Magnetic and Electronic Structural Properties of the S₃ State of Nature’s Water Oxidizing Complex: A Combined Study in ELDOR-Detected Nuclear Magnetic Resonance Spectral Simulation and Broken-Symmetry Density Functional Theory

Abstract

ELDOR-detected nuclear magnetic resonance (EDNMR) spectral simulations combined with broken-symmetry density functional theory (BS-DFT) calculations are used to obtain and to assign the 55 Mn hyperfine coupling constants (hfcs) for modified forms of the water oxidizing complex in the penultimate S 3 state of the water oxidation cycle. The study shows that an open cubane form of the core Mn 4 CaO 6 cluster explains the magnetic properties of the dominant S = 3 species in all cases studied experimentally with no need to invoke a closed cubane intermediate possessing a distorted pentacoordinate Mn 4 ion as recently suggested. EDNMR simulations found that both the experimental bandwidth and multinuclear transitions may alter relative EDNMR peak intensities, potentially leading to incorrect assignment of hfcs. The implications of these findings for the water oxidation mechanism are discussed.

Is There a Different Mechanism for Water Oxidation in Higher Plants?

“…Another recent EPR analysis has instead concluded that S 3 has an open cubane structure. 24 Other S = 6 structures than the one found by Pantazis et al could, for example, be obtained by simply reversing the signs of the spins on some Mn(IV) centers and keep the open cubane. That should only marginally affect the energies and, therefore, not be important for the oxyl–oxo mechanism.…”

“…With the accuracy typical for the methods used here of about 3 kcal/mol, the closed cubane structure must, therefore, be ruled out as a possible S 3 state. Another recent EPR analysis has instead concluded that S 3 has an open cubane structure . Other S = 6 structures than the one found by Pantazis et al could, for example, be obtained by simply reversing the signs of the spins on some Mn­(IV) centers and keep the open cubane.…”

“…In a recent study by O’Malley and co-workers, the EPR analysis of S 3 as a closed cubane was also strongly criticized. In their new EPR analysis, an open cubane structure was instead clearly favored . An open cubane suggestion for the S = 6 state will be given below.…”

“…In their new EPR analysis, an open cubane structure was instead clearly favored. 24 An open cubane suggestion for the S = 6 state will be given below. For blue-green algae, X-FEL studies have identified S 3 as an open cubane, 3 , 4 in very close agreement with previous quantum calculations.…”