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 ⁵⁵Mn hyperfine coupling constants (hfcs) for modified forms of the water oxidizing complex in the penultimate S₃ state of the water oxidation cycle. The study shows that an open cubane form of the core Mn₄CaO₆ 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 Mn₄ 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.

Figure 1

Water oxidizing complex (WOC) S state cycle. The four Mn ions of the complex are progressively oxidized with each photon flash (1F, 2F, 3F, 4F).

Figure 2

Numbering scheme and orientation used throughout for the S₃ state core WOC. Color coding: Mn (purple), oxygen (red), and calcium (cream).

Figure 3

Experimental EDNMR spectra of the methanol-treated PSII reproduced from ref (17) (black); simulated EDNMR spectra summed from simulations with a single ⁵⁵Mn nucleus using the hfcs from Table 2 for closed cubane (blue) and open cubane (red) structures. ¹H resonances are denoted with asterisks and occur around the proton Larmor frequency. The bottom comparison illustrates spectral overlay for 4.4 T simulation to emphasize fit. All simulated data have been multiplied by a Lorentzian function with an FWHM of 400 MHz to mimic the resonator background.

Figure 4

Experimental EDNMR spectra of the methanol-treated PSII reproduced from ref (17) (black); simulated EDNMR spectra summed from simulations with pairs of ⁵⁵Mn nuclei using the hfcs from Table 2 in the main paper for closed cubane (blue) and open cubane (red) structures, calculated at both low and high field positions with an HTA pulse amplitude of 4.7 × 10⁶ (top) and 4.7 × 10⁷ (bottom) rad s^–1. ¹H resonances occur around the proton Larmor frequency as shown in Figure 3; 4.4 T simulations are overlaid to emphasize fit. All simulated data have been multiplied by a Lorentzian function with an FWHM of 400 MHz to mimic the resonator background.