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Modeling Light Harvesting and Primary Charge Separation in Photosystem I and Photosystem II

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Photosynthesis in silico

We discuss how the light harvesting in photosystem I, photosystem II and in light-harvesting complex II can be modeled at a quantitative level by taking into account the exciton structure of the chromophores in the pigment-protein complexes, static (conformational) disorder, and coupling of electronic excitations and charge-transfer (CT) states to fast nuclear motion. We show examples of simultaneous fitting of linear and nonlinear (time-dependent) spectral responses based on the modified Redfield theory that resulted in a consistent physical picture of the energy and electron transfer reactions. This picture (including the time scales and pathways of energy and charge transfer) allows a visualization of the excitation dynamics, thus leading to a deeper understanding of how photosynthetic pigment-proteins perform their function in harvesting of solar energy.

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References

  • Amunts A, Drory O and Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 Ã… resolution. Nature 447: 58–63

    Article  PubMed  CAS  Google Scholar 

  • Barber J (2003) Photosystem II: the engine of life. Quart Rev Biophys 36: 71–89

    Article  CAS  Google Scholar 

  • Barkai E, Jung YJ and Silbey RJ (2004) Theory of single-molecule spectroscopy: Beyond the ensemble average. Annu Rev Phys Chem 55: 457–507

    Article  PubMed  CAS  Google Scholar 

  • Barter LMC, Durrant JR and Klug DR (2003) A quantitative structure-function relationship for the Photosystern II reaction center: Supermolecular behavior in natural photosynthesis. Proc Natl Acad Sci USA 100: 946–951

    Article  PubMed  CAS  Google Scholar 

  • Ben-Shem A, Frolow F and Nelson N (2003) Crystal structure of plant photosystem I. Nature 426: 630–635

    Article  PubMed  CAS  Google Scholar 

  • Bopp MA, Sytnik A, Howard TD, Cogdell RJ and Hochstrasser RM (1999) The dynamics of structural deformations of immobilized single light-harvesting complexes. Proc Natl Acad Sci USA 96: 11271–11276

    Article  PubMed  CAS  Google Scholar 

  • Brüggemann B, Sznee K, Novoderezhkin V, Van Grondelle R and May V (2004) From structure to dynamics: Modeling exciton dynamics in the photosynthetic antenna PS1, J Phys Chem B 108: 13536–13546

    Article  Google Scholar 

  • Byrdin M, Jordan P, Krauss N, Fromme P, Stehlik D and Schlodder E (2002) Light harvesting in photosystem I: Modeling based on the 2.5-Ã… structure of photosystem I from Synechococcus elongatus. Biophys J 83: 433–457

    Article  PubMed  CAS  Google Scholar 

  • Cho M, Vaswani HM, Brixner T, Stenger J and Fleming GR (2005) Exciton analysis in 2D electronic spectroscopy. J Phys Chem B 109: 10542–10556

    Article  PubMed  CAS  Google Scholar 

  • Damjanović A, Kosztin I, Kleinekathoefer U and Schulten K (2002a) Excitons in a photosynthetic light-harvesting system: A combined molecular dynamics, quantum chemistry, and polaron model study. Phys Rev E 65: 031919-1– 031919-24

    Google Scholar 

  • Damjanović A, Vaswani HM, Fromme P and Fleming GR (2002b) Chlorophyll excitations in photosystem I of Syne-chococcus elongatus. J Phys Chem B 106: 10251–10262

    Article  Google Scholar 

  • Dekker JP and Van Grondelle R (2000) Primary charge separation in photosystem II. Photosynth Res 63: 195–208

    Article  PubMed  CAS  Google Scholar 

  • Diner BA and Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53: 551–580

    Article  PubMed  CAS  Google Scholar 

  • Diner BA, Schlodder E, Nixon JP, Coleman WJ, Rappaport F, Lavergne J, Vermaas WFJ and Chisholm DA (2001) Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: Sites of primary charge separation and cation and triplet stabilization. Biochemistry 40: 9265–9281

    Article  PubMed  CAS  Google Scholar 

  • Durrant JR, Klug DR, Kwa SLS, Van Grondelle R, Porter G and Dekker JP (1995) A multimer model for P680, the primary electron donor of photosystem II. Proc Natl Acad Sci USA 92: 4798–4802

