Five-coordinate Mn ^IV intermediate in the activation of nature’s water splitting cofactor

Abstract

Nature’s water splitting cofactor passes through a series of catalytic intermediates (S0-S4) before O-O bond formation and O2 release. In the second last transition (S2 to S3) cofactor oxidation is coupled to water molecule binding to Mn1. It is this activated, water-enriched all MnIV form of the cofactor that goes on to form the O-O bond, after the next light-induced oxidation to S4. How cofactor activation proceeds remains an open question. Here, we report a so far not described intermediate (S3') in which cofactor oxidation has occurred without water insertion. This intermediate can be trapped in a significant fraction of centers (>50%) in (i) chemical-modified cofactors in which Ca2+ is exchanged with Sr2+; the Mn4O5Sr cofactor remains active, but the S2-S3 and S3-S0 transitions are slower than for the Mn4O5Ca cofactor; and (ii) upon addition of 3% vol/vol methanol; methanol is thought to act as a substrate water analog. The S3' electron paramagnetic resonance (EPR) signal is significantly broader than the untreated S3 signal (2.5 T vs. 1.5 T), indicating the cofactor still contains a 5-coordinate Mn ion, as seen in the preceding S2 state. Magnetic double resonance data extend these findings revealing the electronic connectivity of the S3' cofactor is similar to the high spin form of the preceding S2 state, which contains a cuboidal Mn3O4Ca unit tethered to an external, 5-coordinate Mn ion (Mn4). These results demonstrate that cofactor oxidation regulates water molecule insertion via binding to Mn4. The interaction of ammonia with the cofactor is also discussed.

Untangling the sequence of events during the S 2 → S 3 transition in photosystem II and implications for the water oxidation mechanism

“…Mn3 O3 et al (35), based on W-band EPR results, proposed oxidation of Mn1 prior to binding of water, which would also be consistent with our results presented above.…”

“…•+ is followed by proton transfer/release in the S 2 → S 3 transition, and that only thereafter can the electron transfer from Mn to Y Z • occur (33,34). The order of the two other important steps of this transition, oxidation of Mn and insertion of water, is not clear yet, and proposals for either oxidation first or insertion first have been put forward (26,30,(35)(36)(37)(38)(39). Additionally, it was suggested that the cluster undergoes some rearrangement between a "rightopen" or "open-cubane" and a "left-open" or "closed-cubane" structure during the S 2 → S 3 transition (SI Appendix, Fig.…”

“…7B). Chrysina et al (35) Fig. 7A summarizes the sequence of events that are observed around the OEC during the S 2 → S 3 transition, based on crystallography and XES data.…”

Substrate water exchange in the S2 state of photosystem II is dependent on the conformation of the Mn4Ca cluster

“…7 If left in the dark, the OEC will eventually relax into the dark-stable S 1 state. 8 The lowest oxidation state of the Mn 4 Ca cluster in the water splitting cycle, the S 0 state, was shown by 55 Mn-ENDOR spectroscopy to have the oxidation states Mn(III,III,III,IV). 9 These overall 'high' oxidation states were recently confirmed by photoactivation experiments.…”

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

“…Lastly, Cox et al . reported high field (Q, W band) pulsed EPR on the S 3 state in native thermophilic PSII cores and very recently in Sr/MeOH modified samples . The S 3 state is heterogeneous in these systems, one population (∼60 %) exhibits a high spin, S T =3 magnetic state, while the other is EPR silent.…”