The primary energy conversion steps of bacterial and plant photosynthesis proceed via light-induced radical pairs as short-lived intermediates. Time-resolved EPR experiments of the photosynthetic reaction centers monitor the key charge separated state between the oxidized electron donor and reduced acceptor P•+ 700A1 •– of Photosystem I. The observed EPR spectra of P•+ 700A1 •– are indicative of a spin-correlated radical pair that is populated from the excited singlet state of the primary electron donor. Importantly, the spin-correlated radical pair nature of the charge-separated state is a common feature of all photosynthetic reaction centers, which gives rise to several interesting spin-phenomena such as quantum beats, observed at short delay times after optical excitation. In this chapter we present details of the quantum beat phenomena studied by high-time resolution transient and pulsed EPR of Photosystem I reaction centers. The understanding and analysis of the quantum beat oscillations in combination with high-field EPR allows us to obtain the three-dimensional structure of P•+ 700A1 •– as well as its arrangement in the membrane. We expect that this is of general interest, because the detailed structure of radical pair intermediates can be determined on a nanosecond time scale. In addition, by monitoring the quantum beat oscillations with a pulsed EPR approach, we shed new light on the electronic structure of the oxidized primary electron donor, P•+ 700.
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References
Angerhofer A and Bittl R (1996) Radicals and radical pairs in photosynthesis. Photochem Photobiol 63: 11–38
Atkins PW and McLauchlan KA (1973) Electron spin polarization. In: Lepley AR and Closs GL (eds) Chemically Induced Magnetic Polarization, pp 41–93. John Wiley & Sons, New York
Berthold T, Bechtold M, Heinen U, Link G, Poluektov O, Utschig L, Tang J, Thurnauer MC and Kothe G (1999) Magnetic field induced orientation of photosynthetic reaction centers as revealed by time-resolved W-Band EPR of spin-cor related radical pairs. J Phys Chem B 103: 10733–10736
Bittl R and Kothe G (1991) Transient EPR of radical pairs in photosynthetic reaction centers: Prediction of quantum beats. Chem Phys Lett 177: 547–553
Bittl R, van der Est A, Kamlowski A, Lubitz W and Stehlik •–D (1994) Time-resolved EPR of the radical pair P•+ in 865QA bacterial reaction centers. Obser vation of transient nutations, quantum beats and envelope modulation effects. Chem Phys Lett 226: 349–358
Borovykh IV, Kulik LV, Dzuba SA and Hoff AJ (2001) Selective excitation in pulsed EPR of spin-cor related radical pairs: Electron-electron interactions, zero-, single-, and double-quantum relaxation and spectral diffusion. Chem Phys Lett 338: 173–179
Brettel K (1997) Electron transfer and ar rangement of the redox cofactors in Photosystem I. Biochim Biophys Acta 1318: 322–373
Buckley CD, Hunter DA, Hore PJ and McLauchlan KA (1987) ESR of spin-cor related radical pairs. Chem Phys Lett 135: 307–312
Closs GL, Forbes MDE and Nor ris JR (1987) Spin-polarized electron paramagnetic resonance spectra of radical pairs in micelles. Observation of electron spin-spin interactions. J Phys Chem 91: 3592–3599
Dzuba SA, Gast P and Hoff AJ (1995) ESEEM study of spin-spin interactions in spin-polarised P•+QA •- pairs in the photosynthetic purple bacterium Rhodobacter sphaeroides R26. Chem Phys Lett 236: 595–602
Dzuba SA, Bosch MK and Hoff AJ (1996) Electron spin echo detection of quantum beats and double-quantum coherence in spin-correlated radical pairs of protonated photosynthetic reaction centers. Chem Phys Lett 248: 427–433
Furrer R and Thurnauer MC (1981) Nanosecond time resolution in EPR transient nutation spectroscopy of triplet states. Chem Phys Lett 79: 28–33