    Article  PubMed  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838

    Article  PubMed  CAS  Google Scholar 

  • Förster T (1965) Delocalized excitation and excitation transfer. In: SinanoÄŸlu (ed) Modern Quantum Chemistry, Part III. B. Action of Light and Organic Crystals, pp. 93–137. Academic, New York

    Google Scholar 

  • Frese RN, Palacios MA, Azzizi A, Van Stokkum IHM, Kruip J, Roegner M, Karapetyan NV, Schlodder E, Van Gron-delle R and Dekker JP (2002) Electric field effects on red chlorophylls, β-carotenes and P700 in cyanobacterial photosystem I complexes. Biochim Biophys Acta 1554: 180–191

    Article  PubMed  CAS  Google Scholar 

  • Gillie JK, Small GJ and Golbeck JH (1989) Nonphotochem-ical hole burning of the native antenna complex of photo-system I (PS I-200). J Phys Chem 93: 1620–1627

    Article  CAS  Google Scholar 

  • Gobets B and Van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507: 80–99

    Article  PubMed  CAS  Google Scholar 

  • Gobets B, Van Stokkum IHM, Van Mourik F, Dekker JP and Van Grondelle R (2003) Excitation wavelength dependence of the fluorescence kinetics in photosystem I particles from Synechocystis PCC 6803 and Synechococcus elongatus. Biophys J 85: 3883–3898

    Article  PubMed  CAS  Google Scholar 

  • Gradinaru CC, Özdemir S, Gülen D, Van Stokkum IHM, Van Grondelle R and Van Amerongen H (1998) The flow of excitation energy in LHCII monomers. Implications for the structural model of the major plant antenna. Biophys J 75: 3064–3077

    Article  PubMed  CAS  Google Scholar 

  • Greenfield SR, Seibert M, Govindjee and Wasielewski M (1997) Direct measurement of the effective rate constant for primary charge separation in isolated photosystem II reaction centers. J Phys Chem B 101: 2251–2255

    Article  CAS  Google Scholar 

  • Groot M-L, Pawlowicz NP, Van Wilderen LJGW, Breton J, Van Stokkum IHM and Van Grondelle R (2005) Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spec-troscopy. Proc Natl Acad Sci USA 102: 13087–13092

    Article  PubMed  CAS  Google Scholar 

  • Jang S, Newton MD and Silbey RJ (2004) Multichro-mophoric Förster resonance energy transfer. Phys Rev Lett 92: 218301-1–218301-4

    Google Scholar 

  • Jean JM and Fleming GR (1995) Competition between energy and phase relaxation in electronic curve crossing processes. J Chem Phys 103: 2092–2101

    Article  CAS  Google Scholar 

  • Jordan P, Fromme P, Witt HT, Klukas O, Saenger W and Krauß N (2001) Three-dimensional structure of cyanobac-terial photosystem I at 2.5 Ã… resolution. Nature 411: 909–917

    Article  PubMed  CAS  Google Scholar 

  • Kamiya N and Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vul-canus at 3.7 Ã… resolution. Proc Natl Acad Sci USA 100: 98–103

    Article  PubMed  CAS  Google Scholar 

  • Kamlowski A, Frankemoller L, Van der Est A, Stehlik D and Holzwarth AR (1996) Evidence for delocalization of the triplet state 3P680 in the D1-D2cytb559-complex of pho-tosystem II. Ber Bunsenges Phys Chem 100: 2045–2051

    CAS  Google Scholar 

  • Karapetyan N, Schlodder E, Van Grondelle R and Dekker JP (2006) The long wavelength chlorophylls of photosys-tem I. In: Golbeck JH (ed) Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase, pp. 177– 192. Springer, The Netherlands

    Google Scholar 

  • Kleima FJ, Gradinaru CC, Calkoen F, Van Stokkum IHM, Van Grondelle R and Van Amerongen H (1997) Energy transfer in LHCII monomers at 77 K studied by sub-picosecond transient absorption spectroscopy. Biochemistry 36: 15262–15268

    Article  PubMed  CAS  Google Scholar 

  • Kühlbrandt W, Wang DN and Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367: 614–621

