Rationalizing the Geometries of the Water Oxidising Complex in the Atomic Resolution, Nominal S State Crystal Structures of Photosystem II.

Three atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S intermediate state of its Mn Ca Water Oxidising Complex (WOC), have now been presented, at 2.25, 2.35 and 2.

Explaining the Different Geometries of the Water Oxidising Complex in the Nominal S State Crystal Structures of Photosystem II at 2.25 Å and 2.35 Å.

Recently two atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S intermediate state of its Mn Ca water oxidising complex (WOC), have been presented (Young et al., Nature 2016, 540, 453; Suga et al., Nature 2017, 543, 131).

What Mn K spectroscopy reveals concerning the oxidation states of the Mn cluster in photosystem II.

The oxygen evolving complex, (OEC) in Photosystem II contains a MnCa cluster and catalyses oxidation of water to molecular oxygen and protons, the most energetically demanding reaction in nature. The catalytic mechanism remains unresolved and the precise Mn oxidation levels through which the cluster cycles during functional turnover are controversial. Two proposals for these redox levels exist; the 'high' and 'low' oxidation state paradigms, which differ systematically by two oxidation equivalents throughout the redox accumulating catalytic S state cycle (states S…S).

Rationalizing the 2.25 Å Resolution Crystal Structure of the Water Oxidising Complex of Photosystem II in the S State.

Quantum chemical calculations are described which rationalize the recent X-ray diffraction (XRD) structure at 2.25 Å of the Mn Ca water oxidising complex (WOC) of photosystem II (PSII) in the S intermediate state. The new S XRD structure shows remarkable similarity to earlier atomic resolution (1.

What computational chemistry and magnetic resonance reveal concerning the oxygen evolving centre in Photosystem II.

Density Functional Theory (DFT) computational studies of the Mn/Ca Oxygen Evolving Complex (OEC) region of Photosystem II in the paramagnetic S and S states of the water oxdizing catalytic cycle are described. These build upon recent advances in computationally understanding the detailed S state OEC geometries, revealed by the recent high resolution Photosystem II crystal structures of Shen et al., at 1.

Deprotonation of Water/Hydroxo Ligands in Clusters Mimicking the Water Oxidizing Complex of PSII and Its Effect on the Vibrational Frequencies of Ligated Carboxylate Groups.

The IR absorptions of several first-shell carboxylate ligands of the water oxidizing complex (WOC) have been experimentally shown to be unaffected by oxidation state changes in the WOC during its catalytic cycle. Several model clusters that mimic the Mn4O5Ca core of the WOC in the S1 state, with electronic configurations that correspond to both the so-called "high" and "low" oxidation paradigms, were investigated. Deprotonation at W2, W1, or O3 sites was found to strongly reduce carboxylate ligand frequency shifts on oxidation of the metal cluster.

Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water-Oxidizing Complex.

Great progress has been made in characterizing the water-oxidizing complex (WOC) in photosystem II (PSII) with the publication of a 1.9 Å resolution X-ray diffraction (XRD) and recently a 1.95 Å X-ray free-electron laser (XFEL) structure.

Rationalising the geometric variation between the A and B monomers in the 1.9 Å crystal structure of photosystem II.

Density functional theory calculations are reported on a set of models of the water-oxidising complex (WOC) of photosystem II (PSII), exploring structural features revealed in the most recent (1.9 Å resolution) X-ray crystallographic studies of PSII. Crucially, we find that the variation in the Mn-Mn distances seen between the A and B monomers of this crystal structure can be entirely accounted for, in the low oxidation state (LOS) paradigm, by consideration of the interplay between two hydrogen-bonding interactions involving proximate amino acid residues with the oxo bridges of the WOC, that is, His337 with O3 (which leads to a general elongation in the Mn-Mn distances between Mn1, Mn2 and Mn3) and Arg357 with O2 (which results in a specific elongation of the Mn2-Mn3 distance).

Electronic structure of the oxygen evolving complex in photosystem II, as revealed by 55Mn Davies ENDOR studies at 2.5 K.

