Analysis of electron donors in photosystems in oxygenic photosynthesis by photo-CIDNP MAS NMR

Abstract

Both photosystem I and photosystem II are considerably similar in molecular architecture but they operate at very different electrochemical potentials. The origin of the different redox properties of these RCs is not yet clear. In recent years, insight was gained into the electronic structure of photosynthetic cofactors through the application of photochemically induced dynamic nuclear polarization (photo-CIDNP) with magic-angle spinning NMR (MAS NMR). Non-Boltzmann populated nuclear spin states of the radical pair lead to strongly enhanced signal intensities that allow one to observe the solid-state photo-CIDNP effect from both photosystem I and II from isolated reaction center of spinach (Spinacia oleracea) and duckweed (Spirodela oligorrhiza) and from the intact cells of the cyanobacterium Synechocystis by (13)C and (15)N MAS NMR. This review provides an overview on the photo-CIDNP MAS NMR studies performed on PSI and PSII that provide important ingredients toward reconstruction of the electronic structures of the donors in PSI and PSII.

15N photo-CIDNP MAS NMR on both photosystems and magnetic field-dependent 13C photo-CIDNP MAS NMR in photosystem II of the diatom Phaeodactylum tricornutum

“…Photo-CIDNP (photochemically induced dynamic nuclear polarization) MAS NMR presents a versatile tool to investigate electronic and chemical structures of the most substantial cofactors involved in photosynthesis as well as the underlying spin dynamics (Jeschke and Matysik 2003;Daviso et al 2008;Matysik et al 2009;Thamarath et al 2012;Bode et al 2013;Najdanova et al 2015). This technique allows for the selective enhancement of NMR signals from the donor and the primary electron acceptor molecules in photosynthetic reaction centers (RCs).…”

Quantum Chemical Spin Densities for Radical Cations of Photosynthetic Pigment Models

“…The PRCs of purple bacteria contain a so‐called “special pair”, which is a dimer of bacteriochlorophylls (BChls). The primary electron donor in the PRC in photosystem I (PSI) of higher plants is a chlorophyll a (Chl a ) – chlorophyll a ′ (Chl a ′) heterodimer known as P700 . The plant photosystem II (PSII) reaction center contains a central pair of Chl a molecules known as P680.…”

“…The plant photosystem II (PSII) reaction center contains a central pair of Chl a molecules known as P680. Possibly, also neighboring (so‐called accessory ) Chl a molecules are involved in the initial charge separation in PSII .…”

“…As the initial charge‐transfer event produces a radical cation in these primary donors, experiments sensitive to the spin density are important to characterize the electronic structure of these intermediates. Hence, photochemically induced dynamic nuclear polarization nuclear magnetic resonance allows to reconstruct spin‐density maps in the primary electron donors of PRCs of higher plants and bacteria . Techniques such as standard electron paramagnetic resonance, electron nuclear double resonance and electron spin echo envelope modulation can be applied for measurements of hyperfine coupling constants of single cofactors as well as of primary electron donors .…”

Analysis of the Electronic Structure of the Special Pair of a Bacterial Photosynthetic Reaction Center by 13C Photochemically Induced Dynamic Nuclear Polarization Magic‐Angle Spinning NMR Using a Double‐Quantum Axis

“…The high sensitivity and selectivity of the photo-CIDNP MAS NMR experiment provide an excellent analytical tool for studying photosynthetic SCRPs in great detail (29,30). This method has been applied to various photosynthetic systems (31)(32)(33)(34).…”