Analysis of the electronic asymmetry of the primary electron donor of photosystem I of <i>Spirodela oligorrhiza</i> by photo-CIDNP solid-state NMR

Abstract

Abstract. The electron donor in photosystem I, the chlorophyll dimer P700, is studied by photo-CIDNP (photochemically induced dynamic nuclear polarization) MAS (magic-angle spinning) 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 labelled 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 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 functional symmetry breaking across photosynthetic RC species.

Theoretical Assessment of Hinge-Type Models for Electron Donors in Reaction Centers of Photosystems I and II as well as of Purple Bacteria

“…Therefore, the obtained results for both protonated and deprotonated complexes in PSI show only a minor degree of the spin density delocalization between Chl and His molecules. This agrees well with experimental photo-CIDNP NMR studies, ,, where all spectroscopic signals were attributed to either a single Chl a molecule or the [P A ···P B ] dimer. , Unfortunately, this small degree of delocalization in the calculated complexes prevents us from drawing an unambiguous conclusion about the protonation state of the axial His molecules in PSI.…”

“…This agrees well with experimental photo-CIDNP NMR studies, 3,18,78 where all spectroscopic signals were attributed to either a single Chl a molecule 78 or the [P A ••• P B ] dimer. 3,79 Unfortunately, this small degree of delocalization in the calculated complexes prevents us from drawing an unambiguous conclusion about the protonation state of the axial His molecules in PSI. 4.3.…”

“…In addition to the structural differences, the cofactors in PSII and PSI are perturbed differently by the surrounding protein matrices and show distinct extents of asymmetry in experimentally reconstructed spin density distributions compared to monomeric Chl a in solution . The inner pair cofactors from PSII are known to interact strongly with the nearby protein environment, while the analogous pair in PSI is essentially unperturbed. , Measured photo-CIDNP MAS NMR signals of PSI were assigned to a single Chl molecule and showed only a slight degree of asymmetry (absence of photo-CIDNP intensities at Chl atoms C-5 and C-20). , Hovewer, more recent measurements with 13 C isotope labels introduced revealed a dimeric nature of the donor in PSI . Similar experiments for PSII reported a highly asymmetrical spin density distribution over P D1 . ,, A substitution of axial His molecules in PSI by other uncharged polar amino acids using site-directed mutagenesis did not lead to significant changes in the spin density pointing at a rather weak interaction between Chl and His molecules in PSI.…”

“…18,78 Hovewer, more recent measurements with 13 C isotope labels introduced revealed a dimeric nature of the donor in PSI. 79 Similar experiments for PSII reported a highly asymmetrical spin density distribution over P D1 . 3,17,18 A substitution of axial His molecules in PSI by other uncharged polar amino acids using site-directed mutagenesis did not lead to significant changes in the spin density 80 pointing at a rather weak interaction between Chl and His molecules in PSI.…”

Spin Hyperpolarization in Modern Magnetic Resonance

“…On the other hand, in photosystem I, no functional symmetry breaking occurs and both branches of cofactors are active. Chemical shifts of the two cofactors in the “special pair” are rather different; however, the differences are not much larger than those observed in the donor dimer of photosystem I . Therefore, the ground-state electronic structure does not appear to be the decisive factor.…”