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Fantuzzi, Andrea; Allgöwer, Friederike; Baker, Holly; McGuire, Gemma; Teh, Wee Kii; Gamiz-Hernandez, Ana P; I Kaila, Ville R; Rutherford, A William
Proceedings of the National Academy of Sciences - PNAS, 02/2022, Letnik: 119, Številka: 6Journal Article
Photosystem II (PSII), the water/plastoquinone photo-oxidoreductase, plays a key energy input role in the biosphere. Q∙−A, the reduced semiquinone form of the nonexchangeable quinone, is often considered capable of a side reaction with O2, forming superoxide, but this reaction has not yet been demonstrated experimentally. Here, using chlorophyll fluorescence in plant PSII membranes, we show that O2 does oxidize Q∙−A at physiological O2 concentrations with a t1/2 of 10 s. Superoxide is formed stoichiometrically, and the reaction kinetics are controlled by the accessibility of O2 to a binding site near Q∙−A, with an apparent dissociation constant of 70 ± 20 µM. Unexpectedly, Q∙−A could only reduce O2 when bicarbonate was absent from its binding site on the nonheme iron (Fe2+) and the addition of bicarbonate or formate blocked the O2-dependant decay of Q∙−A. These results, together with molecular dynamics simulations and hybrid quantum mechanics/molecular mechanics calculations, indicate that electron transfer from Q∙−A to O2 occurs when the O2 is bound to the empty bicarbonate site on Fe2+. A protective role for bicarbonate in PSII was recently reported, involving long-lived Q∙−A triggering bicarbonate dissociation from Fe2+ Brinkert et al., Proc. Natl. Acad. Sci. U.S.A. 113, 12144–12149 (2016). The present findings extend this mechanism by showing that bicarbonate release allows O2 to bind to Fe2+ and to oxidize Q∙−A. This could be beneficial by oxidizing Q∙−A and by producing superoxide, a chemical signal for the overreduced state of the electron transfer chain.
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