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

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 350 ns, 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 30 angstrom(3) (time constant of 350 ns at 25 degrees C; activation energy of 285 +/- 50 meV). 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 (similar to 350 ns), 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 350 ns 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. (C) 2012 Elsevier B.V. All rights reserved.