Trapping of Metalloradical Intermediates of the S-States at Liquid Helium Temperatures. Overview of the Phenomenology and Mechanistic Implications

Abstract

The oxygen-evolving complex (OEC) of photosystem II (PSII) consists of a Mn cluster (believed to be tetranuclear) and a tyrosine (Tyr Z or Y(Z)). During the sequential absorption of four photons by PSII, the OEC undergoes four oxidative transitions, S(0) to S(1), ..., S(3) to (S(4))S(0). Oxygen evolves during the S(3) to S(0) transition (S(4) being a transient state). Trapping of intermediates of the S-state transitions, particularly those involving the tyrosyl radical, has been a goal of ultimate importance, as that can test critically models employing a role of Tyr Z in proton (in addition to electron) transfer, and also provide important clues about the mechanism of water oxidation. Until very recently, however, critical experimental information was lacking. We review and evaluate recent observations on the trapping of metalloradical intermediates of the S-state transitions, at liquid helium temperatures. These transients are assigned to Tyr Z(*) magnetically interacting with the Mn cluster. Besides the importance of trapping intermediates of this unique catalytic mechanism, liquid helium temperatures offer the additional advantage that proton motions (unlike electron transfer) are blocked except perhaps across strong hydrogen bonds. This paper summarizes the recent observations and discusses the constraints that the phenomenology imposes.

Low-temperature photochemistry in photosystem II from Thermosynechococcus elongatus induced by visible and near-infrared light

“…This result contrasts somewhat with previous reports in which a decay of this split signal was observed (Petrouleas et al 2005). This discrepancy could originate from a difference in the quality of light, i.e.…”

“…This discrepancy could originate from a difference in the quality of light, i.e. visible light filtered by an RG 715 Schott filter (Petrouleas et al 2005) versus 820 nm laser light used here. Alternatively, the different protocol used to generate the S 3 state could explain the different stabilities of the signal, i.e.…”

“…In S 3 , NIR illumination at 4.2 K does result in the formation of a split signal (Petrouleas et al 2005). However, this signal was attributed to S 2 TyrZ % formed by NIRinduced conversion of the Mn cluster into a state so oxidizing that the back reaction, S 3 TyrZ to S 2 TyrZ % , occurs (Petrouleas et al 2005). The split signals generated in the S 3 state by NIR illumination in Ca-PSII (218 gauss width) and Sr-PSII (295 gauss width) are shown in figure 1d.…”

“…More recently, several other 'split' signals were also observed in functional PSII. They were generated by illuminating PSII in the S 0 , S 1 or S 2 states with visible light or in the S 3 state with near-infrared (NIR) light either at liquid helium temperatures or at 200 K. The species that were formed under these conditions were proposed to correspond to 'non-relaxed' S 0 TyrZ % S 1 TyrZ % and S 2 TyrZ % states (Ioannidis et al 2002;Koulougliotis et al 2003Koulougliotis et al , 2004Zhang & Styring 2003;Zhang et al 2004;Petrouleas et al 2005;Havelius et al 2006;Ioannidis et al 2006) that could correspond to intermediates in the oxygen-evolving process.…”

Misses during Water Oxidation in Photosystem II Are S State-dependent

“…In the last decade we have developed S state-specific EPR probes to the S 1 , S 3 , and S 0 states (36,37 (37,38). In combination with the well known S 2 state multiline EPR signal, these Split EPR signals provide a direct possibility to quantify all S states independently, even in the very same sample.…”