Abstract
Quantum effects in biological systems have recently been studied extensively in the fields of quantum computing (QC) and quantum information processing (QIP). The focus of this review is on quantum coherences and entanglement properties created in natural photosynthesis, whose understanding may be crucial for achieving the remarkable efficiency of its excitation energy transfer. In the beginning, an overview of electron and energy transfer in photosynthetic reaction centers (RCs) and light-harvesting complexes (LHCs) is given. Then the physical aspects of spin-correlated radical pairs (SCRPs) are described, which are ubiquitous intermediates in a wide range of biochemical reactions. Examples are given mainly with relation to quantum coherences in RCs and LHCs, which persist at room temperature, since such long-lived quantum coherences are crucial for quantum information storage and manipulation. Where appropriate, experimental observations of quantum coherences in artificial molecular assemblies are also briefly surveyed. In the second part, site-directed spin-labeling and pulsed electron-electron double resonance (PELDOR or DEER) are described, which are becoming important techniques in QC/QIP.
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References
S. Barz, E. Kashefi, A. Broadbent, J.F. Fitzsimons, Z. Zeilinger, P. Walther, Demonstration of blind quantum computing. Science 335, 303–308 (2012)
B.P. Lanyon, C. Hempel, D. Nigg, M. Müller, R. Gerritsma, F. Zähringer, P. Schindler, J.T. Barreiro, M. Rambach, G. Kirchmair, M. Hennrich, P. Zoller, R. Blatt, C.F. Roos, Universal digital quantum simulation with trapped ions. Science 334, 57–60 (2011)
K.C. Nowack, M. Shafiei, M. Laforest, G.E.D.K. Prawiroatmodjo, L.R. Schreiber, C. Reichl, W. Wegscheider, L.M.K. Vandersypen, Single-shot correlations and two-qubit gate of solid-state spins. Science 333, 1269–1272 (2011)
X. Zhu, S. Saito, A. Kemp, K. Kakuyanagi, S. Karimoto, H. Nakano, W.J. Munro, Y. Tokura, M.S. Everitt, K. Nemoto, M. Kasu, N. Mizuochi, K. Semba, Coherent coupling of a superconducting flux qubit to an electron spin ensemble in diamond. Nature 478, 221–224 (2011)
G.D. Scholes, G.R. Fleming, A. Olaya-Castro, R. van Grondelle, Lessons from nature about solar light harvesting. Nat. Chem. 3, 763–774 (2011)
S. Lloyd, A quantum of natural selection. Nat. Phys. 5, 164–166 (2010)
N. Lambert, Y.N. Chen, Y.C. Cheng, C.M. Li, G.Y. Chen, F. Nori, Quantum biology. Nat. Phys. 9, 10–18 (2013)
P. Ball, The dawn of quantum biology. Nature 474, 272–274 (2011)
E. Romero, R. Augulis, V.I. Novoderezhkin, M. Ferretti, J. Thieme, D. Zigmantas, R. van Grondelle, Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat. Phys. 10, 676–682 (2014)
A. Ishizakia, G.R. Fleminga, Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc. Natl. Acad. Sci. U. S. A. 106, 17255–17260 (2009)
G.S. Schlau-Cohen, A. Ishizaki, T.R. Calhoun, N.S. Ginsberg, M. Ballottari, R. Bassi, G.R. Fleming, Elucidation of the timescales and origins of quantum electronic coherence in LHCII. Nat. Chem. 4, 389–395 (2012)