Furrer R and Thurnauer MC (1983) Resolution of signals attributed to Photosystem I primary reactants by time-resolved EPR at K band. FEBS Lett 153: 399–403
Furrer R, Fujara F, Lange C, Stehlik D, Vieth H-M and Vollmann W (1980) Transient EPR nutation signals in excited triplet states. Chem Phys Lett 75: 332–339
Geacintov NE, van Nostrand F, Becker JF and Tinkel JB (1972) Magnetic field induced orientation of photosynthetic systems. Biochim Biophys Acta 267: 65–79
Heinen U, Berthold T, Kothe G, Stavitski E, Galili T, Levanon H, Wiederrecht G and Wasielewski MR (2002) High time resolution Q-band EPR study of sequential electron transfer in a triad oriented in a liquid crystal. J Phys Chem A 106: 1933–1937
Heinen U, Poluektov O, Stavitski E, Berthold T, Ohmes E, Schlesselman SL, Golecki JR, Moro GJ, Levanon H, Thurnauer MC and Kothe G (2004a) Magnetic fi eld induced orientation of photosynthetic reaction centers as revealed by time-resolved D-band EPR of spin-cor related radical pairs. II. Field dependence of the alignment. J Phys Chem B 108: 4498–9504
Heinen U, Golecki JR, Poluektov O, Berthold T, Schlesselman SL, Frezzato D, Ohmes E, Moro GJ, Thurnauer MC and Kothe G (2004b) Magnetic field induced orientation of photosynthetic reaction centers as revealed by time-resolved W-band EPR of spin-correlated radical pairs. Development of a molecular model. Appl Magn Reson 26: 99–115
Hoff AJ (1984) Electron spin polarization of photosynthetic reactants. Q Rev Biophys 17: 153–282
Hoff AJ and Deisenhofer J (1997) Photophysics of photosynthesis. Structure and spectroscopy of reaction centers of pur ple bacteria. Phys Rep 287: 1–248
Isaacson RA, Lendzian F, Abresch EC, Lubitz W and Feher G (1995) Electronic str ucture of QA- in reaction centers from Rhodobacter sphaeroides. I. Electron Paramagnetic Resonance in single crystals. Biophys J 69: 311–322
Jeschke G (1997) Electron-electron-nuclear three-spin mixing in spin-cor related radical pairs. J Chem Phys 106: 10072–10086
Jeschke G and Matysik J (2003) A reassessment of the origin of photochemically induced dynamic nuclear polarization effects in solids. Chem Phys 294: 239–255
Jeschke G and Schweiger A (1996) Matched two-pulse electron spin echo envelope modulation spectroscopy. J Chem Phys 105: 2199–2211
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauss N (2001) Three-dimensional str ucture of cyanobacterial Photosystem I at 2.5 Å resolution. Nature 411: 909–917
Kandrashkin YE, Salikhov KM, van der Est A and Stehlik D (1998) Electron spin polarization in consecutive spin-cor related radical pairs: Application to shor t-lived and long-lived precursors in type 1 photosynthetic reaction centers. Appl Magn Reson 15: 417–447
Käss H, Bittersmann-Weidlich E, Andréasson L-E, Bönigk B and Lubitz W (1995) ENDOR and ESEEM of the 15N labelled radical cations of chlorophyll a and the primary donor P700 in Photosystem I. Chem Phys 194: 419–432
Kiefer AM, Kast SM, Wasielewski MR, Laukenmann K and Kothe G (1999) Exploring the str ucture of a photosynthetic model by quantum-chemical calculations and time-resolved Q-band electron paramagnetic resonance. J Am Chem Soc 121: 188–198
Kothe G, Weber S, Bittl R, Ohmes E, Thurnauer MC and Norris JR (1991) Transient EPR of light-induced radical pairs in plant Photosystem I: Observation of quantum beats. Chem Phys Lett 186: 474–480
Kothe G, Weber S, Ohmes E, Thurnauer MC and Nor ris JR (1994a) Transient EPR of light-induced spin-cor related radical pairs: Manifestation of zero quantum coherence. J Phys Chem 98: 2706–2712
Kothe G, Weber S, Ohmes E, Thurnauer MC and Nor ris JR (1994b) High time resolution electron paramagnetic resonance of light-induced radical pairs in photosynthetic bacterial reaction centers: Obser vation of quantum beats. J Am Chem Soc 116: 7729–7734
Kothe G, Bechtold M, Link G, Ohmes E and Weidner J-U (1998) Pulsed EPR detection of light-induced nuclear coherences in photosynthetic reaction centers. Chem Phys Lett 283: 51–60
