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Excitation energy transfer in the LHC-II trimer: a model based on the new 2.72 Å structure

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Abstract

Energy transfer of the light harvesting complex LHC-II trimer, extracted from spinach, was studied in the Qy region at room temperature by femtosecond transient absorption spectroscopy. Configuration interaction exciton method [Linnanto et al. (1999) J Phys Chem B 103: 8739–8750] and 2.72 Å structural information reported by Liu et al. was used to calculate spectroscopic properties and excitation energy transfer rates of the complex. Site energies of the pigments and coupling constants of pigment pairs in close contact were calculated by using a quantum chemical configuration interaction method. Gaussian random variation of the diagonal and off-diagonal exciton matrix elements was used to account for inhomogeneous broadening. Rate calculations included only the excitonic states initially excited and probed in the experiments. A kinetic model was used to simulate time and wavelength dependent absorption changes after excitation on the blue side of the Qy transition and compared to experimentally recorded rates. Analysis of excitonic wavefunctions allowed identification of pigments initially excited and probed into later. It was shown that excitation of the blue side of the Qy band of a single LHC-II complex results in energy transfer from chlorophyll b’s of the lumenal side to chlorophyll a’s located primarly on one of the monomers of the stromal side.

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References

  • Agarwal R, Krueger BP, Scholes GD, Yang M, Yom J, Mets L, Fleming GR, (2000) Ultrafast energy transfer in LHC-II revealed by three-pulse photon echo peak shift measurements J Phys Chem B 104: 2908–2918

    Article  CAS  Google Scholar 

  • Agranovich VM, Galanin MD, (1982) Electronic excitation energy transfer in condensed matter. North-Holland Publishing Company, Amsterdam

    Google Scholar 

  • Barzda V, Garab G, Gulbinas V, Valkunas L, (1996) Evidence for long-range excitation energy migration in macroaggregates of the chlorophyll a/b light-harvesting antenna complexes Biochim Biophys Acta 1273: 231–236

    Article  Google Scholar 

  • Barzda V, Gulbinas V, Kananavicius R, Cervinskas V, van Amerongen H, van Grondelle R, Valkunas L, (2001) Singlet-singlet annihilation kinetics in aggregates and trimers of LHC II Biophys J 80: 2409–2421

    CAS  PubMed  Google Scholar 

  • Barzda V, Mustárdy L, Garab G, (1994) Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes Biochem 33: 10837–10841

    Article  CAS  PubMed  Google Scholar 

  • Bittner T, Irrgang K-D, Renger G, Wasielewski MR, (1994) Ultrafast excitation energy transfer and exciton-exciton annihilation processes in isolated light harvesting complexes of photosystem II (LHC II) from spinach J Phys Chem 98: 11821–11826

    Article  CAS  Google Scholar 

  • Bittner T, Wiederrecht GP, Irrgang K-D, Renger G, Wasielewski MR, (1995) Femtosecond transient absorption spectroscopy on the light-harvesting Chl a/b protein complex of Photosystem II at room temperature and 12 K Chem Phys 194: 311–322

    Article  CAS  Google Scholar 

  • Connelly JP, Müller MG, Bassi R, Croce R, Holzwarth AR, (1997a) Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of Photosystem II Biochem 36: 281–287

    Article  CAS  Google Scholar 

  • Connelly JP, Müller MG, Hucke M, Gatzen G, Mullineaux CW, Ruban AV, Horton P, Holzwarth AR, (1997b) Ultrafast spectroscopy of trimeric light-harvesting complex II from higher plants J Phys Chem B 101: 1902–1909

    Article  CAS  Google Scholar 

  • Croce R, Weiss S, Bassi R, (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J Biol Chem 274: 29613–29623

    Article  CAS  PubMed  Google Scholar 

  • Du M, Xie X, Mets L, Fleming GR, (1994) Direct observation of ultrafast energy-transfer processes in light harvesting complex II J Phys Chem 98: 4736–4741