H. Lee, Y.C. Cheng, G.R. Fleming, Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316, 1462–1465 (2007)
G.S. Engel, T.R. Calhoun, E.L. Read, T.K. Ahn, T. Mančal, Y.C. Cheng, R.E. Blankenship, G.R. Fleming, Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007)
G. Panitchayangkoon, D. Hayes, K.A. Fransted, J.R. Caram, E. Harel, J. Wen, R.E. Blankenship, G.S. Engel, Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc. Natl. Acad. Sci. U. S. A. 107, 12766–12770 (2010)
E. Collini, C.Y. Wong, K.E. Wilk, P.M.G. Curmi, P. Brumer, G.D. Scholes, Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–647 (2010)
M. Mohseni, P. Rebentrost, S. Lloyd, A.A. Guzik, Environment-assisted quantum walks in photosynthetic energy transfer. J. Chem. Phys. 129, 174106 (2008)
M. Sarovar, A. Ishizaki, G.R. Fleming, K.B. Whaley, Quantum entanglement in photosynthetic light-harvesting complexes. Nat. Phys. 6, 462–467 (2010)
G.D. Scholes, Green quantum computers. Nat. Phys. 6, 402–403 (2010)
G. Panitchayangkoon, D.V. Voronine, D. Abramavicius, J.R. Caram, N.H.C. Lewis, S. Mukamel, G.S. Engel, Direct evidence of quantum transport in photosynthetic light-harvesting complexes. Proc. Natl. Acad. Sci. U. S. A. 108, 20908–20912 (2011)
E. Harel, G.S. Engel, Quantum coherence spectroscopy reveals complex dynamics in bacterial light harvesting complex 2 (LH2). Proc. Natl. Acad. Sci. U. S. A. 109, 706–711 (2012)
R. Hildner, D. Brinks, J.B. Nieder, R.J. Cogdell, N.F. van Hulst, Quantum coherent energy transfer over varying pathways in single light-harvesting complexes. Science 340, 1448–1451 (2013)
E. Collini, Spectroscopic signatures of quantum-coherent energy transfer. Chem. Soc. Rev. 42, 4932–4947 (2013)
D. Hayes, G.B. Griffin, G.S. Engel, Engineering coherence among excited states in synthetic heterodimer systems. Science 340, 1431–1434 (2013)
C.A. Rozzi, S.M. Falke, N. Spallanzani, A. Rubio, E. Molinari, D. Brida, M. Maiuri, G. Cerullo, H. Schramm, J. Christoffers, C. Lienau, Quantum coherence controls the charge separation in a prototypical artificial light-harvesting system. Nat. Commun. 4, 1602 (2013)
E. Collini, G.D. Scholes, Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323, 369–373 (2009)
S.M. Falke, C.A. Rozzi, D. Brida, M. Maiuri, M. Amato, E. Sommer, A. De Sio, A. Rubio, G. Cerullo, E. Molinari, C. Lienau, Coherent ultrafast charge transfer in an organic photovoltaic blend. Science 344, 1001–1005 (2014)
S. Gélinas, A. Rao, A. Kumar, S.L. Smith, A.W. Chin, J. Clark, T.S. van der Poll, G.C. Bazan, R.H. Friend, Ultrafast long-range charge separation in organic semiconductor photovoltaic diodes. Science 343, 512–516 (2014)
C.J. Brabec, N.S. Serdar Sariciftci, J.C. Hummelen, Plastic solar cells. Adv. Funct. Mater. 11, 15–26 (2001)
K.M. Salikhov, Potential of electron paramagnetic resonance to study Einstein-Podolsky-Rosen-Bohm pairs. Appl. Magn. Reson. 25, 261–276 (2003)
K.M. Salikhov, J.H. Golbeck, D. Stehlik, Quantum teleportation across a biological membrane by means of correlated spin pair dynamics in photosynthetic reaction centers. Appl. Magn. Reson. 31, 237–252 (2007)