We report the first (55)Mn pulsed ENDOR studies on the S2 state multiline spin ½ centre of the oxygen evolving complex (OEC) in Photosystem II (PS II), at temperatures below 4.2 K. These were performed on highly active samples of spinach PS II core complexes, developed previously in our laboratories for photosystem spectroscopic use, at temperatures down to 2.

Ab Initio modeling of the effect of oxidation coupled with HnO deprotonation on carboxylate ligands in Mn/Ca clusters.

Oxidation of some manganese complexes containing both carboxylate and water/hydroxo ligands does not result in changes to the carboxylate stretching frequencies. The water oxidizing complex of photosystem II is one motivating example. On the basis of electronic structure theory calculations, we here suggest that the deprotonation of water or hydroxo ligands minimizes changes in the vibrational frequencies of coligating carboxylates, rendering the carboxylate modes "invisible" in FTIR difference spectroscopy.

What does the Sr-substituted 2.1 Å resolution crystal structure of photosystem II reveal about the water oxidation mechanism?

A density functional study of the Sr-substituted photosystem II water oxidising complex demonstrates that its recent X-ray crystal structure is consistent with a (Mn(III))4 oxidation state pattern, and with a Sr-bound hydroxide ion. The Sr-water-hydroxide interactions rationalize differences in the exchange rates of substrate water and kinetics of dioxygen bond formation relative to the Ca-containing structure.

Computational design of a carbon nanotube fluorofullerene biosensor.

Carbon nanotubes offer exciting opportunities for devising highly-sensitive detectors of specific molecules in biology and the environment. Detection limits as low as 10(-11) M have already been achieved using nanotube-based sensors. We propose the design of a biosensor comprised of functionalized carbon nanotube pores embedded in a silicon-nitride or other membrane, fluorofullerene-Fragment antigen-binding (Fab fragment) conjugates, and polymer beads with complementary Fab fragments.

What spectroscopy reveals concerning the Mn oxidation levels in the oxygen evolving complex of photosystem II: X-ray to near infra-red.

Photosystem II (PS II), found in oxygenic photosynthetic organisms, catalyses the most energetically demanding reaction in nature, the oxidation of water to molecular oxygen and protons. The water oxidase in PS II contains a Mn(4)Ca cluster (oxygen evolving complex, OEC), whose catalytic mechanism has been extensively investigated but is still unresolved. In particular the precise Mn oxidation levels through which the cluster cycles during functional turnover are still contentious.

What are the oxidation states of manganese required to catalyze photosynthetic water oxidation?

Photosynthetic O(2) production from water is catalyzed by a cluster of four manganese ions and a tyrosine residue that comprise the redox-active components of the water-oxidizing complex (WOC) of photosystem II (PSII) in all known oxygenic phototrophs. Knowledge of the oxidation states is indispensable for understanding the fundamental principles of catalysis by PSII and the catalytic mechanism of the WOC. Previous spectroscopic studies and redox titrations predicted the net oxidation state of the S(0) state to be (Mn(III))(3)Mn(IV).

Modelling the metal atom positions of the Photosystem II water oxidising complex: a density functional theory appraisal of the 1.9 Å resolution crystal structure.

Density functional theory (DFT) calculations are reported for a set of model compounds intended to represent the structure of the Photosystem II (PSII) water oxidising complex (WOC) as determined by the recent 1.9 Å resolution single crystal X-ray diffraction (XRD) study of Umena et al. In contrast with several other theoretical studies addressing this structure, we find that it is not necessary to invoke photoreduction of the crystalline sample below the S(1)'resting state' in order to rationalise the observed WOC geometry.

Why nature chose Mn for the water oxidase in Photosystem II.

Nature performs a vital but uniquely energetic reaction within Photosystem II (PS II), resulting in the oxidation of two water molecules to yield O(2) and bio-energetic electrons, as reducing equivalents. Almost all life on earth ultimately depends on this chemistry, which occurs with remarkable efficiency within a tetramanganese and calcium cluster in the photosystem. The thermodynamic constraints for the operation of this water oxidising Mn(4)/Ca cluster within PS II are discussed.

The interaction of His337 with the Mn4Ca cluster of photosystem II.

