Structural changes correlated with magnetic spin state isomorphism in the S₂ state of the Mn₄CaO₅ cluster in the oxygen-evolving complex of photosystem II

Abstract

The Mn4CaO5 cluster in Photosystem II catalyzes the four-electron redox reaction of water oxidation in natural photosynthesis. This catalytic reaction cycles through four intermediate states (Si, i = 0 to 4), involving changes in the redox state of the four Mn atoms in the cluster. Recent studies suggest the presence and importance of isomorphous structures within the same redox/intermediate S-state. It is highly likely that geometric and electronic structural flexibility play a role in the catalytic mechanism. Among the catalytic intermediates that have been identified experimentally thus far, there is clear evidence of such isomorphism in the S2 state, with a high-spin (5/2) (HS) and a low spin (1/2) (LS) form, identified and characterized by their distinct electron paramagnetic resonance (EPR spectroscopy) signals. We studied these two S2 isomers with Mn extended X-ray absorption fine structure (EXAFS) and absorption and emission spectroscopy (XANES/XES) to characterize the structural and electronic structural properties. The geometric and electronic structure of the HS and LS S2 states are different as determined using Mn EXAFS and XANES/XES, respectively. The Mn K-edge XANES and XES for the HS form are different from the LS and indicate a slightly lower positive charge on the Mn atoms compared to the LS form. Based on the EXAFS results which are clearly different, we propose possible structural differences between the two spin states. Such structural and magnetic redox-isomers if present at room temperature, will likely play a role in the mechanism for water-exchange/oxidation in photosynthesis.

Structural isomers of the S2 state in photosystem II: do they exist at room temperature and are they important for function?

“…As discussed above, it has been proposed that such geometric and electronic structural flexibility in S 2 may play a role in the formation of the S 3 state through water binding (Pantazis et al , Cox et al , Cox and Messinger , Isobe et al , Ugur et al , Boussac et al ). Our XAS studies using synchrotron radiation (SR) at cryogenic temperature also shows differences in the geometric and electronic structure of the cryo‐trapped HS and LS S 2 states (Chatterjee et al ). Such structural and magnetic redox‐isomers, if present at RT, will probably play a role during the catalysis for determining the directionality and the kinetics of the reaction.…”

“…As discussed above, there are many indications for the presence of two forms of the S 2 state (high‐spin S total = 5/2 and low spin S total = 1/2 states, Fig. A) at least at cryogenic temperatures (Boussac et al , , Pantazis et al , Bovi et al , Cox et al , Isobe et al , Chatterjee et al ). Nevertheless, the right‐open S 2 state seems to be the one that best explains the diffraction data obtained at room temperature (Fig.…”

“…We have investigated the isomorphism in the S 2 state using Mn K‐edge X‐ray absorption spectroscopy combined with supporting EPR characterization (Chatterjee et al ). Fig.…”

“…The spectrum of the 140 K illuminated sample (HS‐rich) after 200 K annealing is also shown (cyan) (D) EPR spectrum of the sample annealed at 200 K (cyan) after 140 K with illumination compared to the 140 K with NIR (black) spectrum. The figure is adapted from Chatterjee et al .…”

Rationalizing the Geometries of the Water Oxidising Complex in the Atomic Resolution, Nominal S3 State Crystal Structures of Photosystem II

“…One early study from the Berkeley group reported that a 2.73 Å Mn−Mn vector, seen in the S 1 and low spin S 2 states, elongated to 2.85 Å in the high spin S 2 state. However, a recent, more comprehensive study from the same laboratory, did not support this. No evidence of any new Mn–Mn vector of ∼2.85 Å in either the low or high spin S 2 states, was seen in functional systems.…”