Advertisement

Photosynthesis Research

, Volume 86, Issue 1–2, pp 185–201 | Cite as

Red Chlorophylls in the Exciton Model of Photosystem I

  • Sarunas Vaitekonis
  • Gediminas Trinkunas
  • Leonas Valkunas
Regular Paper

Abstract

Structural arrangement of pigment molecules of Photosystem I of photosynthetic cyanobacterium Synechococcus elongatus is used for theoretical modeling of the excitation energy spectrum. It is demonstrated that a straightforward application of the exciton theory with the assumption of the same molecular transition energy does not describe the red side of the absorption spectrum. Since the inhomogeneity in the molecular transition energies caused by a dispersive interaction with the molecular surrounding cannot be identified directly from the structural model, the evolutionary search procedure is used for fitting the low temperature absorption and circular dichroism spectra. As a result, one dimer, three trimers and one tetramer of chlorophyll molecules responsible for the red side of the absorption spectrum with their assignment to the spectroscopically established three bands at 708, 714 and 719 nm are determined. All of them are found to be situated not in the very close vicinity of the reaction center but are encircling it almost at the same distance. In order to explain the unusual broadening on the red side of the spectrum the exciton state mixing with the charge transfer (CT) states is considered. It is shown that two effects can be distinguished as caused by mixing of those states: (i) the oscillator strength borrowing by the CT state from the exciton transition and (ii) the borrowing of the high density of the CT state by the exciton state. The intermolecular vibrations between two counter-charged molecules determine the high density in the CT state. From the broad red absorption wing it is concluded that the CT state should be the lowest state in the complexes under consideration. Such mixing effect enables resolving the diversity in the molecular transition energies as determined by different theoretical approaches.

