Do crystallographic XFEL data support binding of a water molecule to the oxygen-evolving complex of photosystem II exposed to two flashes of light?
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ABSTRACT:
SUBMITTER: Wang J
PROVIDER: S-EPMC8214663 | biostudies-literature | 2021 Jun
REPOSITORIES: biostudies-literature
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Do crystallographic XFEL data support binding of a water molecule to the oxygen-evolving complex of photosystem II exposed to two flashes of light?
Wang Jimin J Armstrong William H WH Batista Victor S VS
Proceedings of the National Academy of Sciences of the United States of America 20210601 24
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Project description:Structural changes induced by radiation damage in X-ray crystallography hinder the ability to understand the structure/function relationship in chemical reactions. Serial femtosecond crystallography overcomes this problem by exposing the sample to very short and intense laser pulse leading to measurement before destruction. Here we use molecular modeling to map the radiation damage during the 10-50 fs to the intensity, the energy and the time duration of the laser pulse on the oxygen-evolving complex (OEC) of photosystem II. In the model, the nuclei move classically in a fully quantum potential created by electron density under the effect of strong laser pulse in the Ehrenfest dynamics regime. The results show that the Mn-Mn and Mn-Ca distances are less affected by radiation damage due to the their heavy masses, while one μ-oxo bridge (O5) moves significantly. The radiation damage may induce conformational changes of the water ligands but only bond elongation for the amino acids ligands. These effects are relatively intensity independent from 1016 to 1017 W/cm2, but changes increase dramatically if the beam intensity is increased to 1018 W/cm2. In addition, the self amplified spontaneous emission (SASE) nature of the laser beam does not affect the dynamics of the ions.
| S-EPMC5101503 | biostudies-literature
Project description:Photosystem II (PSII) oxidizes water to produce oxygen through a four-step photocatalytic cycle. Understanding PSII structure-function relations is important for the development of biomimetic photocatalytic systems. The quantum mechanics/molecular mechanics (QM/MM) analysis of substrate water binding to the oxygen-evolving complex (OEC) has suggested a rearrangement of water ligands in a carousel mechanism around a key Mn center. Here, we find that the most recently reported X-ray free-electron laser (XFEL) crystallographic data obtained for the dark-stable S1 state and the doubly flashed S3 state at 2.25 Å resolution support the carousel mechanism. The features in the XFEL data and QM/MM model-simulated difference Fourier maps suggest that water displacement may occur from the so-called "narrow" channel, resulting in binding of a new water molecule to the OEC, and thus provide new insights into the nature of rearrangements of water ligands along the catalytic cycle before O=O bond formation.
| S-EPMC5644713 | biostudies-literature
Project description:Light damages photosynthetic machinery, primarily photosystem II (PSII), and it results in photoinhibition. A new photodamage model, the two-step photodamage model, suggests that photodamage to PSII initially occurs at the oxygen evolving complex (OEC) by light energy absorbed by manganese and that the PSII reaction center is subsequently damaged by light energy absorbed by photosynthetic pigments due to the limitation of electrons to the PSII reaction center. However, it is still uncertain whether this model is applicable to photodamage to PSII under visible light as manganese absorbs visible light only weakly. In the present study, we identified the initial site of photodamage to PSII upon illumination of visible light using PSII membrane fragments isolated from spinach leaves. When PSII samples were exposed to visible light in the presence of an exogenous electron acceptor, both PSII total activity and the PSII reaction centre activity declined due to photodamage. The supplemental addition of an electron donor to the PSII reaction centre alleviated the decline of the reaction centre activity but not the PSII total activity upon the light exposure. Our results demonstrate that visible light damages OEC prior to photodamage to the PSII reaction center, consistent with two-step photodamage model.
| S-EPMC4642293 | biostudies-literature
Project description:Photodamage to Photosystem II (PSII) has been attributed either to excessive excitation of photosynthetic pigments or by direct of light absorption by Mn4CaO5 cluster. Here we investigated the time course of PSII photodamage and release of Mn in PSII-enriched membranes under high light illumination at 460 nm and 660 nm. We found that the loss of PSII activity, assayed by chlorophyll fluorescence, is faster than release of Mn from the Mn4CaO5 cluster, assayed by EPR. Loss of PSII activity and Mn release was slower during illumination in the presence of exogenous electron acceptors. Recovery of PSII activity was observed, after 30 min of addition of electron donor post illumination. The same behavior was observed under 460 and 660 nm illumination, suggesting stronger correlation between excessive excitation and photodamage compared to direct light absorption by the cluster. A unified model of PSII photodamage that takes into account present and previous literature reports is presented.
