15N Photo-CIDNP MAS NMR To Reveal Functional Heterogeneity in Electron Donor of Different Plant Organisms

Abstract

In plants and cyanobacteria, two light-driven electron pumps, photosystems I and II (PSI, PSII), facilitate electron transfer from water to carbon dioxide with quantum efficiency close to unity. While similar in structure and function, the reaction centers of PSI and PSII operate at widely different potentials with PSI being the strongest reducing agent known in living nature. Photochemically induced dynamic nuclear polarization (photo-CIDNP) in magic-angle spinning (MAS) nuclear magnetic resonance (NMR) measurements provides direct excess to the heart of large photosynthetic complexes (A. Diller, Alia, E. Roy, P. Gast, H.J. van Gorkom, J. Zaanen, H.J.M. de Groot, C. Glaubitz, J. Matysik, Photosynth. Res. 84, 303-308, 2005; Alia, E. Roy, P. Gast, H.J. van Gorkom, H.J.M. de Groot, G. Jeschke, J. Matysik, J. Am. Chem. Soc. 126, 12819-12826, 2004). By combining the dramatic signal increase obtained from the solid-state photo-CIDNP effect with 15 N isotope labeling of PSI, we were able to map the electron spin density in the active cofactors of PSI and study primary charge separation at atomic level. We compare data obtained from two different PSI proteins, one from spinach (Spinacia oleracea) and other from the aquatic plant duckweed (Spirodella oligorrhiza). Results demonstrate a large flexibility of the PSI in terms of its electronic architecture while their electronic ground states are strictly conserved.

Photo-CIDNP in the Reaction Center of the Diatom Cyclotella meneghiniana Observed by 13C MAS NMR

“…The effect is not limited to bacterial RCs but is also observed in RCs of plants, e.g., Spinacia oleracea [20] [21] [22] and Spirodella oligorrhiza. [23] Furthermore, it was demonstrated, that photo-CIDNP can also be observed in the C57S-mutant of phototropin LOV1 [24] from the green alga Chlamydomonas rheinhardtii. This blue-light photoreceptor is presently the only non-photosynthetic system demonstrated to show the effect.…”

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

“…If the electron transfer chain in PSI is bidirectional, a maximum of sixteen nitrogen atoms can occur in the 15 N photo-CIDNP MAS NMR spectrum, originating from up to three Chl a cofactors and the single Chl a 0 cofactor. The photo-CIDNP spectra from duckweed showed a maximum of 11 light-induced signals [56], whereas in spinach only 8 signals were observed [70] (Fig. 3B) ( Table 2).…”

“…Due to the transient non-Boltzmann distribution of the population of nuclear spin states in rigid samples upon photo-reaction, a strong signal enhancement has been observed in several different RC species by 13 C and 15 N MAS NMR [13,[48][49][50][51][52][53][54][55][56]. The representative solid-state photo-CIDNP spectra in RCs of R. sphaeroides WT and R26 are shown in Fig.…”

“…PCC 6803 strain) [55,56]. In the following section we will focus on photo-CIDNP MAS NMR studies on PSI and PSII which lead to an insight into the electronic structure of the primary donor P700 * and P680 Å+ .…”

“…In order to study the rigidity and flexibility of the electronic architecture of PSI in different organism, the data was obtained from two different PSI proteins, one from 15 N labeled spinach [54] and other from the 15 N labeled aquatic plant duckweed (S. oligorrhiza) [56]. If the electron transfer chain in PSI is bidirectional, a maximum of sixteen nitrogen atoms can occur in the 15 N photo-CIDNP MAS NMR spectrum, originating from up to three Chl a cofactors and the single Chl a 0 cofactor.…”