Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

Petko Chernev,Ivelina Zaharieva,Holger Dau,Michael Haumann

doi:10.1074/jbc.m110.202879

Petko Chernev, Ivelina Zaharieva + Show 2 more

Open Access

https://doi.org/10.1074/jbc.m110.202879

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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.

Highlights

Photosystem II (PSII) of plants and cyanobacteria catalyzes the light-driven abstraction of electrons from water molecules at a manganese-calcium complex, the process of water oxidation and dioxygen formation [5, 6]
Because PSII membranes contain two Fe atoms bound directly to the PSII reaction center [38] and possibly spurious contaminations with rubredoxin containing Fe(III) [39], we estimate that about 2.5 additional unspecific Fe atoms per PSII were present in the x-ray absorption spectroscopy (XAS) samples
The density-functional theory (DFT) data and previous XAS and crystallography studies [20, 26] on BRCs, in which the BC is replaced by the carboxyl group of glutamate, favor a similar coordination change in this system

Summary

Introduction

Photosystem II (PSII) of plants and cyanobacteria catalyzes the light-driven abstraction of electrons from water molecules at a manganese-calcium complex, the process of water oxidation and dioxygen formation [5, 6]. A similar QAFeQB triad is found in the non-oxygenic reaction center of purple bacteria (BRC) [9], but instead of plastoquinone molecules as in PSII, other quinone types are employed. Crystal structures of PSII so far were reported only at a lower resolution of Ն2.9 Å [7, 8] (a structure at higher resolution may become available in the future) [24]. For both PSII and BRCs, in particular the function of the non-heme iron and of its carboxyl ligand in the ET reactions has remained enigmatic [15,16,17,18,19].

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