Krabben L, Schlodder E, Jordan R, Carbonera D, Giacometti G, Lee H, Webber AN and Lubitz W (2000) Influence of the axial ligands on the spectral proper ties of P700 of Photosystem I: A study of site-directed mutants. Biochemistr y 39: 13012–13025
Link G, Ber thold T, Bechtold M, Weidner J-U, Ohmes E, Tang J, Poluektov O, Utschig L, Schlesselman SL, Thurnauer MC and •– 700A1Kothe G (2001) Structure of the P•+ 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
Link G, Poluektov OG, Utschig LM, Lalevée J, Yago T, Weidner J-U, Thurnauer MC and Kothe G (2005) Structural organization in photosynthetic proteins as studied by high-fi eld EPR of spin-correlated radical pair states. Magn Reson Chem 43: 103–109
Mac M, Tang XS, Diner BA, McCracken J and Babcock GT (1996) Identification of histidine as an axial ligand to P•+ 700. Biochemistr y 35: 13288–13293
Mac M, Bowlby NR, Babcock GT and McCracken J (1998) Monomeric spin density distrib ution in the primary donor of Photosystem I as determined by electron magnetic resonance: Functional and ther modynamic implications. J Am Chem Soc 120: 13215–13223
McLauchlan K (1989) Time-Resolved EPR. In: Hoff AJ (ed) Advanced EPR, Application in Biology and Biochemistr y, pp 345–369. Elsevier, Amsterdam Möbius K (2000) Primary processes in photosynthesis: What do we learn from high-field EPR spectroscopy? Chem Soc Rev 29: 129–139
Morris AL, Snyder SW, Zhang Y, Tang J, Thurnauer MC, Dutton PL, Robertson DE and Gunner MR (1995) An electron spin polarization model applied to sequential electron transfer in iron-containing photosynthetic bacterial reaction centers with different quinones as QA. J Phys Chem 99: 3854–3866
Norris JR, Uphaus RA, Crespi HL and Katz, JJ (1971) Electron spin resonance of chlorophyll and the origin of signal I in photosynthesis. Proc Natl Acad Sci USA 68: 625–628
Norris JR, Thurnauer MC and Bowman MK (1980) Electron Spin Echo Spectroscopy and the Study of Biological Structure and Function. In: Lawrence JH, Golfman JW and Hayes TL (eds) Advances in Biological and Medical Physics, pp 365–416. Academic Press, New York
Norris JR, Mor ris AL, Thurnauer MC and Tang J (1990) A general model of electron spin polarization arising from the interactions within radical pairs. J Chem Phys 92: 4239–4249
Pauling L (1979) Diamagnetic anisotropy of the peptide g roup. Proc Natl Acad Sci USA 76: 2293–2294
Petrenko A, Redding K, Kispert LD (2005) The influence of the structure of the radical cation dimer pair of aromatic molecules on the principal values of a g-tensor: DFT predictions. Chem Phys Lett 406: 327–331
Poluektov OG, Utschig LM, Schlesselman SL, Lakshmi KV, Brudvig GW, Kothe G and Thurnauer MC (2002) Electronic structure of the P700 special pair from electron paramagnetic resonance spectroscopy. J Phys Chem B 106: 8911–8916
Poluektov OG, Utschig LM, Dubinskij AA and Thurnauer MC (2004) ENDOR of spin-cor related radical pairs in photosynthesis at high magnetic field: A tool for mapping electron transfer pathways, J Am Chem Soc 126: 1644–1645
Poluektov OC, Utschig LM, Dubinskij AA and Thurnauer MC (2005) Electron transfer pathways and protein response to charge separation in photosynthetic reaction centers: Time-resolved high-field ENDOR of the spin-cor related radical pair P+–865QA. J Am Chem Soc 127: 4049–4059
Salikhov KM, Bock CH and Stehlik D (1990) Time development of electron spin polarization in magnetically coupled, spin correlated radical pairs. Appl Magn Reson 1: 195–211
Salikhov KM, Kandrashkin YuE and Salikhov AK (1992) Peculiarities of free induction and primar y spin echo signals for spin-correlated radical pairs. Appl Magn Reson 3: 199–216