Y.E. Kandrashkin, K.M. Salikhov, Numerical simulation of quantum teleportation across biological membrane in photosynthetic reaction centers. Appl. Magn. Reson. 37, 549–566 (2010)
T. Berthold, E.D. von Gromoff, S. Santabarbara, P. Stehle, G. Link, O.G. Poluektov, P. Heathcote, C.F. Beck, M.C. Thurnauer, G. Kothe, Exploring the electron transfer pathways in photosystem I by high-time-resolution electron paramagnetic resonance: observation of the B-side radical pair P700 +A1B − in whole cells of the deuterated green alga chlamydomonas reinhardtii at cryogenic temperatures. J. Am. Chem. Soc. 134, 5563–5576 (2012)
S. Santabarbara, I. Kuprov, W.V. Fairclough, S. Purton, P.J. Hore, P. Heathcote, M.C.W. Evans, Bidirectional electron transfer in photosystem I: determination of two distances between P700 + and A1 − in spin-correlated radical pairs. Biochemistry 44, 2119–2128 (2005)
P.J. Hore, D.A. Hunter, C.D. McKie, A.J. Hoff, Electron paramagnetic resonance of spin-correlated radical pairs in photosynthetic reactions. Chem. Phys. Lett. 137, 495–500 (1987)
R. Bitt, G. Kothe, Transient EPR of radical pairs in photosynthetic reaction centers prediction of quantum beats. Chem. Phys. Lett. 177, 547–553 (1991)
M. Gierer, A. van der Est, D. Stehlik, Transient EPR of weakly coupled spin-correlated radical pairs in photosynthetic reaction centres: increased spectral resolution from nutation analysis. Chem. Phys. Lett. 186, 238–247 (1991)
G. Kothe, S. Weber, R. Bitt, E. Ohmes, M.C. Thurnauer, J.R. Norris, Transient EPR of light-induced radical pairs in plant photosystem I: observation of quantum beats. Chem. Phys. Lett. 186, 474–480 (1991)
G. Zwanenburg, P.J. Hore, EPR of spin-correlated radical pairs. Analytical treatment of selective excitation including zero-quantum coherence. Chem. Phys. Lett. 203, 65–74 (1993)
G. Kothe, S. Weber, E. Ohmes, M.C. Thurnauer, J.R. Norris, High time resolution electron paramagnetic resonance of light-induced radical pairs in photosynthetic bacterial reaction centers: observation of quantum beats. J. Am. Chem. Soc. 114, 1129–1134 (1994)
Z. Wang, J. Tang, J. Norris, The time development of the magnetic moment of correlated radical pairs. J. Magn. Reson. 97, 322–334 (1992)
G. Kothe, S. Weber, E. Ohmes, M.C. Thurnauer, J.R. Norris, Transient EPR of light-induced spin-correlated radical pairs: manifestation of zero quantum coherence. J. Phys. Chem. 98, 2706–2712 (1994)
K. Maekawa, S. Nakazawa, H. Atsumi, D. Shiomi, K. Sato, M. Kitagawa, T. Takui, K. Nakatani, Programmed assembly of organic radicals on DNA. Chem. Commun. 46, 1247–1249 (2010)
H. Atsumi, K. Maekawa, S. Nakazawa, D. Shiomi, D. Sato, M. Kitagawa, T. Takui, K. Nakatani, Tandem arrays of TEMPO and nitronyl nitroxide radicals with designed arrangements on DNA. Chem. Eur. J. 18, 178–183 (2012)
Y. Morita, Y. Yakiyama, S. Nakazawa, T. Murata, T. Ise, D. Hashizume, D. Shiomi, K. Sato, M. Kitagawa, K. Nakasuji, T. Takui, Triple-stranded metallo-helicates addressable as Lloyd’s electron spin qubits. J. Am. Chem. Soc. 132, 6944–6946 (2010)
