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 (S0 to S3). Laser-flash excitation of PSII in the S2 or S3 state induces processes with time constants around 350 ns, which have been assigned previously to energetic relaxation of the oxidized tyrosine (YZox). 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 S2 state, nuclear rearrangements are induced which amount to a contraction of PSII by at least 30 Å3 (time constant of 350 ns at 25 °C; activation energy of 285 +/− 50 meV). In the S3 state, the 350-ns-contraction is about 5 times smaller whereas in S0 and S1, no volume changes are detectable in this time domain. It is proposed that the classical S2 = > S3 transition of the Mn complex is a multi-step process. The first step after YZox formation involves a fast nuclear rearrangement of the Mn complex and its protein–water environment (~ 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 YZox so that energy losses by charge recombination with the QA− anion radical are minimized. The intermediate formed within about 350 ns after YZox formation in the S2-state is discussed in the context of two recent models of the S2 = > S3 transition of the water oxidation cycle. This article is part of a Special Issue entitled: Photosynthesis Research for Sustainability: From Natural to Artificial.

► Photosynthetic water oxidation may be more intricate than previously thought.
► Laser-induced photocoustics reveals structural changes after tyrosine oxidation.
► Nuclear rearrangements amount to sizeable protein contraction in the S2-state.
► Chemical-structural change precedes electron transfer and proton removal.
► Proposed dual role: energetic relaxation and preparation for subsequent steps.