title: Carboxylate shifts steer interquinone electron transfer in photosynthesis.
abstract: Understanding the mechanisms of electron transfer (ET) in photosynthetic reaction centers (RCs) may inspire novel catalysts for sunlight-driven fuel production. The electron exit pathway of type II RCs comprises two quinone molecules working in series and in between a non-heme iron atom with a carboxyl ligand (bicarbonate in photosystem II (PSII), glutamate in bacterial RCs). For decades, the functional role of the iron has remained enigmatic. We tracked the iron site using microsecond-resolution x-ray absorption spectroscopy after laser-flash excitation of PSII. After formation of the reduced primary quinone, Q(A)(-), the x-ray spectral changes revealed a transition (t½ ≈ 150 μs) from a bidentate to a monodentate coordination of the bicarbonate at the Fe(II) (carboxylate shift), which reverted concomitantly with the slower ET to the secondary quinone Q(B). A redox change of the iron during the ET was excluded. Density-functional theory calculations corroborated the carboxylate shift both in PSII and bacterial RCs and disclosed underlying changes in electronic configuration. We propose that the iron-carboxyl complex facilitates the first interquinone ET by optimizing charge distribution and hydrogen bonding within the Q(A)FeQ(B) triad for high yield Q(B) reduction. Formation of a specific priming intermediate by nuclear rearrangements, setting the stage for subsequent ET, may be a common motif in reactions of biological redox cofactors.
authors.affiliation: Freie Universität Berlin, Institut für Experimentalphysik, 14195 Berlin, Germany.
authors.forename: Petko
authors.initials: P
authors.lastname: Chernev
authors.forename: Ivelina
authors.initials: I
authors.lastname: Zaharieva
authors.forename: Holger
authors.initials: H
authors.lastname: Dau
authors.forename: Michael
authors.initials: M
authors.lastname: Haumann
mesh_terms: D016227:Benzoquinones / Q000737:chemistry* / Q000378:metabolism; D004579:Electron Transport / Q000502:physiology; D007501:Iron / Q000737:chemistry* / Q000378:metabolism; D010788:Photosynthesis / Q000502:physiology*; D045332:Photosystem II Protein Complex / Q000737:chemistry* / Q000378:metabolism; D012242:Rhodobacter sphaeroides / Q000201:enzymology*; D056928:X-Ray Absorption Spectroscopy
chemical_list: D016227:Benzoquinones; D045332:Photosystem II Protein Complex; C004532:quinone; D007501:Iron