C.R. Timmel, J.R. Harmer (eds.), Structural Information from Spin-Labels and Intrinsic Paramagnetic Centers in the Biosciences. Structure and Bonding, vol. 152 (Springer, Berlin, 2014), pp. 1–332
S. Nakazawa, S. Nishida, T. Ise, T. Yoshino, N. Mori, R.D. Rahimi, K. Sato, Y. Morita, K. Toyota, D. Shiomi, M. Kitagawa, H. Hara, P. Carl, P. Höfer, T. Takui, A synthetic two-spin quantum bit: g-engineered exchange-coupled biradical designed for controlled-NOT gate operations. Angew. Chem. Int. Ed. 51, 9860–9864 (2012)
K. Sato, S. Nakazawa, R. Rahimi, T. Ise, S. Nishida, T. Yoshino, N. Mori, K. Toyota, D. Shiomi, Y. Yakiyama, Y. Morita, M. Kitagawa, K. Nakasuji, M. Nakahara, H. Hara, P. Carl, P. Höfer, T. Takui, Molecular electron-spin quantum computers and quantum information processing: pulse-based electron magnetic resonance spin technology applied to matter spin-qubits. J. Mater. Chem. 19, 3739–3754 (2009)
P. Jordan, P. Fromme, H.T. Witt, O. Klukas, W. Saenger, N. Krauss, Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. Nature 411, 909–917 (2001)
M.V. Fedin, E.G. Bagryanskaya, H. Matsuoka, S. Yamauchi, S.L. Veber, K.Y. Maryunina, E.V. Tretyakov, V.I. Ovcharenko, R.Z. Sagdeev, W-band time-resolved electron paramagnetic resonance study of light-induced spin dynamics in copper-nitroxide-based switchable molecular magnets. J. Am. Chem. Soc. 134, 16319–16326 (2012)
M. Tanabe, H. Matsuoka, Y. Ohba, S. Yamauchi, K. Sugisaki, K. Toyota, K. Sato, T. Takui, I. Goldberg, I. Saltsman, Z. Gross, Time-resolved electron paramagnetic resonance and phosphorescence studies of the lowest excited triplet states of Rh(III) corrole complexes. J. Phys. Chem. A 116, 9662–9673 (2012)
J. Fujisawa, Y. Ohba, S. Yamauchi, A time-resolved electron paramagnetic resonance study of excited triplet porphyrins in fluid solution. J. Am. Chem. Soc. 119, 8736–8737 (1997)
H. Matsuoka, L. Utschig, O. Poluektov, E. Ohmes, Y. Ohba, M.C. Thurnauer, G. Kothe, S. Yamauchi, W-band cw and pulse EPR studies of photosystem I reaction center, in 7th Asia-Pacific EPR/ESR Symposium 2010, p. 110
Y. Umena, K. Kawakami, J.R. Shen, N. Kamiya, Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–61 (2011)
N. Kamiya, J.R. Shen, Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 Å resolution. Proc. Natl. Acad. Sci. U. S. A. 100, 98–103 (2003)
H. Matsuoka, J.R. Shen, A. Kawamori, K. Nishiyama, Y. Ohba, S. Yamauchi, Proton-coupled electron-transfer processes in photosystem II probed by highly resolved g-anisotropy of redox-active tyrosine Yz. J. Am. Chem. Soc. 133, 4655–4660 (2011)
H. Matsuoka, K. Furukawa, T. Kato, H. Mino, J.R. Shen, A. Kawamori, g-Anisotropy of the S2-state manganese cluster in single crystals of cyanobacterial photosystem II studied by w-band electron paramagnetic resonance spectroscopy. J. Phys. Chem. B 110, 13242–13247 (2006)
A. Kawamori, J.R. Shen, H. Mino, K. Furukawa, H. Matsuoka, T. Kato, in Photosynthesis: Fundamental Aspects to Global Perspectives, ed. by A. van der Est, D. Bruce (Allen Press, Lawrence, 2005), pp. 406–408