The most recent XRD studies of Photosystem II (PS II) reveal that the His337 residue is sufficiently close to the Mn(4)Ca core of the Water Oxidising Complex (WOC) to engage in H-bonding interactions with the μ(3)-oxo bridge connecting Mn(1), Mn(2) and Mn(3). Such interactions may account for the lengthening of the Mn-Mn distances observed in the most recent and highest resolution (1.9 Å) crystal structure of PS II compared to earlier, lower-resolution (2.

Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II--a review.

Applications of Density Functional Theory (DFT) computational techniques to studies of the molecular structure and mechanism of the oxygen evolving, water oxidising Mn(4)/Ca catalytic site in Photosystem II are reviewed. We summarise results from the earlier studies (pre 2000) but concentrate mainly on those developments which have occurred since publication of several PS II crystal structures of progressively increasing resolution, starting in 2003. The work of all computational groups actively involved in PS II studies is examined, in the light of direct PS II structural information from X-ray diffraction crystallography and EXAFS on the metals in the catalytic site.

Hydration preferences for Mn4Ca cluster models of photosystem II: location of potential substrate-water binding sites.

Density functional theory calculations are reported on a set of three model structures of the Mn(4)Ca cluster in the water-oxidizing complex of Photosystem II (PSII), which share the structural formula [CaMn(4)C(9)H(10)N(2)O(16)](q+)·(H(2)O)(n) (q=-1, 0, 1, 2, 3; n=0-7). In these calculations we have explored the preferred hydration sites of the Mn(4)Ca cluster across five overall oxidation states (S(0) to S(4)) and all feasible magnetic-coupling arrangements to identify the most likely substrate-water binding sites. We have also explored charge-compensated structures in which the overall charge on the cluster is maintained at q=0 or +1, which is consistent with the experimental data on sequential proton loss in the real system.

Identification of the QY excitation of the primary electron acceptor of photosystem II: CD determination of its coupling environment.

Low-temperature absorption and CD spectra, measured simultaneously, are reported from Photosystem II (PS II) reduced with sodium dithionite. Spectra were obtained using PS II core complexes before and after photoaccumulation of Pheo(D1)(-), the anion of the primary acceptor. For plant PS II, Pheo(D1)(-) was generated under conditions in which the primary plastoquinone was present as an anion (Q(A)(-)) and as a modified species taken to be the neutral doubly reduced hydroquinone (Q(A)H(2)).

The S(1) split signal of photosystem II; a tyrosine-manganese coupled interaction.

Detailed optical and EPR analyses of states induced in dark-adapted PS II membranes by cryogenic illumination permit characterization and quantification of all pigment derived donors and acceptors, as well as optically silent (in the visible, near infrared) species which are EPR active. Near complete turnover formation of Q(A)((-)) is seen in all centers, but with variable efficiency, depending on the donor species. In minimally detergent-exposed PS II membranes, negligible (<5%) oxidation of chlorophyll or carotenoid centers occurs for illumination temperatures 5-20 K.

Structural, magnetic coupling and oxidation state trends in models of the CaMn4 cluster in photosystem II.

Density functional theory calculations are reported on a set of isomeric structures I, II and III that share the structural formula [CaMn4C9H10N2O16]q+.(H2O)3 (q= -1, 0, 1, 2, 3). Species I has a skeletal structure, which has been previously identified as a close match to the ligated CaMn4 cluster in Photosystem II, as characterized in the most recent 3.

Bridge over troubled water: resolving the competing photosystem II crystal structures.

Density functional theory (DFT) calculations, at the Becke-Perdew/TZP level of theory, were used to investigate a set of CaMn(4)-containing clusters that model the active site of the water-oxidizing complex (WOC) of photosystem II (PSII). Metal-atom positions for three representative isomeric clusters of the formula [CaMn(4)C(9)N(2)O(16)H(10)](+)4 H(2)O are in good agreement with the disparate Mn(4) geometries of the three most recent X-ray crystal structures. Remarkably, interconversion between these three isomeric clusters is found to be facile, resulting from subtle changes in the coordination environment around the CaMn(4) centre.