    Article  CAS  Google Scholar 

  • Ghanotakis DF, Demetriou DM, Yocum CF, (1987) Isolation and characterization of an axygen-evolving Photosystem II reaction center core preparation and a 28 kDa Chl-a-binding protein Biochim Biophys Acta 891: 15–21

    Article  CAS  Google Scholar 

  • Gillbro T, Sundström V, Sandström Å, Spangfort M, Andersson B, (1985) Energy transfer within the isolated light-harvesting chlorophyll a/b protein of photosystem II (LHC-II) FEBS Lett 193: 267–270

    Article  CAS  Google Scholar 

  • Gradinaru CC, van Grondelle R, van Amerongen H, (2003) Selective interaction between xanthophylls and chlorophylls in LHC II probed by femtosecond transient absorption spectroscopy J Phys Chem B 107: 3938–3943

    Article  CAS  Google Scholar 

  • Il’ina MD, Kotova EA, Borisov Ayu, (1981) The detergent and salt effect on the light-harvesting chlorophyll a/b complex from green plants Biochim Biophys Acta 636: 193–200

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Linnanto J, Helenius VM, Oksanen JAI, Peltola T, Garaud J-L, Korppi-Tommola JEI, (1998) Exciton interactions and femtosecond relaxation in chlorophyll a-water and chlorophyll a-dioxane aggregates J Phys Chem A 102: 4337–4349

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola J, (2000) Spectroscopic properties of Mg-chlorin, Mg-porphin and chlorophylls a, b, c 1 , c 2 , c 3 , and d studied by semi-empirical and ab initio MO/CI methods Phys Chem Chem Phys 2: 4962–4970

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola J, (2001) Spectroscopic Properties of Mg-Chlorin, Mg-Bacteriochlorin, and Bacteriochlorophylls a, b, c, d, e, f, g, and h Studied by Semiempirical and Ab Initio MO/CI Methods J Phys Chem A 105: 3855–3866

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola J, (2004a) Semiempirical PM5 molecular orbital study on chlorophylls and bacteriochlorophylls: Comparison of semiempirical, ab initio and density functional results J Comput Chem 25: 123–138

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola J, (2004b) Structure and spectroscopic properties of Mg-bacteriochlorin, and methyl bacteriochlorophyllides a, b, g, and h studied by semiempirical, ab initio and density functional molecular orbital methods J Phys Chem A 108: 5872–5882

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola JEI, (2002) Theoretical study of excitation transfer from modified B800 rings of the LH II antenna complex of Rps. acidophila Phys Chem Chem Phys 4: 3453–3460

    Article  CAS  Google Scholar 

  • Linnanto J, Korppi-Tommola JEI, Helenius VM, (1999) Electronic states, absorption spectrum and circular dichroism spectrum of the photosynthetic bacterial LH2 antenna of Rhodopseudomonas acidophila as predicted by exciton theory and semiempirical calculations J Phys Chem B 103: 8739–8750

    Article  CAS  Google Scholar 

  • Linnanto JM, Korppi-Tommola JEI, (2000) Excitation energy-transfer in the LH2 antenna of photosynthetic purple bacteria via excitonic B800 and B850 states J Chin Chem Soc 47: 657–665

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Björkman O, Grossman AR, (1997) The roles of specific xanthophylls in photoprotection Proc Nat Acad Sci USA 94: 14162–14167

    Article  CAS  PubMed  Google Scholar 

  • Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R, (2004) Energy-transfer dynamics in the LHC II complex of higher plants: modified redfield approach J Phys Chem B 108: 10363–10375

    Article  CAS  Google Scholar 

  • Pålsson LO, Spangfort MD, Gulbinas V, Gillbro T, (1994) Ultrafast chlorophyll b-chlorophyll a excitation energy transfer in the isolated light harvesting complex, LHC II, of green plants FEBS Lett 339: 134–138

    Article  PubMed  Google Scholar 

  • Pearlstein RM, (1991) Theoretical interpretation of antenna spectra. In: Scheer H, (ed) Chlorophylls, CRC Press, Boca Raton pp 1047–1078

