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D‐Band EPR and ENDOR Spectroscopy of 15N‐Labeled Photosystem I

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Abstract

For billions of years, nature has optimized the photosynthetic machinery that converts light energy into chemical energy. Key primary reactions of photosynthesis occur in large membrane protein–cofactor complexes. The light-induced sequential electron transfer reactions occur through a chain of donor/acceptor cofactors embedded in the protein matrix resulting in a long-lived transmembrane charge-separated state. EPR is the method of choice to study electron transfer and the interaction of protein environment with redox-active cofactors. However, the spectra of organic cofactor radicals typically are not fully resolved and severely overlap at conventional X-band EPR. Even at Q-band EPR, this overlap is present and often a serious problem. As a result, there is a large variation of the reported EPR data and limited understanding of electronic structures of several redox-active cofactors. These serious problems can often be overcome by the excellent spectral resolution provided by high-frequency EPR (HF EPR). Here, we study the electronic structure of the primary electron donor P700 and the secondary electron acceptor A1 of Photosystem I (PSI) using 130 GHz (D-band) EPR and Electron–Nuclear-Double-Resonance (ENDOR) spectroscopy. PSI was isotopically labeled with 15N (I = ½) to avoid quadrupolar interactions in the most abundant nitrogen isotope 14N (I = 1) and simplify the ENDOR spectra. ENDOR spectroscopy is central for determining the hyperfine coupling of nitrogen atoms of the two chlorophyll molecules comprising oxidized P700 and the involvement of protein nitrogen atoms with reduced A1. While HF ENDOR of A1− allows identification of two nitrogen atoms, HF ENDOR of P700+ still does not permit unique assignment of the recorded hyperfine couplings.

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Acknowledgements

The authors gratefully acknowledge support by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences, through Argonne National Laboratory under Contract No. DE-AC02-06CH11357. The authors acknowledge Arlene Wagner for growth of perdeuterated and 15N-labeled cyanobacteria.

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  1. Chemical Sciences and Engineering Division, Argonne National Laboratory, 9700 S. Cass Ave., Lemont, IL, 60439, USA

    Jens Niklas, Udita Brahmachari, Lisa M. Utschig & Oleg G. Poluektov

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Niklas, J., Brahmachari, U., Utschig, L.M. et al. D‐Band EPR and ENDOR Spectroscopy of 15N‐Labeled Photosystem I. Appl Magn Reson 53, 1175–1193 (2022). https://doi.org/10.1007/s00723-021-01438-8

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