| S-EPMC5548768 | biostudies-literature
Project description:Singlet oxygen (1 O2 ) is a harmful species that functions also as a signaling molecule. In chloroplasts, 1 O2 is produced via charge recombination reactions in photosystem II, but which recombination pathway(s) produce triplet Chl and 1 O2 remains open. Furthermore, the role of 1 O2 in photoinhibition is not clear. We compared temperature dependences of 1 O2 production, photoinhibition, and recombination pathways. 1 O2 production by pumpkin thylakoids increased from -2 to +35°C, ruling out recombination of the primary charge pair as a main contributor. S2 QA - or S2 QB - recombination pathways, in turn, had too steep temperature dependences. Instead, the temperature dependence of 1 O2 production matched that of misses (failures of the oxygen (O2 ) evolving complex to advance an S-state). Photoinhibition in vitro and in vivo (also in Synechocystis), and in the presence or absence of O2 , had the same temperature dependence, but ultraviolet (UV)-radiation-caused photoinhibition showed a weaker temperature response. We suggest that the miss-associated recombination of P680 + QA - is the main producer of 1 O2 . Our results indicate three parallel photoinhibition mechanisms. The manganese mechanism dominates in UV radiation but also functions in white light. Mechanisms that depend on light absorption by Chls, having 1 O2 or long-lived P680 + as damaging agents, dominate in red light.
| S-EPMC10092662 | biostudies-literature
Project description:Photosystem II (PSII), which catalyzes photosynthetic water oxidation, is composed of more than 20 subunits, including membrane-intrinsic and -extrinsic proteins. The PSII extrinsic proteins shield the catalytic Mn4CaO5 cluster from the outside bulk solution and enhance binding of inorganic cofactors, such as Ca(2+) and Cl(-), in the oxygen-evolving center (OEC) of PSII. Among PSII extrinsic proteins, PsbO is commonly found in all oxygenic organisms, while PsbP and PsbQ are specific to higher plants and green algae, and PsbU, PsbV, CyanoQ, and CyanoP exist in cyanobacteria. In addition, red algae and diatoms have unique PSII extrinsic proteins, such as PsbQ' and Psb31, suggesting functional divergence during evolution. Recent studies with reconstitution experiments combined with Fourier transform infrared spectroscopy have revealed how the individual PSII extrinsic proteins affect the structure and function of the OEC in different organisms. In this review, we summarize our recent results and discuss changes that have occurred in the structural coupling of extrinsic proteins with the OEC during evolutionary history.
| S-EPMC4743485 | biostudies-literature
Project description:Photosystem II (PSII) is a multisubunit membrane protein complex performing light-induced electron transfer and water-splitting reactions, leading to the formation of molecular oxygen. The first crystal structure of PSII from a thermophilic cyanobacterium Thermosynechococcus elongatus was reported recently [Zouni, A., Witt, H. T., Kern, J., Fromme, P., Krauss, N., Saenger, W. & Orth, P. (2001) Nature 409, 739-743)] at 3.8-A resolution. To analyze the PSII structure in more detail, we have obtained the crystal structure of PSII from another thermophilic cyanobacterium, Thermosynechococcus vulcanus, at 3.7-A resolution. The present structure was built on the basis of the sequences of PSII large subunits D1, D2, CP47, and CP43; extrinsic 33- and 12-kDa proteins and cytochrome c550; and several low molecular mass subunits, among which the structure of the 12-kDa protein was not reported previously. This yielded much information concerning the molecular interactions within this large protein complex. We also show the arrangement of chlorophylls and cofactors, including two beta-carotenes recently identified in a region close to the reaction center, which provided important clues to the secondary electron transfer pathways around the reaction center. Furthermore, possible ligands for the Mn-cluster were determined. In particular, the C terminus of D1 polypeptide was shown to be connected to the Mn cluster directly. The structural information obtained here provides important insights into the mechanism of PSII reactions.
