ESE-ENDOR and ESEEM Characterization of Water and Methanol Ligation to a Dinuclear Mn(III)Mn(IV) Complex

Abstract

Interactions of water and methanol with a mixed valence Mn(III)Mn(IV) complex are explored with 1H electron spin echo (ESE)-electron nuclear double resonance (ENDOR) and 1H and 2H ESE envelope modulation (ESEEM). Derivatives of the (2-OH-3,5-Cl2-SALPN)2 Mn(III)Mn(IV) complex are ideal for structural and spectroscopic modeling of water binding to multinuclear Mn complexes in metalloproteins, specifically photosystem II (PSII) and manganese catalase (MnCat). Using ESE-ENDOR and ESEEM techniques, 1H hyperfine parameters are determined for both water and methanol ligated to the Mn(III) ion of the complex. The protons of water directly bound to Mn(III) are inequivalent and exhibit roughly axial dipolar hyperfine interactions (T dip = 8.4 MHz and T dip = 7.4 MHz), permitting orientations and radial distances to be determined using a model where the proton experiences a point dipole interaction with each Mn ion. General equations are given for the components of the rhombic dipolar hyperfine interaction between a proton and a spin coupled dinuclear metal cluster. The observed ENDOR pattern is from water protons 2.65 and 2.74 Å from the Mn(III) which make an Mn(IV)−Mn(III)−H angle of ∼160°. For the alcohol proton in the analogous methanol bound complex, a 2.65 Å Mn(III)−H distance is observed. Three pulse 2H ESEEM gives best fit Mn(III)−2H(1H) radial distances of 3.0, 3.5, and 4.0 Å for the three methyl deuterons in this complex.

Simulations of the 1 H electron spin echo–electron nuclear double resonance and 2 H electron spin echo envelope modulation spectra of exchangeable hydrogen nuclei coupled to the S 2 –state photosystem II manganese cluster

“…One interesting substrate water binding possibility arises from an examination of the hyperfine couplings in table 1. The class described in the first row, with the largest dipolar coupling and the shortest dipolar distance (2.59 Å ), also has an appreciable isotropic hyperfine coupling (3.58 MHz), which is consistent with it corresponding to a direct ligand to a paramagnetic Mn ion (Randall et al 1997). However, the class described in the second row, with a 2.71 Å dipolar distance, is simulated with only a dipolar coupling.…”

An Oscillating Manganese Electron Paramagnetic Resonance Signal from the S0 State of the Oxygen Evolving Complex in Photosystem II

“…Studies of synthetic Mn complexes might elucidate the phenomenon. For instance, an ESEEM study indicates that methanol replaces water bound to a Mn III -Mn IV dimer (15).…”

Reflections on small molecule manganese models that seek to mimic photosynthetic water oxidation chemistry

“…Based on the magnitude of the hyperfine coupling constants and energy of the transition, it was concluded that the OEC contained a mixed valence manganese cluster [112]. Subsequent analysis suggested that to simulate the OEC spectrum, one needed a cluster of at least three and then four manganese ions to match the EPR, ESEEM and ENDOR spectra [113][114][115]. Thus, this and related Mn III Mn IV species played a crucial role in our early understanding of the enzyme.…”

“…The Mn-Mn separations remain within 0.1Å across this series (∼3.2-3.3Å) and the reduction potential for each successive compound shifts by ∼350 mV. A related series of compounds have also been prepared {[Mn III (2-OH-SALPN)] 2 (L)} which contain a terminal ligand such as water or alcohol [81,115,146,147]. These later compounds were particularly important for establishing the HBDEs for coordinated water protons.…”