Model of the Oxygen Evolving Complex Which Is Highly Predisposed to O–O Bond Formation

Abstract

Light-driven water oxidation is a fundamental reaction in the biosphere. The MnCa cluster of photosystem II cycles through five redox states termed S-S, after which oxygen is evolved. Critically, the timing of O-O bond formation within the Kok cycle remains unknown. By combining recent crystallographic, spectroscopic, and DFT results, we demonstrate an atomistic S state model with the possibility of a low barrier to O-O bond formation prior to the final oxidation step. Furthermore, the associated one electron oxidized S state does not provide more advantages in terms of spin alignment or the energy of O-O bond formation. We propose that a high energy peroxide isoform of the S state can preferentially be oxidized by Tyr in the course of final electron transfer leading to O evolution. Such a mechanism may explain the peculiar kinetic behavior of O evolution as well as serve as an evolutionary adaptation to avoid release of the harmful peroxides.

Theoretical and computational investigations of geometrical, electronic and spin structures of the CaMn4OX (X = 5, 6) cluster in the Kok cycle Si (i = 0–3) of oxygen evolving complex of photosystem II

“…A was assigned as the SFX structure by Okayama group (Suga et al ). Recent density functional theory (DFT) calculations (Beal et al , Pushkar et al ) also concluded the same assignment from their DFT calculations. However, the optimized Mn 4(a) ‐Mn 3(b) distance for Mn‐peroxide was about 2.96 Å in contradiction to the SFX result (2.74 Å by Suga et al () and 2.77 Å by Kern et al ()) as shown in Fig.…”

Two‐Color Valence‐to‐Core X‐ray Emission Spectroscopy Tracks Cofactor Protonation State in a Class I Ribonucleotide Reductase

“…Only recently was a combined EXAFS / ENDOR study able to suggest, based on Mn-Fe distance and absence of strong hyperfine coupling to hydrogen, that 4/4 possesses a di-μ-oxo Mn IV (O) 2 Fe IV core and terminal OH ligand bound to Mn. [7e] Previously, 4/3 was proposed to have a Mn IV (O)(OH)Fe III core, [7b, 8] suggesting the protonation pattern depicted in Scheme 1. These assignments rely, however, on indirect arguments, as intermetallic distances and absence of magnetic coupling are only proxies for the protonation state of the metallocofactor.…”

“…Studies of such systems using element-specific x-ray spectroscopies typically involve serial measurement of each metal, a strategy that can lead to errors from sample variability and difficulty in assessing photoreduction of all metal centers. [7e] Serial data collection also multiplies required collection time and sample quantity, a nontrivial consideration with enzyme intermediates. Ideally, data from all metals in a heterometallic cofactor should be collected simultaneously.…”

“…[15b] Kβ” energy, meanwhile, is determined by donor 2s orbital ionization energy, with larger ionization energies yielding lower XES energies. In Ct RNR-β, the (hydr)oxo ligands in 4/4 and 4/3 exhibit significantly shorter M-L bonds than the rest of the ligands [7b, 7e] and therefore dominate the Kβ” region. Conversion from 4/4 to 4/3 is proposed to result in protonation of one oxo ligand in the di-μ-oxo core of 4/4 (Scheme 1), which should elongate the M-O bonds and delocalize O 2s character away from the metals; both effects would reduce metal n p overlap and thus reduce Kβ” intensity.…”

“…Both of these structural elements—the short terminal Mn-OH bond and the Mn-O oxo contraction in the 4/3 —have been seen in previous DFT calculations on Ct RNR-β. [7b, 21] The possibility of protonation occurring at the terminal Mn-bound OH was also explored and found to be inconsistent with the data (details in the Supporting Information). The calculated spectra for Fe are also consistent with experiment; specifically, an intense Kβ” peak calculated for 4/4 is predicted to become markedly less intense upon conversion to 4/3 , consistent with the loss of one oxo moiety and the generally longer bonds present for Fe III compared to Fe IV .…”