Mechanism Of Photosynthetic Oxygen Evolution Research Articles

Theoretical Study on the Mechanism of Photosynthetic Oxygen Evolution by ABEEM/MM/MD and BS-DFT

Theoretical Study on the Mechanism of Photosynthetic Oxygen Evolution by ABEEM/MM/MD and BS-DFT

Dynamics of Proton Transfer to Internal Water during the Photosynthetic Oxygen-Evolving Cycle.

In photosynthesis, the light-driven oxidation of water is a sustainable process, which converts solar to chemical energy and produces protons and oxygen. To enable biomimetic strategies, the mechanism of photosynthetic oxygen evolution must be elucidated. Here, we provide information concerning a critical step in the oxygen-evolving, or S-state, cycle. During this S3-to-S0 transition, oxygen is produced, and substrate water binds to the manganese-calcium catalytic site. Our spectroscopic and H218O labeling experiments show that this S3-to-S0 step is associated with the protonation of an internal water cluster in a hydrogen-bonding network, which contains calcium. When compared to the protonated water cluster, formed during a preceding step, the S1-to-S2 transition, the S3-to-S0 hydronium ion is likely to be coordinated by additional water molecules. This evidence shows that internal water and the hydrogen bonding network act as a transient proton acceptor at multiple points in the oxygen-evolving cycle.

Time-Resolved Infrared Detection of the Proton and Protein Dynamics during Photosynthetic Oxygen Evolution

Photosynthetic oxygen evolution by plants and cyanobacteria is performed by water oxidation at the Mn(4)CaO(5) cluster in photosystem II. The reaction is known to proceed via a light-driven cycle of five intermediates called S(i) states (i = 0-4). However, the detailed reaction processes during the intermediate transitions remain unresolved. In this study, we have directly detected the proton and protein dynamics during the oxygen-evolving reactions using time-resolved infrared spectroscopy. The time courses of the absorption changes at 1400 and 2500 cm(-1), which represent the reactions and/or interaction changes of carboxylate groups and the changes in proton polarizability of strong hydrogen bonds, respectively, were monitored upon flash illumination. The results provided experimental evidence that during the S(3) → S(0) transition, drastic proton rearrangement, most likely reflecting the release of a proton from the catalytic site, takes place to form a transient state before the oxidation of the Mn(4)CaO(5) cluster that leads to O(2) formation. Early proton movement was also detected during the S(2) → S(3) transition. These observations reveal the common mechanism in which proton release facilitates the transfer of an electron from the Mn(4)CaO(5) cluster in the S(2) and S(3) states that already accumulate oxidizing equivalents. In addition, relatively slow rearrangement of carboxylate groups was detected in the S(0) → S(1) transition, which could contribute to the stabilization of the S(1) state. This study demonstrates that time-resolved infrared detection is a powerful method for elucidating the detailed molecular mechanism of photosynthetic oxygen evolution by pursuing the reactions of substrate and amino acid residues during the S-state transitions.

Orientations of Carboxylate Groups Coupled to the Mn Cluster in the Photosynthetic Oxygen-Evolving Center As Studied by Polarized ATR-FTIR Spectroscopy

It is essential to clarify the structures and interactions of amino acids surrounding the Mn cluster in photosystem II (PSII) to understand the molecular mechanism of photosynthetic oxygen evolution. In this study, polarized attenuated total reflection Fourier transform infrared spectroscopy (ATR-FTIR) was applied for the first time to PSII to investigate the orientation of carboxylate groups coupled to the oxygen-evolving Mn cluster. PSII membranes from spinach were oriented on the surface of a silicon ATR crystal, and flash-induced polarized ATR-FTIR difference spectra for the S(1) --> S(2) transition (S(2)/S(1) spectra) were obtained. The distribution of membrane orientations by mosaic spread was estimated from the semiquinone CO peak in polarized Q(A)(-)/Q(A) difference spectra recorded using the same oriented sample by buffer exchange. The orientations of carboxylate groups coupled to the Mn cluster were estimated from the dichroic ratios of the symmetric COO(-) bands in the polarized S(2)/S(1) ATR-FTIR spectra. We found that most of the carboxylate groups perturbed during the S(1) --> S(2) transition, due to direct ligation to the Mn cluster or though a hydrogen bond network, have orientations in a relatively narrow angle range of 34-48 degrees with respect to the membrane normal. Implications of the obtained orientations and the changes upon formation of S(2) are discussed on the basis of the information from previous FTIR studies and the X-ray structures. The results in this study show that polarized ATR-FTIR difference spectroscopy is a fruitful method for investigating the orientations and their reaction-induced changes in redox cofactors and coupled amino acid side chains in photosynthetic proteins.

Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution

The molecular mechanism of photosynthetic oxygen evolution remains a mystery in photosynthesis research. Although recent X-ray crystallographic studies of the photosystem II core complex at 3.0-3.5 A resolutions have revealed the structure of the oxygen-evolving center (OEC), with approximate positions of the Mn and Ca ions and the amino acid ligands, elucidation of its detailed structure and the reactions during the S-state cycle awaits further spectroscopic investigations. Light-induced Fourier transform infrared (FTIR) difference spectroscopy was first applied to the OEC in 1992 as detection of its structural changes upon the S(1)-->S(2) transition, and spectra during the S-state cycle induced by consecutive flashes were reported in 2001. These FTIR spectra provide extensive structural information on the amino acid side groups, polypeptide chains, metal core, and water molecules, which constitute the OEC and are involved in its reaction. FTIR spectroscopy is thus becoming a powerful tool in investigating the reaction mechanism of photosynthetic oxygen evolution. In this mini-review, the measurement method of light-induced FTIR spectra of OEC is introduced and the results obtained thus far using this technique are summarized.

Consequences of structural and biophysical studies for the molecular mechanism of photosynthetic oxygen evolution: functional roles for calcium and bicarbonate

Possible chemical mechanisms for catalyzing O2 evolution from water in natural photosynthesis are summarized, based on the atomic and electronic structures of the inorganic core as revealed by spectroscopic and X-ray diffraction experiments and insights gained from inorganic complexes that achieve O–O bond formation. The thermodynamic and kinetic requirements for this multi-step reaction are reexamined, including the coupling of the individual electron-proton steps (PCET) and the O–O bond formation step. The four oxygen atoms at the corners of the proposed hetero-cubical Mn3CaO4 core (3 μ3-oxos and one μ4-oxo) can be distinguished by the number and types of chemical bonds to Ca2+ and Mn (geometries and orbital hybridization). Two of these μ3-oxos, postulated as substrates, are located at unique sites indicative of sp2 + pπ hybridized orbitals. Both proposed substrate oxos are strongly hydrogen-bonded to different protein carboxylate residues, which are postulated as the initial proton transfer sites. Ca2+ is weakly bonded to these substrate oxos via non-directional ionic bonds that are postulated to provide stereochemical flexibility for the homolytic formation of the O–O bond. A previously postulated heterolytic pathway involving an electrophilic oxo and nucleophilic hydroxide species is reevaluated. We extend this mechanism by postulating roles for (bi)carbonate either in proton transfer or delivering the nucleophile for O2 formation.

Apparatus and mechanism of photosynthetic oxygen evolution: a personal perspective.

This historical minireview describes basic lines of progress in our understanding of the functional pattern of photosynthetic water oxidation and the structure of the Photosystem II core complex. After a short introduction into the state of the art about 35 years ago, results are reviewed that led to identification of the essential cofactors of this process and the kinetics of their reactions. Special emphasis is paid on the flash induced oxygen measurements performed by Pierre Joliot (in Paris, France) and Bessel Kok (Baltimore, MD) and their coworkers that led to the scheme, known as the Kok-cycle. These findings not only unraveled the reaction pattern of oxidation steps leading from water to molecular oxygen but also provided the essential fingerprint as prerequisite for studying individual redox reactions. Starting with the S. Singer and G. Nicolson model of membrane organization, attempts were made to gain information on the structure of the Photsystem II complex that eventually led to the current stage of knowledge based on the recently published X-ray crystal structure of 3.8 A resolution in Berlin (Germany).With respect to the mechanism of water oxidation, the impact of Gerald T. Babcock's hydrogen abstractor model and all the considerations of electron/proton transfer coupling are outlined. According to my own model cosiderations, the protein matrix is not only a 'cofactor holder' but actively participates by fine tuning via hydrogen bond networks, playing most likely an essential role in water substrate coordination and in oxygen-oxygen bond formation as the key step of the overall process.

