Fast structural changes (200–900 ns) may prepare the photosynthetic manganese complex for oxidation by the adjacent tyrosine radical

Abstract

The Mn complex of photosystem II (PSII) cycles through 4 semi-stable states (S(0) to S(3)). Laser-flash excitation of PSII in the S(2) or S(3) state induces processes with time constants around 350ns, which have been assigned previously to energetic relaxation of the oxidized tyrosine (Y(Z)(ox)). Herein we report monitoring of these processes in the time domain of hundreds of nanoseconds by photoacoustic (or 'optoacoustic') experiments involving pressure-wave detection after excitation of PSII membrane particles by ns-laser flashes. We find that specifically for excitation of PSII in the S(2) state, nuclear rearrangements are induced which amount to a contraction of PSII by at least 30Å(3) (time constant of 350ns at 25°C; activation energy of 285+/-50meV). In the S(3) state, the 350-ns-contraction is about 5 times smaller whereas in S(0) and S(1), no volume changes are detectable in this time domain. It is proposed that the classical S(2)=>S(3) transition of the Mn complex is a multi-step process. The first step after Y(Z)(ox) formation involves a fast nuclear rearrangement of the Mn complex and its protein-water environment (~350ns), which may serve a dual role: (1) The Mn- complex entity is prepared for the subsequent proton removal and electron transfer by formation of an intermediate state of specific (but still unknown) atomic structure. (2) Formation of the structural intermediate is associated (necessarily) with energetic relaxation and thus stabilization of Y(Z)(ox) so that energy losses by charge recombination with the Q(A)(-) anion radical are minimized. The intermediate formed within about 350ns after Y(Z)(ox) formation in the S(2)-state is discussed in the context of two recent models of the S(2)=>S(3) transition of the water oxidation cycle. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: From Natural to Artificial.

Pathway for Mn-cluster oxidation by tyrosine-Z in the S 2 state of photosystem II

“…In particular, the resulting Mn 4 (IV) geometry has an elongated Mn1-Mn4 distance, conferring to the cluster a more open structure, which might lead to an increase in the molecular volume. Interestingly, a significant increase in the molecular volume has been also observed by Dau and coworkers in photo-acoustic experiments between S 2 and S 3 states (52,53) and attributed to a proton release from the cluster. In this regard it should be noted that the PCET mechanism involving the simultaneous proton shuffling between Tyr-Z and His190 and the electron transfer from the Mn4 to the radical Tyr-Z cannot be associated with the proton release observed by Dau and coworkers (52).…”

Probing the role of arginine 323 of the D1 protein in photosystem II function

“…Firstly, the slowdown of the P 680 + decay occurs in a time domain proposed to correspond to the establishment of the Tyr Z P 680 + ↔ [Tyr Z ox P 680 ] initial after the pure electron transfer between Tyr Z and P 680 + in the tens of nanosecond time range and before the proton movements resulting from the oxidation of Tyr Z ; these proton movements occurring on a large scale in the microsecond time domain. This equilibrium has been considered as a dielectric relaxation (Renger 2012, Klauss et al 2012a, 2012b) and it would stabilize the Tyr Z ox initially formed by lowering its free‐energy level (Klauss et al 2012a, 2012b). In the PsbA3/R323E mutant, the slowdown of the Tyr Z P 680 + ↔ [Tyr Z ox P 680 ] initial equilibrium would therefore correspond to an increase of the free energy level of the [Tyr Z ox P 680 ] initial state.…”

“…In the S 4 ‐state, the two water molecules bound to the cluster are oxidized, the O=O bond is formed, O 2 is released and the S 0 ‐state is regenerated. During the enzyme cycle, the increase in charge resulting from electron abstraction from the Mn 4 CaO 5 cluster is compensated for by proton releases which help to maintain its redox potential below that of Tyr Z • /Tyr Z (Rappaport and Lavergne 2001, Siegbahn and Lundberg 2005, Klauss et al 2012a, 2012b). At pH 6.5, the stoichiometry for the proton release into the bulk is close to 1, 0, 1, 2 in the S 0 → S 1 , S 1 → S 2 , S 2 → S 3 and S 3 → S 0 transitions, respectively (Fowler 1977, Saphon and Crofts 1977, Förster and Junge 1985, Schlodder and Witt 1985, Rappaport and Lavergne 1991, Suzuki et al 2009).…”

Water oxidation in photosystem II

“…In this sequence, Y Z promotes both electron and proton transfer in the catalytic cycle displaying a dual function (Bovi et al 2013; Klauss et al 2012b; Perez-Navarro et al 2016). Between S i and S i +1 states (for i = 0–3) the short-lived S i Y Z ˙ intermediates exist.…”