Keywords

exciton–CT mixing PS I red pigments Synechococcus elongatus 

Abbreviations

CD

circular dichroism

Chl

chlorophyll

CT

charge transfer

ESA

excited state absorption

FWHM

full width at half maximum

LD

linear dichroism

LHCI

light-harvesting complex I

OD

optical density, absorption

PS I

Photosystem I

PS II

Photosystem II

RC

reaction center

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agranovich, VM, Garstein, YuN, Zakhidov, A, Bussimer, P 1984An adiabatic local model for the internal structure of charge-transfer excitons: dimers and trimersChem Phys Lett110270274CrossRefGoogle Scholar
  2. Balaban, TS 2003Are syn-ligated (bacterio)chlorophyll dimers energetic traps in light-harvesting systems?FEBS Lett54597102CrossRefPubMedGoogle Scholar
  3. Balaban, TS, Fromme, P, Holzwarth, AR, Krauß, N, Prokhorenko, VI 2002Relevance of the diastereotopic ligation of magnesium atoms of chlorophylls in Photosystem IBiochim Biophys Acta1556197207PubMedGoogle Scholar
  4. Ben-Shem, A, Frolow, F, Nelson, N 2003Crystal structure of plant Photosystem INature426630635PubMedGoogle Scholar
  5. Brüggemann, B, Sznee, K, Novoderezhkin, V, Grondelle, R, May, V 2004From structure to dynamics: Modeling exciton dynamics in the photosynthetic antenna PS1J Phys Chem B1081353613546CrossRefGoogle Scholar
  6. Byrdin, M, Rimke, I, Schlodder, E, Stehlik, D, Roelofs, TA 2000Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: are the kinetics of excited state decay trap-limited or transfer limited?Biophys J799921007PubMedGoogle Scholar
  7. Byrdin, M, Jordan, P, Krauss, N, Fromme, P, Stehlik, D, Schlodder, E 2002Light Harvesting in Photosystem I: modeling based on the 2.5-Å structure of Photosystem I from Synechococcus elongatusBiophys J83433457PubMedGoogle Scholar
  8. Damjanovic, A, Vaswani, HM, Fromme, P, Fleming, GR 2002Chlorophyll excitations in Photosystem I of Synechococcus elongatusJ Phys Chem B1061025110262CrossRefGoogle Scholar
  9. Engelmann, E, Tagliabue, T, Karapetyan, NV, Garlaschi, FM, Zucchelli, G, Jennings, RC 2001CD spectroscopy provides evidence for excitonic interactions involving red-shifted chlorophyll forms in Photosystem IFEBS Lett499112115CrossRefPubMedGoogle Scholar
  10. Frese, RN, Palacios, MA, Azzizi, A, Stokkum, IHM, Kruip, J, Rögner, M, Karapetyan, NV, Schlodder, E, Grondelle, R, Dekker, JP 2002Electric field effects on red chlorophylls, β-carotenes and P700 in cyanobacterial Photosystem I complexesBiochim Biophys Acta1554180191PubMedGoogle Scholar
  11. Gobets, B, Grondelle, R 2001Energy transfer and trapping in Photosystem IBiochim Biophys Acta11887585Google Scholar
  12. Gobets, B, Dekker, JP, Grondelle, R 1998Transfer-to-the-trap limited model of energy transfer in Photosystem IGarab, G eds. Photosynthesis: Mechanisms and EffectsKluwer Academic PublishersDordrecht, The Netherlands503508Google Scholar
  13. Gobets, B, Amerongen, H, Monshouwer, R, Kruip, J, Rögner, M, Grondelle, R, Dekker, JP 1994Polarized site-selected fluorescence spectroscopy of isolated Photosystem I particlesBiochim Biophys Acta11887585Google Scholar
  14. Gobets, B, Stokkum, IHM, Rögner, M, Kruip, J, Schlodder, E, Karapetian, NV, Dekker, JP, Grondelle, R 2001Tine-resolved fluorescence emission measurements of Photosystem I particles of various cyanobacteria: a unified compartment modelBiophys J81407424PubMedGoogle Scholar
  15. Gobets, B, Valkunas, L, Grondelle, R 2003aBridging the gap between structural and lattice models: a parametrization of energy transfer and trapping in Photosystem IBiophys J8538723882Google Scholar
  16. Gobets, B, Stokkum, IHM, Mourik, F, Dekker, JP, van Grondelle, R 2003bExcitation wavelength dependence of the fluorescence kinetics in Photosystem I particles from Synechocystis PC 6803 and Synechococcus elongatusBiophys J8538833898Google Scholar
  17. Goldberg, DE 1989Genetic Algorythms in Search, Optimization, and Machine LearningAddison-WesleyReading, MAGoogle Scholar
  18. Holland, JH 1975Adaptation in Natural and Artificial SystemsUniversity of Michigan PressAnn Arbor, MIGoogle Scholar
  19. Holzwarth, AR, Dora, D, Müller, MG, Karapetyan, NV 1998Structure-function relationship and excitation dynamics in Photosystem IGarab, G eds. Photosynthesis: Mechanisms and EffectsKluwer Academic PublishersDordrecht, The Netherlands497502Google Scholar
  20. Hsin, TM, Zazubovich, V, Hayes, JM, Small, GJ 2004Red antenna states of PS I of cyanobacteria: Stark effect and interstate energy transferJ Phys Chem B1081051510521CrossRefGoogle Scholar
  21. Ihalainen, JA, Rätsep, M, Jensen, PE, Scheller, HV, Croce, R, Bassi, R, Korppi-Tommola, JEI, Freiberg, A 2003Red spectral forms of chlorophylls in green plant PS I– a site-selective and high-pressure spectroscopy studyJ Phys Chem B10790869093CrossRefGoogle Scholar
  22. Jordan, P, Fromme, P, Witt, HT, Klukas, O, Saenger, W, Krauss, N 2001Three-dimensional structure of cyanobacterial Photosystem I at 2.5 Å resolutionNature411909917PubMedGoogle Scholar
  23. Kennis, JTM, Gobets, B, Stokkum, IHM, Dekker, JP, Grondelle, R, Fleming, GR 2001Light harvesting by chlorophylls and carotenoids in the Photosystem I core complex of Synechococcus elongatus. A fluorescence upconversion studyJ Phys Chem B10544854494CrossRefGoogle Scholar
  24. Knox, RS, Amerongen, H 2002Refractive index dependence of the Förster resonance excitation transfer rateJ Phys Chem B20652895293CrossRefGoogle Scholar