    Google Scholar 

  • Peterman EJG, Gradinaru CC, Calkoen F, Borst JC, van Grondelle R, van Amerongen H, (1997) Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching Biochem 36: 12208–12215

    Article  CAS  Google Scholar 

  • Peterman EJG, Hobe S, Calkoen F, van Grondelle R, Paulsen H, van Amerongen H, (1996) Low-temperature spectroscopy of monomeric and trimeric forms of reconstituted light-harvesting chlorophyll a/b complex Biochim Biophys Acta 1273: 171–174

    Article  Google Scholar 

  • Pieper J, Rätsep M, Jankowiak R, Irrgang K-D, Voigt J, Renger G, Small GJ, (1999) Qy-level structure and dynamics of solubilized light-harvesting complex II of green plants: pressure and hole burning studies J Phys Chem A 103: 2412–2421

    Article  CAS  Google Scholar 

  • Reddy NRS, van Amerongen H, Kwa SLS, van Grondelle R, Small GJ, (1994) Low-energy exciton level structure and dynamics in light harvesting complex II trimers from the Chl a/b antenna complex of Photosystem II J Phys Chem 98: 4729–4735

    Article  CAS  Google Scholar 

  • Remelli R, Varotto C, Sandonà D, Croce R, Bassi R, (1999) Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophore-binding residues J Biol Chem 274: 33510–33521

    Article  CAS  PubMed  Google Scholar 

  • Ruban AV, Calkoen F, Kwa SLS, van Grondelle R, Horton P, Dekker JP, (1997) Characterisation of LHC II in the aggregated state by linear and circular dichroism spectroscopy Biochim Biophys Acta 1321: 61–70

    Article  CAS  Google Scholar 

  • Salverda JM, Vengris M, Krueger BP, Scholes GD, Czarnoleski AR, Novoderezhkin V, van Amerongen H, van Grondelle R, (2003) Energy transfer in light-harvesting complexes LHC II and CP29 of spinach studied with three pulse echo peak shift and transient grating Biophys J 84: 450–465

    Article  CAS  PubMed  Google Scholar 

  • Stewart JJP, (1989) Optimization of parameters for semiempirical methods I Method J Comput Chem 10: 209–220

    Article  CAS  Google Scholar 

  • Tracewell CA, Vrettos JS, Bautista JA, Frank HA, Brudvig GW, (2001) Carotenoid photooxidation in Photosystem II Arch Biochem Biophys 385: 61–69

    Article  CAS  PubMed  Google Scholar 

  • van Amerongen H, van Grondelle R, (2001) Understanding the energy transfer function of LHC II, the major light-harvesting complex of green plants J Phys Chem B 105: 604–617

    Article  CAS  Google Scholar 

  • Visser HM, Kleima FJ, van Stokkum IHM, van Grondelle R, van Amerongen H, (1996) Probing the many energy-transfer processes in the photosynthetic light-harvesting complex II at 77 K using energy-selective sub-picosecond transient absorption spectroscopy Chem Phys 210: 297–312

    Article  CAS  Google Scholar 

  • Wentworth M, Ruban AV, Horton P, (2003) Thermodynamic investigation into the mechanism of the chlorophyll fluorescence quenching in isolated Photosystem II light-harvesting complexes J Biol Chem 278: 21845–21850

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the Chinese group of Liu et al., who sent us their accurate co-ordinates of the LHC-II trimer prior to publication in the Brookhaven Data Bank. M.Sc. Elina Wük is acknowledged for helping in the literature search (42). JL acknowledges the scholarship form the Finnish Cultural Foundation, Financial support (JM, RK) from Academy of Finland is acknowledged (Contracts No. 74003, 204557 and 205475).

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Correspondence to Juha Linnanto.

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Linnanto, J., Martiskainen, J., Lehtovuori, V. et al. Excitation energy transfer in the LHC-II trimer: a model based on the new 2.72 Å structure. Photosynth Res 87, 267–279 (2006). https://doi.org/10.1007/s11120-005-9004-1

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