    Article  PubMed  Google Scholar 

  • Leegwater JA, Durrant JR and Klug DR (1997) Exciton equilibration induced by phonons: Theory and application to PS II reaction centers. J Phys Chem B 101: 7205–7210

    Article  CAS  Google Scholar 

  • Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X and Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Ã… resolution. Nature 428: 287–292

    Article  PubMed  CAS  Google Scholar 

  • Loll B, Kern J, Saenger W, Zouni A and Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Ã… resolution structure of photosystem II. Nature 438: 1040–1044

    Article  PubMed  CAS  Google Scholar 

  • Meier T, Chernyak V and Mukamel S (1997) Femtosecond photon echoes in molecular aggregates. J Chem Phys 107: 8759–8774

    Article  CAS  Google Scholar 

  • Moerner WE (2002) A dozen years of single-molecule spec-troscopy in physics, chemistry, and biophysics. J Phys Chem B 106: 910–927

    Article  CAS  Google Scholar 

  • Mukamel S (1995) Principles of Nonlinear Optical Spec-troscopy. Oxford University Press, New York, Oxford

    Google Scholar 

  • Noguchi T, Inoue Y and Satoh K (1993) FT-IR studies on the triplet state of P680 in the photosystem II reaction center: Triplet equilibrium within a chlorophyll dimer. Biochemistry 32: 7186–7195

    Article  PubMed  CAS  Google Scholar 

  • Novoderezhkin VI and Razjivin AP (1994) Exciton states of the antenna and energy trapping by the reaction center. Photosynth Res 42: 9–15

    Article  CAS  Google Scholar 

  • Novoderezhkin VI and Razjivin AP (1996) The theory of Förster-type migration between clusters of strongly interacting molecules: Application to light-harvesting complexes of purple bacteria. Chem Phys 211: 203–214

    Article  CAS  Google Scholar 

  • Novoderezhkin VI, Palacios MA, Van Amerongen H and Van Grondelle R (2004a) Energy-transfer dynamics in the LHCII complex of higher plants: Modified Redfield approach. J Phys Chem B 108: 10363–10375

    Article  CAS  Google Scholar 

  • Novoderezhkin VI, Yakovlev AG, Van Grondelle R and Shuvalov VA (2004b) Coherent nuclear and electronic dynamics in primary charge separation in photosynthetic reaction centers: A Redfield theory approach. J Phys Chem B 108: 7445–7457

    Article  CAS  Google Scholar 

  • Novoderezhkin VI, Palacios MA, Van Amerongen H and Van Grondelle R (2005a) Excitation dynamics in the LHCII complex of higher plants: Modeling based on 2.72 A crystal structure. J Phys Chem B 109: 10493–10504

    Article  CAS  Google Scholar 

  • Novoderezhkin VI, Andrizhiyevskaya EG, Dekker JP and Van Grondelle R (2005b) Pathways and timescales of primary charge separation in the photosystem II reaction center as revealed by a simultaneous fit of time-resolved fluorescence and transient absorption. Biophys J 89: 1464–1481

    Article  CAS  Google Scholar 

  • Novoderezhkin VI, Rutkauskas D and Van Grondelle R (2006) Dynamics of the emission spectrum from single LH2 complex: Interplay of slow and fast nuclear motions. Biophys J 90: 2890–2902

    Article  PubMed  CAS  Google Scholar 

  • Novoderezhkin VI, Dekker JP and Van Grondelle R (2007) Mixing of exciton and charge-transfer states in photosys-tem II reaction centers: Modeling of Stark spectra with modified Redfield theory. Biophys J 93: 1293–1311

    Article  PubMed  CAS  Google Scholar 

  • Peterman EJG, Pullerits T, Van Grondelle R and Van Amerongen H (1997) Electron-phonon coupling and vibronic fine structure of light-harvesting complex II of green plants: Temperature dependent absorption and high-resolution fluorescence spectroscopy. J Phys Chem B 101: 4448–4457

    Article  CAS  Google Scholar 

  • Peterman EJG, Van Amerongen H, Van Grondelle R and Dekker JP (1998) The nature of the excited state of the reaction center of photosystem II of green plants: A high-resolution fluorescence spectroscopy study. Proc Natl Acad Sci USA 95: 6128–6133