  25. Krauss, N, Schubert, WD, Klukas, O, Fromme, P, Witt, HT, Saenger, W 1996Photosystem I at 4 Å resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna systemNat Struct Biol3965973CrossRefPubMedGoogle Scholar
  26. Kumazaki, S, Ikegami, I, Furusawa, H, Yoshihara, K 2003Energy equilibration among the chlorophylls in the electron-transfer system of Photosystem I reaction center from spinachJ Phys Chem A10732283235CrossRefGoogle Scholar
  27. Laible, PD, Zipfel, W, Owens, TG 1994Excited state dynamics in chlorophyll-based antennae: the role of transfer equillibratiumBiophys J66844860PubMedGoogle Scholar
  28. Melkozernov, AN, Lin, S, Blankenship, RE 2000aExcitation dynamics and heterogeneity of energy equilibration in the core antenna of Photosystem I from cyanobacterium Synechocystis sp. PCC 6803Biochemistry3914891498CrossRefGoogle Scholar
  29. Melkozernov, AN, Lin, S, Blankenship, RE 2000bFemtosecond transient spectroscopy and exciton interactions in Photosystem IJ Phys Chem B10416511656CrossRefGoogle Scholar
  30. Melkozernov, AN, Lin, S, Blankenship, RE, Valkunas, L 2001Spectral inhomogeneity of Photosystem I and its influence on excitation equilibration and trapping in the cyanobacterium Synechocystis sp. PCC6803 at 77KBiophys J8111441154PubMedGoogle Scholar
  31. Müller, MG, Niklas, J, Lubitz, W, Holzwarth, AR 2003Ultrafast transient absorption studies of Photosystem I reaction center from Chlamidomonas reinhardtii. 1. A new interpretation of the energy trapping and early electron transfer steps in Photosystem IBiophys J8538993922PubMedGoogle Scholar
  32. Pålsson, L-O, Dekker, JP, Schlodder, E, Monshouwer, R, Grondelle, R 1996Polarized site-selective fluorescence spectroscopy of the long-wavelength emitting chlorophylls in isolated Photosystem I particles of Synechococcus elongatusPhotosynth Res48239246CrossRefGoogle Scholar
  33. Pearlstein, RM 1991Theoretical interpretation of antenna spectraScheer, H eds. Chlorophylls CRC PressNew York10471078Google Scholar
  34. Rätsep, M, Johnson, TW, Chitnis, PR, Small, GJ 2000The red-absorbing chlorophyll a antenna states of Photosystem IJ Phys Chem B104836847CrossRefGoogle Scholar
  35. Reinot, T, Zazubovich, V, Hayes, JM, Small, GJ 2001New insights on persistent nonphotochemical hole burning and its application to photosynthetic complexesJ Phys Chem B10550835098CrossRefGoogle Scholar
  36. Savikhin, S, Xu, W, Soukoulis, V, Chitnis, PR, Struve, WS 1999Ultrafast primary processes in Photosystem I of the cyanobacterium Synechocystis sp. PCC 6803Biophys J7632783288PubMedGoogle Scholar
  37. Schubert, WD, Klukas, O, Krauss, N, Saenger, W, Fromme, P, Witt, HT 1997Photosystem I of Synechococcus elongatus at 4 Å resolution: comprehensive structure analysisJ Mol Biol272741769CrossRefPubMedGoogle Scholar
  38. Sener, MK, Lu, D, Ritz, T, Park, S, Fromme, P, Schulten, K 2002Robustness and optimality of light harvesting in cyanobacterial Photosystem IJ Phys Chem B10679487960CrossRefGoogle Scholar
  39. Soukoulis, V, Savikhin, S, Xu, W, Chitnis, PR, Struve, WS 1999Electronic spectra of PS I mutants: the peripheral subunits do not bind red chlorophylls in Synechocystis sp. PCC 6803Biophys J7627112715PubMedGoogle Scholar
  40. Trinkunas, G, Holzwarth, AR 1994Kinetic modeling of exciton migration on photosynthetic systems. 2. Simulations of exciton dynamics in two-dymensional Photosystem I core antenna/reaction center complexesBiophys J66415429PubMedGoogle Scholar
  41. Trinkunas, G, Holzwarth, AR 1996Kinetic modeling of exciton migration on photosynthetic systems. 3. Application of generic algorithm of exciton dynamics in three-dimensional Photosystem I core antenna/reaction center complexesBiophys J71351364PubMedGoogle Scholar
  42. Valkunas, L, Liuolia, V, Dekker, JP, Grondelle, R 1995Description of energy migration in Photosystem I by a model with two distance scaling paprametersPhotosynth Res43149154CrossRefGoogle Scholar
  43. Amerongen, H, Valkunas, L, Grondelle, R 2000Photosynthetic ExcitonsWorld ScientificSingaporeGoogle Scholar
  44. Grondelle, R, Dekker, JP, Gillbro, T, Sundström, V 1994Energy transfer and trapping in photosynthesisBiochim Biophys Acta1187165CrossRefGoogle Scholar
  45. Zandvoort, MAMJ, Wrobel, D, Lettinga, P, Ginkel, G, Levine, YK 1995The orientation of the transition dipole moments of chlorophyll a and pheophytin a in their molecular framePhotochem Photobiol62299308Google Scholar
  46. Werst, M, Jia, Y, Mets, L, Fleming, GR 1992Energy transfer and trapping in Photosystem I core antenna: a temperature studyBiophys J61868878PubMedGoogle Scholar
  47. White, NT, Beddard, GS, Thorne, JRG, Feehan, TM, Keytes, TE, Hearhcote, P 1996Primary charge separation and energy transfer in the Photosystem I Reaction Center of Higher PlantsJ Phys Chem1001208612099CrossRefGoogle Scholar
  48. Yang, M, Damjanovic, A, Vaswani, HM, Fleming, GR 2003Energy transfer in Photosystem I of cyanobacteria Synechococcus elongatus: model study with structure-based semi-empirical Hamiltonian and experimental spectral densityBiophys J85140158PubMedGoogle Scholar
  49. Zazubovich, V, Matsuzaki, S, Johnson, TW, Hayes, JM, Chitnis, PR, Small, GJ 2002Red antenna states of Photosystem I from cyanobacterium Synechococcus elongatus: a spectral hole burning studyChem Phys2754759CrossRefGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Sarunas Vaitekonis
    • 1
  • Gediminas Trinkunas
    • 1
  • Leonas Valkunas
    • 1
    • 2
  1. 1.Institute of PhysicsVilniusLithuania
  2. 2.Theoretical Physics ChairFaculty of Physics of Vilnius universityVilniusLithuania

Personalised recommendations