| S-EPMC140893 | biostudies-literature
Project description:Photosystem II (PS II) is unique among photosynthetic reaction centers in having secondary electron donors that compete with the primary electron donors for reduction of P680(+). We have characterized the photooxidation and dark decay of the redox-active accessory chlorophylls (Chl) and beta-carotenes (Car) in oxygen-evolving PS II core complexes by near-IR absorbance and EPR spectroscopies at cryogenic temperatures. In contrast to previous results for Mn-depleted PS II, multiple near-IR absorption bands are resolved in the light-minus-dark difference spectra of oxygen-evolving PS II core complexes including two fast-decaying bands at 793 and 814 nm and three slow-decaying bands at 810, 825, and 840 nm. We assign these bands to chlorophyll cation radicals (Chl(+)). The fast-decaying bands observed after illumination at 20 K could be generated again by reilluminating the sample. Quantization by EPR gives a yield of 0.85 radicals per PS II, and the yield of oxidized cytochrome b 559 by optical difference spectroscopy is 0.15 per PS II. Potential locations of Chl(+) and Car(+) species, and the pathways of secondary electron transfer based on the rates of their formation and decay, are discussed. This is the first evidence that Chls in the light-harvesting proteins CP43 and CP47 are oxidized by P680(+) and may have a role in Chl fluorescence quenching. We also suggest that a possible role for negatively charged lipids (phosphatidyldiacylglycerol and sulfoquinovosyldiacylglycerol identified in the PS II structure) could be to decrease the redox potential of specific Chl and Car cofactors. These results provide new insight into the alternate electron-donation pathways to P680(+).
| S-EPMC2674297 | biostudies-literature
Project description:The identity and insertion pathway of the substrate oxygen atoms that are coupled to dioxygen by the oxygen-evolving complex (OEC) remains a central question toward understanding Nature's water oxidation mechanism. In several studies, ammonia has been used as a small "water analogue" to elucidate the pathway of substrate access to the OEC and to aid in determining which of the oxygen ligands of the tetramanganese cluster are substrates for O-O bond formation. On the basis of structural and spectroscopic investigations, five first-sphere binding modes of ammonia have been suggested, involving either substitution of an existing H2O/OH-/O2- group or addition as an extra ligand to a metal ion of the Mn4CaO5 cluster. Some of these modes, specifically the ones involving substitution, have already been subject to spectroscopy-oriented quantum chemical investigations, whereas more recent suggestions that postulate the addition of ammonia have not been examined so far with quantum chemistry for their agreement with spectroscopic data. Herein, we use a common structural framework and theoretical methodology to evaluate structural models of the OEC that represent all proposed modes of first-sphere ammonia interaction with the OEC in its S2 state. Criteria include energetic, magnetic, kinetic, and spectroscopic properties compared against available experimental EPR, ENDOR, ESEEM, and EDNMR data. Our results show that models featuring ammonia replacing one of the two terminal water ligands on Mn4 align best with experimental data, while they definitively exclude substitution of a bridging μ-oxo ligand as well as incorporation of ammonia as a sixth ligand on Mn1 or Mn4.
| S-EPMC10875651 | biostudies-literature
Project description:The structural and electronic properties of a series of manganese complexes with terminal oxido ligands are described. The complexes span three different oxidation states at the manganese center (III-V), have similar molecular structures, and contain intramolecular hydrogen-bonding networks surrounding the Mn-oxo unit. Structural studies using X-ray absorption methods indicated that each complex is mononuclear and that oxidation occurs at the manganese centers, which is also supported by electron paramagnetic resonance (EPR) studies. This gives a high-spin Mn(V)-oxo complex and not a Mn(IV)-oxy radical as the most oxidized species. In addition, the EPR findings demonstrated that the Fermi contact term could experimentally substantiate the oxidation states at the manganese centers and the covalency in the metal-ligand bonding. Oxygen-17-labeled samples were used to determine spin density within the Mn-oxo unit, with the greatest delocalization occurring within the Mn(V)-oxo species (0.45 spins on the oxido ligand). The experimental results coupled with density functional theory studies show a large amount of covalency within the Mn-oxo bonds. Finally, these results are examined within the context of possible mechanisms associated with photosynthetic water oxidation; specifically, the possible identity of the proposed high valent Mn-oxo species that is postulated to form during turnover is discussed.
| S-EPMC4418911 | biostudies-literature