D. Leupold, B. Voigt, W. Beenken, H. Stiel, Pigment-protein architecture in the light-harvesting antenna complexes of purple bacteria: does the crystal structure reflect the native pigment-protein arrangement? FEBS Lett. 480, 73–78 (2000)
P. Atkins, J. de Paula, Atkins’ Physical Chemistry, 8th edn. (Oxford University Press, Oxford, 2006), p. 856
T. Ritz, P. Thalau, J.B. Phillips, R. Wiltschko, W. Wiltschko, Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004)
K. Maeda, K.B. Henbest, F. Cintolesi, I. Kuprov, C.T. Rodgers, P.A. Liddell, D. Gust, C.R. Timmel, P.J. Hore, Chemical compass model of avian magnetoreception. Nature 453, 387–390 (2008)
G. Link, T. Berthold, M. Bechtold, J.U. Weidner, E. Ohmes, J. Tang, O. Poluektov, L. Utschig, S.L. Schlesselman, M.C. Thurnauer, G. Kothe, Structure of the P700 +A1 − radical pair intermediate in photosystem I by high time resolution multifrequency electron paramagnetic resonance: analysis of quantum beat oscillations. J. Am. Chem. Soc. 123, 4211–4222 (2001)
T. Takui, S. Nakazawa, H. Matsuoka, K. Furukawa, K. Sato, D. Shiomi, Molecule-based exchange-coupled high-spin clusters: conventional high-field/high-frequency and pulse-based electron spin resonance of molecule-based magnetically coupled systems, in EPR of Free Radicals in Solids II: Trends in Method and Applications, ed. by A. Lund, M. Shiotani, 2nd edn. (Springer, Dordrecht, 2012), pp. 71–162
H. Matsuoka, K. Sato, D. Shiomi, T. Takui, 2D electron spin transient nutation spectroscopy of lanthanoid ion Eu2+(8S7/2) in a CaF2 single crystal on the basis of FT-pulsed electron spin resonance spectroscopy: transition moment spectroscopy. Appl. Magn. Reson. 23, 517–538 (2003)
A. Furusawa, P. van Loock, Quantum Teleportation and Entanglement: A Hybrid Approach to Optical Quantum Information Processing (Wiley-VCH, Weinheim, 2011)
H. Matsuoka, Toward Manipulation of Quantum Spin Information in Biomolecules, Quantum Cybernetics Newsletter, vol. 12, pp. 15, (2014)
C. Altenbach, T. Marti, H.G. Khorana, W.L. Hubbell, Transmembrane protein structure: spin labeling of bacteriorhodopsin mutants. Science 248, 1088–1092 (1990)
O.H. Griffith, H.M. McConnell, A nitroxide-maleimide spin label. Proc. Natl. Acad. Sci. U. S. A. 55, 8–11 (1966)
S. Ogawa, H.M. McConnell, Spin label study of hemoglobin conformations in solution. Proc. Natl. Acad. Sci. U. S. A. 58, 19–26 (1967)
L.J. Berliner, J. Grundwald, H.O. Hankovszky, K. Hideg, A novel reversible thiol-specific spin label: papain active site labeling and inhibition. Anal. Biochem. 119, 450–455 (1982)
M.R. Fleissner, E.M. Brustad, T. Kálái, C. Altenbach, D. Cascio, F.B. Peters, K. Hideg, S. Peuker, P.G. Schultz, W.L. Hubbell, Site-directed spin labeling of a genetically encoded unnatural amino acid. Proc. Natl. Acad. Sci. U. S. A. 106, 21637–21642 (2009)
M.J. Schmidt, J. Borbas, M. Drescher, D. Summerer, A genetically encoded spin label for electron paramagnetic resonance distance measurements. J. Am. Chem. Soc. 136, 1238–1241 (2014)
