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Incorporation of 2,3-Disubstituted-1,4-Naphthoquinones into the A1 Binding Site of Photosystem I Studied by EPR and ENDOR Spectroscopy

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Abstract

Transient electron paramagnetic resonance and pulsed electron-nuclear double resonance (ENDOR) spectra of the state \( P_{700}^{ \cdot + } A_{1}^{ \cdot - } \) in photosystem I containing a series of non-native naphthoquinones (NQs) are presented. Previous studies have shown that quinones bind to the A1 site with only one of their carbonyl groups H-bonded to the protein and that the asymmetric H-bond produces an odd alternant distribution of the spin density within the quinone. It is known that the native phylloquinone binds with its methyl group meta and its phytyl tail ortho to the H-bonded carbonyl. Monosubstituted NQs with short alkyl chains have been found to bind preferentially with their alkyl side groups meta to the H-bonded carbonyl. The selectivity of the binding site toward methyl and short chain substituents is studied by incorporating disubstituted NQs that have a methyl group at the 2-position and a short chain at the 3-position of the quinone ring. The hyperfine couplings (hfcs) of the methyl group protons are sensitive to the spin density distribution on the quinone and are used to deduce the position of the methyl group relative to the H-bonded carbonyl. The measured methyl proton hfcs indicate that the disubstituted quinones bind exclusively with their methyl group in the meta position relative to the H-bonded carbonyl and no evidence for binding with the methyl group in the ortho position is found. The disubstituted quinones have also been chosen to study the effect of electron withdrawing substituents on the spin density distribution. When the short chain contains electronegative atoms such as sulfur or chlorine, the methyl proton hfcs of the quinone in the A1 binding site are found to be significantly larger than those of 2-methyl-1,4-naphthoquinone and phylloquinone in the same environment. Solution ENDOR measurements of the quinone radical anions in isopropanol and density functional theory (DFT) calculations in vacuo show that this increase in the hfcs is mostly intrinsic to the quinones due to the electron-withdrawing ability of the short chain and is not a result of differences in the binding to the protein. The DFT calculations suggest that the main reason for the increased methyl proton hfcs is delocalization of the singly occupied molecular orbital onto the side chain, which leads to an increase of the spin density on the neighboring carbon, which carries methyl group.

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Acknowledgments

This article is dedicated to the memory of Dietmar Stehlik, mentor, scientist and friend. This work was supported by grants from the Natural Science and Engineering Research Council Canada to A.v.d.E. and T.D. and from the US National Science Foundation to J.H.G. (MCB-0519743), as well as by the Deutsche Forschungsgemeinschaft (Sfb 663, TP A7).

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Authors and Affiliations

  1. Department of Chemistry, Brock University, 500 Glenridge Ave., St. Catharines, ON, L2S 3A1, Canada

    Art van der Est, Branden Fonovic & Travis Dudding

  2. Department of Physics, Purdue University, 525 Northwestern Ave., West Lafayette, IN, 47907, USA

    Yulia Pushkar

  3. Max Planck Institute for Biophysical Chemistry, Am Faßberg 11, 37077, Göttingen, Germany

    Irina Karyagina

  4. Max-Planck-Institut für Bioanorganische Chemie, Stiftstrasse 34-36, 45470, Mülheim an der Ruhr, Germany

    Jens Niklas & Wolfgang Lubitz

  5. Department of Biochemistry and Molecular Biology and Department of Chemistry, The Pennsylvania State University, University Park, PA, 16802, USA

    John H. Golbeck

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  1. Art van der Est
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van der Est, A., Pushkar, Y., Karyagina, I. et al. Incorporation of 2,3-Disubstituted-1,4-Naphthoquinones into the A1 Binding Site of Photosystem I Studied by EPR and ENDOR Spectroscopy. Appl Magn Reson 37, 65–83 (2010). https://doi.org/10.1007/s00723-009-0047-x

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