Analysis of the electronic structure of the primary electron donor of photosystem I of <i>Spirodela</i> <i>oligorrhiza</i> by photochemically induced dynamic nuclear polarization (photo-CIDNP) solid-state nuclear magnetic resonance (NMR)

Abstract

Abstract. The electron donor in photosystem I (PSI), the chlorophyll dimer P700, is studied by photochemically induced dynamic nuclear polarization (photo-CIDNP) magic angle spinning (MAS) nuclear magnetic resonance (NMR) on selectively 13C and uniformly 15N labeled PSI core preparations (PSI-100) obtained from the aquatic plant duckweed (Spirodela oligorrhiza). Light-induced signals originate from the isotope-labeled nuclei of the cofactors involved in the spin-correlated radical pair forming upon light excitation. Signals are assigned to the two donor cofactors (Chl a and Chl a') and the two acceptor cofactors (both Chl a). Light-induced signals originating from both donor and acceptor cofactors demonstrate that electron transfer occurs through both branches of cofactors in the pseudo-C2 symmetric reaction center (RC). The experimental results supported by quantum chemical calculations indicate that this functional symmetry occurs in PSI despite similarly sized chemical shift differences between the cofactors of PSI and the functionally asymmetric special pair donor of the bacterial RC of Rhodobacter sphaeroides. This contributes to converging evidence that local differences in time-averaged electronic ground-state properties, over the donor are of little importance for the functional symmetry breaking across photosynthetic RC species.

Electronic Structures of Radical-Pair-Forming Cofactors in a Heliobacterial Reaction Center

“…A comparable observation of emissive light-induced 15 N signals has been reported from the carotenoid-less mutant R. sphaeroides R26, which is known to show a strong DR effect [ 52 ]. Such 1D spectra allow the assignment of the 15 N chemical shift and are based on our preliminary studies on Chl a in PSI [ 53 , 54 ] and PSII [ 73 ], as well as BChl a in R. sphaeroides WT [ 74 ] and R26 [ 52 ]. The 15 N chemical shift assignments are shown in Table 1 .…”

“…This appears to be a ubiquitous property of ET in all natural photosynthetic RCs [ 48 ]. The effect has been observed in various RC types, such as the type-II RCs of purple bacteria of Rhodobacter ( R. ) sphaeroides wild type (WT) [ 49 , 50 ] and its carotenoid-less mutant R26 [ 51 , 52 ], as well as in PSI and II from plants [ 53 , 54 ] and diatoms [ 55 ]. Also, homodimeric type-I RCs of Hb.…”

Photo-CIDNP in Solid State

“…Here, the question of the extremely high redox potential of photosystem II was addressed suggesting a chlorophyll-histidine complex acting as donor [ 90 ]. In photosystem I, the activities of the two branches of cofactors were explored [ 91 ]. Photo-CIDNP MAS NMR allowed signals from 13 C labels introduced into reaction centers to be detected directly from entire plants (Fig.…”

“…A sign change of the solid-state photo-CIDNP effect in the diatom Phaeodactylum tricornutum was also observed at higher magnetic fields and has not yet been rationalized [ 93 ]. Second, sign changes related to selective 13 C isotope incorporation shifting the ratio between enhanced absorptive and emissive intensities in favor of the former have been observed in reaction centers of heliobacteria [ 86 , 99 ] and photosystem I [ 91 ]. Hence, it appears that magnetic 13 C isotopes are not “innocent” but involved into the spin-chemical machinery producing the hyperpolarization.…”