Electrostatics and proton transfer in photosynthetic water oxidation

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Abstract
Photosystem II (PSII) oxidizes two water molecules to yield dioxygen plus four protons. Dioxygen is released during the last out of four sequential oxidation steps of the catalytic centre (S0⇒ S1, S1⇒ S2, S2⇒ S3, S3⇒ S4→ S0). The release of the chemically produced protons is blurred by transient, highly variable and electrostatically triggered proton transfer at the periphery (Bohr effect). The extent of the latter transiently amounts to more than one H+/e–under certain conditions and this is understood in terms of electrostatics. By kinetic analyses of electron–proton transfer and electrochromism, we discriminated between Bohr–effect and chemically produced protons and arrived at a distribution of the latter over the oxidation steps of 1 : 0 : 1 : 2. During the oxidation of tyr–161 on subunit D1 (YZ), its phenolic proton is not normally released into the bulk. Instead, it is shared with and confined in a hydrogen–bonded cluster. This notion is difficult to reconcile with proposed mechanisms where YZacts as a hydrogen acceptor for bound water. Only in manganese (Mn) depleted PSII is the proton released into the bulk and this changes the rate of electron transfer between YZand the primary donor of PSII P+680from electron to proton controlled. D1–His190, the proposed centre of the hydrogen–bonded cluster around YZ, is probably further remote from YZthan previously thought, because substitution of D1–Glu189, its direct neighbour, by Gln, Arg or Lys is without effect on the electron transfer from YZto P+680(in nanoseconds) and from the Mn cluster to YoxZ.