    Article  PubMed  CAS  Google Scholar 

  • Pieper J, Voigt J and Small GJ (1999) Chlorophyll a Franck-Condon factors and excitation energy transfer. J Phys Chem B 103: 2319–2322

    Article  CAS  Google Scholar 

  • Prokhorenko VI and Holzwarth AR (2000) Primary processes and structure of the photosystem II reaction center: A) Photon echo study. J Phys Chem B 104: 1563–11578

    Article  Google Scholar 

  • Raszewski G, Saenger W and Renger Th (2005) Theory of optical spectra of photosystem II reaction centers: Location of the triplet state and the identity of the primary electron donor. Biophys J 88: 986–998

    Article  PubMed  CAS  Google Scholar 

  • Redfield AG (1965) The theory of relaxation processes. Adv Mag Res 1: 1–32

    Google Scholar 

  • Renger Th and Marcus R (2002) Photophysical properties of PS-2 reaction centers and a discrepancy in exciton relaxation times. J Phys Chem B 106: 1809–1819

    Article  CAS  Google Scholar 

  • Renger Th and May V (1997) Theory of multiple exciton effects in the photosynthetic antenna complex LHC-II. J Phys Chem B 101: 7232–7240

    Article  CAS  Google Scholar 

  • Renger Th and Schlodder E (2006). Modeling of optical spectra and light harvesting in photosystem I. In: Golbeck JH (ed) Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase, pp. 595–610. Springer, The Netherlands

    Google Scholar 

  • Renger Th, May V and Kühn O (2001) Ultrafast excitation energy transfer dynamics in photosynthetic pigment-protein complexes. Phys Rep 343: 137–254

    Article  CAS  Google Scholar 

  • Rutkauskas D, Novoderezhkin V, Cogdell RJ and Van Grondelle R (2004) Fluorescence spectral fluctuations of single LH2 complexes from Rhodopseudomonas aci-dophila strain 10050. Biochemistry 43: 4431–4438

    Article  PubMed  CAS  Google Scholar 

  • Rutkauskas D, Novoderezhkin V, Cogdell RJ and Van Grondelle R (2005) Fluorescence spectroscopy of confor-mational changes of single LH2 complexes. Biophys J 88: 422–435

    Article  PubMed  CAS  Google Scholar 

  • Rutkauskas D, Novoderezhkin V, Gall A, Olsen J, Cogdell RJ, Hunter CN and Van Grondelle R (2006) Spectral trends in the fluorescence of single bacterial light-harvesting complexes: Experiments and modified Redfield simulations. Biophys J 90: 2475–2485

    Article  PubMed  CAS  Google Scholar 

  • Savikhin S (2006) Ultrafast optical spectroscopy of photo-system I. In: Golbeck JH (ed) Photosystem I: The Light-Driven Plastocyanin:Ferredoxin Oxidoreductase, pp 155– 176. Springer, The Netherlands

    Google Scholar 

  • Schlodder E, Shubin VV, El Mohsnawy E, Roegner M and Karapetyan NV (2007) Steady-state and transient polarized absorption spectroscopy of photosystem I complexes from the cyanobacteria Arthrospira platensis and Thermosynechococcus elongatus. Biochim Biophys Acta 1767: 732–741

    Article  PubMed  CAS  Google Scholar 

  • Scholes GD and Fleming GR (2000) On the mechanism of light harvesting in purple bacteria: B800 to B850 energy transfer. J Phys Chem B 104: 1854–1868

    Article  CAS  Google Scholar 

  • Sener MK, Lu DY, Ritz T, Park S, Fromme P and Schulten K (2002) Robustness and optimality of light harvesting in cyanobacterial photosystem I. J Phys Chem B 106: 7948– 7960

    Article  CAS  Google Scholar 

  • Standfuss J, Van Scheltinga1 ACT, Lamborghini M and Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light harvesting complex at 2.5 Ã… resolution. EMBO J 24: 919–928

    Article  PubMed  CAS  Google Scholar 

  • Sumi H (1999) Theory on rates of excitation-energy transfer between molecular aggregates through distributed transition dipoles with application to the antenna system in bacterial photosynthesis. J Phys Chem B 103: 252–260

