Nuclear hyperpolarization in electron-transfer proteins: Revealing unexpected light-induced 15N signals with field-cycling magic-angle spinning NMR

Journal of Magnetic Resonance Open, vol. 21, pp. 100168

Abstract

• Field-dependent 15 N shuttle-MAS photo-CIDNP NMR of a flavoprotein and photosynthetic reaction center. • Unexpected polarization occurs in both proteins at low magnetic fields (1-Tesla range). • Analysis of solid-state photo-CIDNP mechanisms with DFT calculations. The solid-state photo-CIDNP (photo-chemically induced dynamic nuclear polarization) effect allows for nuclear hyperpolarization, i.e., non-Boltzmann nuclear spin population. The effect relies on the light-induced formation of a spin-correlated radical pair (SCRP) and has been observed in various photosynthetic reaction center (RC) proteins and flavin-containing light, oxygen, voltage (LOV) proteins. Both systems exhibit strongly enhanced NMR signals originating from the electron transfer partners. Here, we present experimental data on the magnetic field dependence of the 15 N solid-state photo-CIDNP effect in both phototropin LOV1 C57S from Chlamydomonas reinhardtii and the bacterial photosynthetic RC from Rhodobacter sphaeroides. Using a pneumatic field-cycling system, samples containing a frozen solution of the proteins are explored between 0.25 T and 9.4 T. Both systems yield hyperpolarized 15 N NMR signals across the entire magnetic field range originating from the electron transfer moieties. Also, in both systems, hyperpolarized signals from unexpected positions are detected between 1.0 T and 2.0 T: position N-1 of the flavin in the LOV1 protein and the τ-N of the axial magnesium-coordinating histidine of the donor. A first attempt to explain the occurrence of these unexpected signals based on quantum chemical calculations is presented.

Authors 8

1. Patrick Kurle-Tucholski

   Leipzig University

   Affiliation as printed

   Institut für Analytische Chemie, Universität Leipzig, Linnéstraße 3, 04103, Leipzig, Germany

2. Luca Gerhards corresponding

   Carl von Ossietzky Universität Oldenburg

   Affiliation as printed

   Institut für Physik, Carl-von-Ossietzky Universität Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26129, Oldenburg, Germany

3. Yonghong Ding

   Leipzig University

   Affiliation as printed

   Institut für Analytische Chemie, Universität Leipzig, Linnéstraße 3, 04103, Leipzig, Germany

4. Yunmi Kim

   Leipzig University

   Affiliation as printed

   Institut für Analytische Chemie, Universität Leipzig, Linnéstraße 3, 04103, Leipzig, Germany

5. Irina S. Anisimova

   Carl von Ossietzky Universität Oldenburg

   Affiliation as printed

   Institut für Physik, Carl-von-Ossietzky Universität Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26129, Oldenburg, Germany

6. A. Alia Aachen

   Leiden University · Leipzig University

   Affiliation as printed

   Institut für Medizinische Physik und Biophysik, Universität Leipzig, Härtelstr. 16-18, 04107, Leipzig, Germany

   Leiden Institute of Chemistry, Leiden University, Einsteinweg 55, Leiden, RA 2301, the Netherlands

7. Ilia A. Solov’yov

   Carl von Ossietzky Universität Oldenburg

   Affiliation as printed

   Center for Nanoscale Dynamics (CENAD), Carl von Ossietzky Universität, Carl-von-Ossietzky Str. 9-11, 26129, Oldenburg, Germany

   Institut für Physik, Carl-von-Ossietzky Universität Oldenburg, Carl-von-Ossietzky-Str. 9-11, 26129, Oldenburg, Germany

   Research Centre for Neurosensory Sciences, Carl von Ossietzky Universität, Carl-von-Ossietzky Str. 9-11, 26129, Oldenburg, Germany

8. Jörg Matysik corresponding

   Leipzig University

   Affiliation as printed

   Institut für Analytische Chemie, Universität Leipzig, Linnéstraße 3, 04103, Leipzig, Germany