G. Hagelueken, F.G. Duthie, N. Florin, E. Schubert, O. Schiemann, Expression, purification and spin labelling of the ferrous iron transporter FeoB from Escherichia coli BL21 for EPR studies. Protein Expr. Purif. 114, 30–36 (2015)
A.J. Fielding, M.G. Concilio, G. Heaven, M.A. Hollas, New developments in spin labels for pulsed dipolar EPR. Molecules 19, 16998–17025 (2014)
T. Kalai, W. Hubbell, K. Hideg, Click reactions with nitroxides. Synthesis 2009, 1336–1340 (2009)
I. Krstic, R. Hänsel, O. Romainczyk, J.W. Engels, V. Dötsch, T.F. Prisner, Long-range distance measurements on nucleic acids in cells by pulsed EPR spectroscopy. Angew. Chem. Int. Ed. 50, 5070–5074 (2011)
A.P. Jagtap, I. Krstic, N.C. Kunjir, R. Hänsel, T.F. Prisner, S.T. Sigurdsson, Sterically shielded spin labels for in-cell EPR spectroscopy: analsis of stability in reducing environments. Free Radic. Res. 49, 78–85 (2015)
I.A. Kirilyuk, A.A. Bobko, I.A. Grigorev, V.V. Khramtsov, Synthesis of the tetraethyl substituted pH-sensitive nitroxides of imidazole series with enhanced stability towards reduction. Org. Biomol. Chem. 2, 1025–1030 (2004)
S. Schreier, J.C. Bozelli, N. Marin, R.F.F. Vieira, C.R. Nakaie, The spin label amino acid TOAC and its use in studies of peptides: chemical, physicochemical, spectroscopic, and conformational aspects. Biophys. Rev. 4, 45–66 (2012)
N. Florin, O. Schiemann, G. Hagelueken, High-resolution crystal structure of spin labelled (T21R1) azurin from Pseudomonas aeruginosa: a challenging structural benchmark for in silico spin labelling algorithms. BMC Struct. Biol. 14(16), 1–10 (2014)
L. Urban, H.J. Steinhoff, Hydrogen bonding to the nitroxide of protein bound spin labels. Mol. Phys. 111, 2873–2881 (2013)
M.R. Fleissner, M.D. Bridges, E.K. Brooks, D. Cascio, T. Kalai, K. Hideg, W.L. Hubbell, Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 108, 16241–16246 (2011)
G.W. Reginsson, N.C. Kunjir, S.T. Sigurdsson, O. Schiemann, Trityl radicals: spin labels for nanometer distance measurements. Chem. Eur. J. 18, 13580–13584 (2012)
N.C. Kunjir, G.W. Reginsson, O. Schiemann, S.T. Sigurdsson, Measurements of short distances between trityl spin labels with CW EPR, DQC and PELDOR. Phys. Chem. Chem. Phys. 15, 19673–19685 (2013)
Z. Yang, Y. Liu, P. Borbat, J.L. Zweier, J.H. Freed, W.L. Hubbell, Pulsed ESR dipolar spectroscopy for distance measurements in immobilized spin labeled proteins in liquid solution. J. Am. Chem. Soc. 134, 9950–9952 (2012)
D. Goldfarb, Gd3+ spin labeling for distance measurements by pulse EPR spectroscopy. Phys. Chem. Chem. Phys. 16, 9685–9699 (2014)
M. Qi, A. Gross, G. Jeschke, A. Godt, M. Drescher, Gd(III)-PyMTA label is suitable for in-cell EPR. J. Am. Chem. Soc. 136, 15366–15378 (2014)
E. Matalon, T. Huber, G. Hagelueken, B. Graham, A. Feintuch, V. Frydman, G. Otting, D. Goldfarb, Angew. Chem. Int. Ed. 52, 11831–11834 (2013)
H. Yagi, D. Banerjee, B. Graham, T. Huber, D. Goldfarb, O. Gottfried, J. Am. Chem. Soc. 133, 10418–10421 (2011)
H.Y. Ching, P. Demay-Drouhard, H.C. Bertrand, C. Policar, L.C. Tabares, S. Un, Nanometric distance measurements between Mn(II)DOTA centers. Phys. Chem. Chem. Phys. 17(36), 23368–23377 (2015). doi:10.1039/c5cp03487f
