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Soft Dynamic Confinement of Membrane Proteins by Dehydrated Trehalose Matrices: High-Field EPR and Fast-Laser Studies

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Abstract

In memory of the 85th birthday of Yakov S. Lebedev (Moscow), who died in 1996, we start this Review on soft-glass matrix effects in donor–acceptor complexes with an appreciation of his pioneering work on high-field EPR spectroscopy on tribochemically generated donor–acceptor complexes. The mechanochemical activation of polycrystalline mixtures of porphyrins (and other donors) and quinone acceptors was found to produce large concentrations of triplet donor molecules and donor–acceptor radical pairs with unusual stability. The Review is continued with reporting on W-band high-field EPR and fast-laser studies on disaccharide matrix effects on structure and dynamics of donor–acceptor protein complexes related to photosynthesis, including the non-oxygenic bacterial reaction center (RC) and the oxygenic RCs Photosystem I (PS I) and Photosystem II (PS II, preliminary results). Some organisms can survive complete dehydration and high temperatures by adopting an anhydrobiotic state in which the intracellular medium contains large amounts of disaccharides, in particular trehalose and sucrose. Trehalose is most effective in protecting biostructures, both in vivo and in vitro. To clarify the molecular mechanisms of disaccharide bioprotection, structure and dynamics of sucrose and trehalose matrices at different controlled hydration levels were probed by perdeuterated nitroxide spin labels and native cofactor intermediates in their charge-separated states. Trehalose forms a homogeneous amorphous phase in which the hosted molecules are uniformly distributed. Notably, their rotational mobility at room temperature is dramatically impaired by the trehalose H-bonding network confinement to an extent that in normal protein–matrix systems is only observed at low temperatures around 150 K. From the experimental results, formation of an extended H-bonding network of trehalose with protein molecules is inferred, involving both bulk and local water molecules. The H-bond network extends homogeneously over the whole matrix integrating and immobilizing the hosted protein. Taken together, these observations suggest that in photosystems, such as bacterial RCs and PS I complexes, of different size and complexity regarding subunit composition and oligomeric organization, the molecular configuration of the cofactors involved in the primary processes of charge separation is not significantly distorted by incorporation into trehalose glass, even under extensive dehydration. By means of pulsed W-band high-field multiresonance EPR spectroscopies, such as ELDOR-detected NMR and ENDOR, in conjunction with using isotope labeled water (D2O and H217O), the biologically important issue of sensing and quantification of local water in proteins is addressed. The bacterial RC embedded into the trehalose glass matrix is used as model system. The two native radical cofactor ions of the primary electron donor and acceptor as well as an artificial nitroxide spin label site-specifically attached to the protein surface are studied in the experiments. The three paramagnetic reporter groups probe distinctly different local environments. They sense water molecules via their magnetic hyperfine and quadrupole interactions with either deuterons or 17O nuclei. It is shown that by using oxygen-17 labeled water, quantitative conclusions can be drawn differentiating between local and bulk water. It is concluded that dry trehalose operates as anhydrobiotic protein stabilizer by means of selective changes in the first solvation shell of the protein upon trehalose–matrix dehydration with subsequent changes in the hydrogen-bonding network. Such changes usually have an impact on the global function of a biological system. Finally, preliminary results of optical and W-band EPR experiments on the extremolytes ectoine and its derivative hydroxyectoine are reported; these compounds appear to share several stress-protecting properties with trehalose in terms of stabilizing protein matrices. For instance, they display remarkable stabilizing capabilities towards sensitive proteins and enzymes with respect to freeze-thawing, heat-treatment, and freeze-drying procedures. Moreover, hydroxyectoine is a good glass-forming compound and exhibits a remarkable bioprotective effect against desiccation and heat denaturation of functional protein complexes.

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Acknowledgements

Financial support from MIUR of Italy (RFO2018) is gratefully acknowledged by F. F. and G. V. This work was supported by the Russian Foundation for Basic Research (Grant 17-00-00201 to A. Yu. S.). The Max-Planck-Gesellschaft and the Cluster of Excellence RESOLV (EXC 1069), funded by the Deutsche Forschungsgemeinschaft (DFG), supported this work. K. M. gratefully acknowledges sustaining support by the Free University Berlin.

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Authors and Affiliations

  1. Department of Physics, Free University Berlin, Berlin, Germany

    Klaus Möbius

  2. Faculty of Physics, Technical University Dortmund, Dortmund, Germany

    Anton Savitsky

  3. Department of Chemistry “Giacomo Ciamician”, University of Bologna, Bologna, Italy

    Marco Malferrari

  4. Laboratory of Biochemistry and Molecular Biophysics, Department of Pharmacy and Biotechnology, FaBiT, University of Bologna, Bologna, Italy

    Francesco Francia & Giovanni Venturoli

  5. A.N. Belozersky Institute of Physical-Chemical Biology, Lomonosov Moscow State University, Moscow, Russia

    Mahir D. Mamedov & Alexey Yu. Semenov

  6. N.N. Semenov Federal Research Center for Chemical Physics, Russian Academy of Sciences, Moscow, Russia

    Alexey Yu. Semenov

  7. Max-Planck-Institute for Chemical Energy Conversion, Mülheim (Ruhr), Germany

    Wolfgang Lubitz

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Möbius, K., Savitsky, A., Malferrari, M. et al. Soft Dynamic Confinement of Membrane Proteins by Dehydrated Trehalose Matrices: High-Field EPR and Fast-Laser Studies. Appl Magn Reson 51, 773–850 (2020). https://doi.org/10.1007/s00723-020-01240-y

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