New structure model of oxygen-evolving center and mechanism for oxygen evolution in photosynthesis

So far, many important questions and problems concerning the structure and mechanism of photosynthetic oxygen evolution are still unsolved. On the basis of recent achievements in this field, a new structure model is proposed whereby two H2O molecules bind asymmetrically to two manganese ions (Mn 1 II and Mn 4 III ) at the open end of “C” shaped cluster and keep rather large distance. Two histidine residues coordinate to the other two manganese ions in higher oxidation state (Mn 2 IV and Mn 3 IV ) through their nitrogen atoms of the imidazole. CI bound as terminal ligand to Mn 4 III is connected to Ca, and the latter is needed to maintain the special configuration of two Mn2O2 units by bridged-oxo and bridged-carboxylate ligands. The whole structure of oxygen evolution center is asymmetry. A new mechanism for oxygen evolution invokes predictions of asymmetric oxidation of two H2O molecules, dynamic structural changes of oxygen evolving center and indirect proton transport, etc. Only in S2 state, could Mn 1 IV = O, intermediate with high oxidation potential be formed. The S2→ S3 process occurs with significant structural changes, as well as intramolecular and intermolecular hydrogen transfer. The S3 state corresponds to intermediate of Mn 1 IV -O … H … O-Mn 4 IV . During S3 → [S4] → S0, the 0-0 bond is formed only in S4 state. The change of nucleophilic interaction between Cl and manganese ions different oxidation states has consequence for the significant structural changes in H2O oxidation process.

Molecular mechanism of photosynthetic oxygen evolution. A theoretical approach

Possible mechanisms for O2 evolution in photosystem I1 (PSII) are studied with a semiempirical one-electron molecular orbital procedure, the extended Hiickel method. The oxygen coupling is examined starting from some known inorganic complexes of manganese. Idealized geometries of four binuclear complexes (two di-p-oxo, one tri-p-oxo and one p-carboxylato-di-1-oxo) are distorted to transform into Oz-bound complexes. The computed Walsh diagrams are analyzed. For these structures the predicted oxidation to dioxygen is energetically unfavorable and would require two two-electron steps forming bound peroxide as an intermediate. An in-plane approach of two oxo ligands has a lower barrier for peroxide bond formation. Four tetranuclear Mn clusters are built combining binuclear complexes, a Mn404 cubane-like core, three (Mn202),(p-02) dimer of dimers cores with p4,t2-02 bound either in or out of the Mn4 plane formed by two parallel Mn202 units, and a planar T combination of two orthogonal MnzO2 units with a Mn3O2 core and p3,q2-O2 bound to three Mn atoms. The assumed pathway leading to peroxide bond formation in each of these is found to have appreciably lower energy for the (Mn202),(p-02) and the planar T models with in-plane 0-0 approach. A slight energetic advantage is calculated in the peroxide to dioxygen step when the oxo ligands are coordinated to at least three Mn ions compared to coordination to only two Mn ions. Qualitative valence bond analysis indicates that release of symmetrically coordinated dioxygen, as in cis- and trans-p-02, requires overcoming an -1-eV electronic barrier for formation of ground-state O2 (triplet). The tetranuclear models are introduced into speculative mechanisms and compared with current knowledge of the photosynthetic water oxidation reaction.

A model for the molecular mechanism of photosynthetic oxygen evolution

A model for the molecular mechanism of photosynthetic oxygen evolution

Sulfolipid Metabolism in Chlorella

When S-deficient cells of Chlorella cllipsoidea were incubated in radio-sulfate in light or in aerobic darkness for 1 hour, equal amounts of radioactivity were found in sulfolipid and glutathione but none was detected in sulfoquinovosyl glycerol which is one of the major S-compounds in this alga. No assimilation of radiosulfate was observed under anaerobic darkness.To elucidate the function of sulfolipid in algal cells uniformly (35)S-labeled Chlorella cells were transferred to S-deficient culture medium or unlabeled normal culture medium and the changes of radioactivity in sulfolipid and the related compounds were followed. A) On incubating (35)S-labeled algal cells in S-deficient medium under photosynthetic conditions, the amounts of radioactivity in sulfate, sulfoquinovosyl glycerol and sulfolipid decreased rapidly. B) When (35)S-labeled cells were cultured photoautotrophically in unlabeled medium, no decrease of radioactivity was observed in sulfoquinovosyl glycerol and sulfolipid. C) A decrease of (35)S-sulfolipid and an increase of (35)S-sulfoquinovosyl glycerol were observed when the uniformly (35)S-labeled algal cells were illuminated in CO(2)-free air.When S-deficient Chlorella cells were incubated in (35)S-sulfolipid under photosynthetic conditions, significant radioactivity was found in the insoluble fraction of the cells. A similar result was observed when normal Chlorella cells were incubated in (14)C-sulfolipid and CO(2)-free air.It is inferred from these observations that sulfolipid is a reservoir of sulfur and carbon compounds.In order to ascertain if the sulfolipid is involved in the mechanism of photosynthetic oxygen evolution, the rate of photosynthesis was measured during the incubation of (35)S-labeled cells in a S-deficient medium. Parallelism was not observed between the rate of photosynthetic activity and the decrease of sulfolipid.