T.F. Cunningham, M.R. Putterman, A. Desai, W.S. Horne, S. Saxena, The double histidine Cu(II)-binding motif: a highly rigid, site-specific spin probe for ESR distance measurements. Angew. Chem. Int. Ed. 54, 6330–6334 (2015)
A.V. Astashkin, H. Hara, A. Kawamori, The pulsed electro-electron double-resonance and 2-spin echo study of the oriented oxygen-evolving and mn-depleted preparations of photosystem-II. J. Chem. Phys. 108, 3805–3812 (1998)
C. Elsässer, M. Brecht, R. Bittl, Pulsed electron-electron double resonance on multinuclear metal clusters: assignment of spin projection factors based on the dipolar interaction. J. Am. Chem. Soc. 124, 12606–12611 (2002)
Z. Yang, M. Kurpiewski, M. Ji, J.E. Townsend, P. Mehta, L. Jen-Jacobson, S. Saxena, ESR spectroscopy identifies inhibitory Cu(II) sites in a DNA modifying enzyme to reveal determinants of catalytic specificity. Proc. Natl. Acad. Sci. U. S. A. 109, E993–E1000 (2012)
D. Abdullin, N. Florin, G. Hagelueken, O. Schiemann, EPR-based approach for the localization of paramagnetic metal ions in biomolecules. Angew. Chem. Int. Ed. 54, 1827–1831 (2015)
S. Milikisyants, F. Scarpelli, M.G. Finiguerra, M. Ubbink, M.A. Huber, Pulsed EPR method to determine distances between paramagnetic centers with strong spectral anisotropy and radicals: the dead-time free RIDME sequence. J. Magn. Reson. 201, 48–56 (2009)
D. Abdullin, F. Duthie, A. Meyer, E.S. Müller, G. Hagelueken, O. Schiemann, Comparison of PELDOR and RIDME for distance measurements between nitroxides and low spin Fe(III) ions. J. Phys. Chem. B 119(43), 13534–13542 (2015). doi:10.1021/acs.jpcb.5b02118
A.V. Astashkin, Mapping the structure of metalloproteins with RIDME. Methods Enzymol. 563, 251–284 (2015). doi:10.1016/bs.mie.2015.06.031
R. Ward, O. Schiemann, Structural information from oligonucleotides. Struct. Bond. 152, 249–282 (2014)
P.Z. Quin, I.S. Haworth, Q. Cai, A.K. Kusnetzow, G.P. Grant, E.A. Price, G.Z. Sowa, A. Popova, B. Herreos, H. He, Measuring nanometer distances in nucleic acids using a sequence-independent nitroxide probe. Nat. Protoc. 2, 2354–2365 (2007)
O. Schiemann, A. Weber, T.E. Edwards, T.F. Prisner, S.T. Sigurdsson, Nanometer distance measurements on RNA using PELDOR. J. Am. Chem. Soc. 125, 3434–3435 (2003)
N. Piton, Y. Mu, G. Stock, T.F. Prisner, O. Schiemann, J.W. Engels, Base-specific spin labeling of RNA for structure determination. Nucleic Acids Res. 35, 3128–3143 (2007)
C. Giordano, F. Fratini, D. Attanasio, L. Cellai, Preparation of spin-labeled 2-amino-dA, dA, dC and 5-methyl-dC phosphoramidites for the automatic synthesis of EPR active oligonucleotides. Synthesis 4, 565–572 (2001)
P. Ding, D. Wunnicke, H.J. Steinhoff, F. Seela, Site-directed spin-labeling of DNA by the azide-alkyne ‘click’ reaction: nanometer distance measurements on 7-deaza-2′-deoxyadenosin and 2′-deoxyuridine nitroxide conjugates spatially separated or linked to a ‘dA-dT’ base pair. Chem. Eur. J. 16, 14385–14396 (2010)
