Electron−Nuclear Spin Dynamics in a Bacterial Photosynthetic Reaction Center

Abstract

The solid-state photo-CIDNP effect is known to occur in natural photosynthetic reaction centers (RCs) where it can be observed by magic-angle spinning (MAS) NMR as strong modification of signal intensities under illumination compared to experiments performed in the dark. The origin of the effect has been debated. In this paper, we report time-resolved photo-CIDNP MAS NMR data of reaction centers of quinone depleted Rhodobacter sphaeroides. It is demonstrated that the build-up of nuclear polarization on the primary donor and the bacteriopheophytin acceptor depends on the presence and lifetimes of the molecular triplet states of the donor and carotenoid. Analysis of the data proves that up to three electron-nuclear spin-coupling mechanisms and two transient effects are working concomitantly in the spin-chemical machinery of the reaction center.

Photochemically Induced Dynamic Nuclear Polarization Observed by Solid-State NMR in a Uniformly 13C-Isotope-Labeled Photosynthetic Reaction Center

“…However, at 9.4 T production of hyperpolarization appears to be slower than its dissipation, and no hyperpolarization has been observed under continuous illumination (data not shown). These results demonstrate that the solid-state photo-CIDNP effect also occurs in quantitatively 13 C labeled samples; the results also show the occurrence of polarization transfer to near-by aliphatic nuclei. The latter is presumably driven by spin-diffusion.…”

“…The high density of carbon nuclear spins allows for spread of polarization to nearby aliphatic carbon atoms. The emissive signals, caused by the dominance of the TSM over the DD mechanism 19 , might suggest the absence of a strong impact of the high 13 C concentration on the spin dynamics. At 4.7 T the photo-CIDNP generation has been shown to be very efficient in RCs of natural isotope abundance 3 .…”

“…The latter is presumably driven by spin-diffusion. For studying primary nuclear hyperpolarization prior to any secondary spin-diffusion processes occurring on millisecond time-scales, we employed laser-flash experiments for time-resolved generation of nuclear hyperpolarization 13 .…”

“…carbon-proton decoupling 23 at a temperature of 222 K. The optimum length of the (π/2) carbon pulse, determined on uniformly 13 C labelled histidine, is ~ 6.3 µs at a strength of -3 dB. The rotational frequency for MAS was 8 kHz.…”

“…Alternatively, it might be that the nuclear polarization occurs undisturbed but dissipates into the strongly coupled network of 13 C-13 C interactions. In an attempt to shed light on this question, we studied a fully labeled bacterial RC sample, entirely labeled at all 13 …”