Schlodder E, Falkenberg K, Gergeleit M and Brettel K (1998) Temperature dependence of forward and reverse electron transfer from A•–1 , the reduced secondary electron acceptor in Photosystem I. Biochemistry 37: 9466–9476
Sétif P, Mathis P and Vänngard T (1984) Photosystem I photochemistry at low temperature. Heterogeneity in pathways for electron transfer to the secondar y acceptors and for recombination processes. Biochim Biophys Acta 767: 404–414
Snyder SW and Thurnauer MC (1993) Electron spin polarization in photosynthetic reaction centers. In: Deisenhofer H and Norris JR (eds) The Photosynthetic Reaction Center, Vol 2, pp 285–329. Academic Press, New York
Stehlik D and Möbius K (1997) New EPR methods for investigating photoprocesses with paramagnetic inter mediates. Annu Rev Phys Chem 48: 745–784
Stehlik D, Bock CH and Thurnauer MC (1989a) Transient EPR spectroscopy of photoinduced electronic spin states in rigid matrices. In Hoff AJ (ed) Advanced EPR, Application in Biology and Biochemistr y, pp 371– 403. Elsevier, Amsterdam
Stehlik D, Bock CH and Petersen J (1989b) Anisotropic electron spin polarization in photosynthetic reaction centers. J Phys Chem 93: 1612–1619
Stone AJ (1963) G-tensors of aromatic hydrocarbons. Mol Phys 7: 311–316
Tang J and Nor ris JR (1995) Multiple-quantum EPR coherence in a spin-cor related radical pair system. Chem Phys Lett 233: 192–200
Tang J, Thurnauer MC and Nor ris JR (1994) Electron spin echo modulation due to exchange and dipolar interactions in a spin-correlated radical pair. Chem Phys Lett 219: 283–290
Thurnauer MC and Nor ris JR (1980) An electron spin echo phase shift observed in photosynthetic algae. Possible evidence for dynamic radical pair interactions. Chem Phys Lett 76: 557–561
Thurnauer MC, Poluektov OG and Kothe G (2004) Time-resolved high-frequency and multifrequency EPR studies of spin-cor-related radical pairs in photosynthetic reaction center proteins. In: Grinberg OY and Berliner LJ (eds) Biological Magnetic Resonance. Very High Frequency ESR/EPR, pp 165–206. Kluwer Academic Publisheres, New York
Torrey HC (1949) Transient nutations in nuclear magnetic resonance. Phys Rev 76: 1059–1072
Trifunac AD and Nor ris JR (1978) Nanosecond time resolved EPR spectroscopy. EPR time profile by electron spin echo CIDEP. Chem Phys Lett 59: 140–142
Trifunac AD and Thurnauer MC (1979) Time-resolved electron spin resonance of transient radicals. In: Kevan L and Schwartz RN (eds) Time Domain Electron Spin Resonance, pp 107–152. John Wiley & Sons, New York
Turro NJ and Khudyakov IV (1999) Applications of chemically induced dynamic electron polarization to mechanistic photochemistry. Res Chem Intermed 25: 505–529
Weber S, Kothe G and Nor ris JR (1997) Transient nutation electron spin resonance spectroscopy on spin-cor related racial pairs: A theoretical analysis of hyperfine-induced nuclear modulations. J Chem Phys 106: 6248–6261
Worcester DL (1978) Structural origins of diamagnetic anisotropy in proteins. Proc Natl Acad Sci USA 75: 5475–5477
Zech SG, Hofbauer W, Kamlowski A, Fromme P, Stehlik D, Lubitz W and Bittl R (2000) A structural model for the charge separated state P•+•–700A1 in Photosystem I from the orientation of the magnetic interaction tensors. J Phys Chem B 104: 9728–9739
Zwanenburg G and Hore PJ (1993) EPR of spin-cor related radical pairs. Analytical treatment of selective excitation including zero quantum coherence. Chem Phys Lett 203: 65–74
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Kothe, G., Norris, J.R., Poluektov, O.G., Thurnauer, M.C. (2008). High-Time Resolution Electron Paramagnetic Resonance Study of Quantum Beat Oscillations Observed in Photosynthetic Reaction Center Proteins. In: Aartsma, T.J., Matysik, J. (eds) Biophysical Techniques in Photosynthesis. Advances in Photosynthesis and Respiration, vol 26. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8250-4_15
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