated by thioredoxins that had been reduced either chemically by dithiothreitol or photochemically by reduced ferredoxin and ferredoxin-thioredoxin reductase. Like their chloroplast counterparts, N. muscorum FBPase and SBPase were activated preferentially by reduced thioredoxin f. SBPase was also partially activated by thioredoxin m. PRK, which was present in two regulatory forms in N. muscorum, was activated similarly by thioredoxins f and m. Despite sharing the capacity for regulation by thioredoxins, the cyanobacterial FBPase and SBPase target enzymes differed antigenically from their chloroplast counterparts. The corresponding enzymes from Chromatium vinosum, an anoxygenic photosynthetic purple bacterium found recently to contain the NADP/thioredoxin sytem, differed from both those of cyanobacteria and chloroplasts in showing no response to reduced thioredoxin. Instead, C. vinosum FBPase, SBPase, and PRK activities were regulated by a metabolite effector, 5-AMP. The evidence is in accord with the conclusion that thioredoxins function in regulating the reductive pentose phosphate cycle in oxygenic prokaryotes (cyanobacteria) that contain the ferredoxin/thioredoxin system, but not in anoxygenic prokaryotes (photosynthetic purple bacteria) that contain the NADP/thioredoxin system. In organisms of the latter type, enzyme effectors seem to play a dominant role in regulating photosynthetic carbon dioxide assimilation.     

Density functional theory calculations on the thermodynamic properties of polynitrosoprismanes

A series of polynitrosoprismanes, C(6)H(6 - n )(NO)( n ) (n?=?1-6), considered as high energy density compounds (HEDCs), have been designed computationally. We calculated the electronic structures, the heats of formation, the specific enthalpies of combustion, the bond dissociation energies, and the strain energies of the title compounds using density functional theory (DFT) with the 6-311G** basis set. It was found that the ΔE (LUMO-HOMO) values of the title compounds decrease as the number of nitroso groups increase, and the energy gaps of the prismane derivatives are much lower than that of TATB. Their high positive heats of formation indicate that polynitrosoprismanes can store a great deal of energy. Furthermore, the HOFs for the nitrosoprismane series were observed to decrease until three nitroso groups were connected to the prismane skeleton. For the polynitrosoprismanes, the trigger bond was confirmed to be the C-C bond in the skeleton. According to our calculations, all nitrosoprismanes appear to have large strain energies, and these calculations can provide basic information that may prove useful for the molecular design of novel high energy density materials.