    Article  CAS  Google Scholar 

  • Tietz C, Chekhlov O, Dräbenstedt A, Schuster J and Wrachtrup J (1999) Spectroscopy on single light-harvesting complexes at low temperature. J Phys Chem B 103: 6328–6333

    Article  CAS  Google Scholar 

  • Van Amerongen H and Dekker JP (2003) Light-harvesting in photosystem II. In: Green BR and Parson WW (ed) Light-Harvesting Antennas in Photosynthesis. Kluwer, Dordrecht, pp. 219–251

    Google Scholar 

  • Van Amerongen H, Valkunas L and Van Grondelle R (2000) Photosynthetic Excitons. World Scientific Publishers, Singapore

    Google Scholar 

  • Van Grondelle R and Gobets B (2004) Transfer and trapping of excitations in plant photosystems. In: Papageorgiou GC and Govindjee (eds) Chlorophyll a Fluorescence: A Signature of Photosynthesis, pp. 107–132. Springer, The Netherlands

    Google Scholar 

  • Van Grondelle R and Novoderezhkin V (2006) Energy transfer in photosynthesis: Experimental insights and quantitative models. Phys Chem Chem Phys 8: 793–807

    Article  PubMed  Google Scholar 

  • Van Grondelle R, Dekker JP, Gilbro T and Sundstroem V (1994) Energy transfer and trapping in photosynthesis. Biochim Biophys Acta 1187: 1–65

    Article  CAS  Google Scholar 

  • Van Mieghem FJE, Satoh K and Rutherford AW (1991) A chlorophyll tilted 30° relative to the membrane in the pho-tosystem II reaction centre. Biochim Biophys Acta 1058: 379–385

    Article  Google Scholar 

  • Van Oijen AM, Ketelaars M, Köhler J, Aartsma TJ and Schmidt J (1999) Unraveling the electronic structure of individual photosynthetic pigment-protein complexes. Science 285: 400–402

    Article  PubMed  Google Scholar 

  • VisserHM,KleimaFJ,VanStokkumIHM,VanGrondelleRand Van Amerongen H (1996) Probing of many energy-transfer processes in the photosynthetic light-harvesting complex II at 77 K by energy-selective sub-picosecond transient absorption spectroscopy. Chem Phys 210: 297–312

    Article  CAS  Google Scholar 

  • Yang M and Fleming GR (2002) Influence of phonons on exciton transfer dynamics: comparison of the Redfield, Förster, and modified Redfield equations. Chem Phys 275: 355–372

    Article  CAS  Google Scholar 

  • Yang M, Damjanović A, Harsha M. Vaswani and Graham R. Fleming (2003) Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: Model study with structure-based semi-empirical hamiltonian and experimental spectral density. Biophys J 85: 140–158

    Article  PubMed  CAS  Google Scholar 

  • Yoder LM, Cole AG and Sension RJ (2002) Structure and function in the isolated reaction center complex of pho-tosystem II: Energy and charge transfer dynamics and mechanism. Photosynth Res 72: 147–158

    Article  PubMed  CAS  Google Scholar 

  • Zazubovich V, Matsuzaki S, Johnson TW, Hayes JM, Chitnis PR and Small GJ (2002) Red antenna states of pho-tosystem I from cyanobacterium Synechococcus elon-gatus: A spectral hole-burning study. Chem Phys 275: 47–59

    Article  CAS  Google Scholar 

  • Zhang WM, Meier T, Chernyak V and Mukamel S (1998) Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J Chem Phys 108: 7763–7774

    Article  CAS  Google Scholar 

  • Zouni A, Witt HT, Kern J, Fromme P, Krauß N, Saenger W and Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Ã… resolution. Nature 409: 739–743

    Article  PubMed  CAS  Google Scholar 

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van Grondelle, R., Novoderezhkin, V.I., Dekker, J.P. (2009). Modeling Light Harvesting and Primary Charge Separation in Photosystem I and Photosystem II. In: Laisk, A., Nedbal, L., Govindjee (eds) Photosynthesis in silico . Advances in Photosynthesis and Respiration, vol 29. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9237-4_3

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