Tyrosine radicals are involved in the photosynthetic oxygen-evolving system.

Abstract

In addition to the reaction-center chlorophyll, at least two other organic cofactors are involved in the photosynthetic oxygen-evolution process. One of these cofac.tors, called "Z," transfers electrons from the site of water oxidation to the reaction center of photosystem II. The other species, "D," has an uncertain function but gives rise to the stable EPR signal known as signal II. ZV and D+ have identical EPR spectra and are generally assumed to arise from species with the same chemical structure. Results from a variety of experiments have suggested that Z and D are plastoquinones or plastoquinone derivatives. In general, however, the evidence to support this assignment is indirect. To address this situation, we have developed more direct methods to assign the structure of the ZV/Dt radicals. By selective in vivo deuteration of the methyl groups of plastoquinone in cyanobacteria, we show that hyperfine couplings from the methyl protons cannot be responsible for the partially resolved structure seen in the Dt EPR spectrum. That is, we verify by extraction and mass spectrometry that quinones are labeled in algae fed deuterated methionine, but no change is observed in the line shape of signal II.Considering the spectral properties ofthe Dt radical, a tyrosine origin is a reasonable alternative. In a second series of experiments, we have found that deuteration of tyrosine does indeed narrow the Dt signal. Extraction and mass spectral analysis of the quinones in these cultures show that they are not labeled by tyrosine. These results eliminate a plastoquinone origin for Dt; we conclude instead that Dt, and most likely Zt, are tyrosine radicals.In plant and algal photosynthesis, photosystem II (PSII) catalyzes the light-induced oxidation of water and reduction of plastoquinone. The smallest purified unit that is capable of carrying out this reaction consists of seven polypeptides and contains chlorophyll, plastoquinone, manganese, and several other bound cofactors (for review, see refs. 1 and 2). Water oxidation occurs at a site that contains a cluster of four Mn atoms. This center is interfaced to the photochemically active PSII reaction-center chlorophyll, P680, by at least one intermediate electron carrier, which is usually designated The oxidized form of this cofactor, Zt, has a light-induced EPR signal that identifies it as an organic radical (3-6). A variety of kinetic data indicates that Z reduces P680+ directly and that the resulting Zt species is in turn reduced by the manganese ensemble (refs. 1 and 2, but see refs. 7 and 8). In addition to the EPR signal from Z+, PSII preparations also show a stable EPR signal (signal II) with the same lineshape as Zt (9). The radical giving rise to this spectrum is now usually referred to as "D+". Recent data reported by Styring and Rutherford suggest that D may be involved in maintaining the integrity of the manganese complex (10).Because the Zt and Dt EPR spectra are identical, it is generally assumed that Z and D are species that have the same chemical str...

Proton-coupled electron transfer: the mechanistic underpinning for radical transport and catalysis in biology

“…The recent crystal structures of photosystem II (PSII; Ferreira et al 2004;Loll et al 2005) support suggestions that as the oxygen-evolving complex (OEC) steps through its various S-states (Vrettos & Brudvig 2002;Hoganson & Tommos 2004), substratederived protons are shuttled to the lumen via a proton exit channel, the headwater of which appears to be the D61 residue hydrogen bonded to Mn-bound water . As shown by the structure reproduced in figure 3, D61 is diametrically opposite to Y Z , which has long been known (Barry & Babcock 1987;Debus et al 1988a,b) to be the electron relay between the reaction centre and the OEC. The crystal structure of PSII also suggests that orthogonal PCET may be used to generate amino acid radicals.…”

Mechanism of tyrosine D oxidation in Photosystem II

“…7). TyrD oxidizes Mn 4 CaO 5 in the S0 state to form S1 (8) and oxidizes overreduced states of Mn 4 CaO 5 (9), and this may be relevant to the oxidative assembly of the Mn 4 CaO 5 cluster (6,8,10). It has also been proposed that TyrD has an electrostatic influence on energetics of the cationic [P D1 /P D2 ]…”

Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation

“…In this process, Tyr Z loses its phenolic proton, likely to the nearby D 1 His190 group, to generate the neutral tyrosine radical Tyr Z -O • (E 0 ¼ 0.9-1.0 V vs. SCE). The radical Tyr Z -O • then removes one electron from the OEC on the microsecond timescale, increasing its oxidation state (6,(9)(10)(11). After four light-induced charge separations, the OEC oxidizes two water molecules, releases molecular oxygen, and returns to its initial oxidation state.…”