O. Schiemann, P. Cekan, D. Margraf, T.F. Prisner, S.T. Sigurdsson, Relative orientation of rigid nitroxides by PELDOR: beyond distance measurements in nucleic acids. Angew. Chem. Int. Ed. 48, 3292–3295 (2009)
G.W. Reginsson, S. Shelke, C. Rouillon, M.F. White, S.T. Sigurdsson, O. Schiemann, Protein-induced changes in DNA structure and dynamics observed with non-covalent site-directed spin-labelling and PELDOR. Nucleic Acids Res. 41(1), e11 (2013). doi:10.1093/nar/gks817
S.A. Shelke, S.T. Sigurdsson, Site-directed nitroxide spin labeling of biopolymers. Struct. Bond. 152, 121–162 (2014)
G.J. Shevlev, O.A. Krumkacheva, A.A. Lomzov, A.A. Kuzhelev, O.Y. Rogozhnikova, D.V. Trukhin, T.I. Troitskaya, V.M. Tormyshev, M.V. Fedin, D.V. Pyshnyi, E.G. Bagryanskaya, Physiological-temperature distance measurements in nucleic acids using triarylmethyl-based spin labels and pulsed dipolar EPR spectroscopy. J. Am. Chem. Soc. 136, 9874–9877 (2014)
X. Zhang, P. Cekan, S.T. Sigurdsson, P.Z. Qin, Studying RNA using site-directed spin-labeling and continuous-wave electron paramagnetic resonance spectroscopy. Methods Enzymol. 469, 303–328 (2009)
O. Schiemann, T.F. Prisner, Long-range distance determinations in biomacromolecules by EPR spectroscopy. Q. Rev. Biophys. 40, 1–53 (2007)
P. Schöps, P.E. Spindler, A. Marko, T.F. Prisner, Broadband spin echoes and broadband SIFTER in EPR. J. Magn. Reson. 250, 55–62 (2015)
A.D. Milov, K.M. Salikhov, M.D. Shirov, Application of ENDOR in electron-spin echo for paramagnetic center space distribution in solids. Fiz. Tverd. Tela 23, 975–982 (1981)
G. Jeschke, DEER distance measurements on proteins. Annu. Rev. Phys. Chem. 63, 419–446 (2012)
G.W. Reginsson, O. Schiemann, Pulsed electron-electron double resonance on biomacromolecules: beyond nanometer distance measurements. Biochem. J. 434, 353–363 (2011)
D. Margraf, P. Cekan, T. Prisner, S. Sigurdsson, O. Schiemann, Ferro- and antiferromagnetic exchange coupling constants in PELDOR spectra. Phys. Chem. Chem. Phys. 11, 6708–6714 (2009)
K. Ayabe, K. Sato, S. Nakazawa, S. Nishida, K. Sugisaki, T. Ise, Y. Morita, K. Toyota, D. Shiomi, M. Kitagawa, S. Suzuki, K. Okada, T. Takui, Pulsed electron spin nutation spectroscopy for weakly exchange-coupled multi-spin molecular systems with nuclear hyperfine couplings: a general approach to bi- and triradicals and determination of their spin dipolar and exchange interactions. Mol. Phys. 111, 2767–2787 (2013)
Acknowledgments
We gratefully acknowledge financial support of the Deutsche Forschungsgemeinschaft (DFG) through the Collaborative Research Center SFB813 “Chemistry at Spin Centers.” This work was also supported by Grants-in-Aid for Scientific Research (C) and Scientific Research on Innovative Areas, “Quantum Cybernetics,” MEXT, Japan.
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Matsuoka, H., Schiemann, O. (2016). Molecular Spins in Biological Systems. In: Takui, T., Berliner, L., Hanson, G. (eds) Electron Spin Resonance (ESR) Based Quantum Computing. Biological Magnetic Resonance, vol 31. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-3658-8_3
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