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Spectroscopic Characterization of the Excitation Energy Transfer in the Fucoxanthin–Chlorophyll Protein of Diatoms

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Abstract

We characterized the energy transfer pathways in the fucoxanthin–chlorophyll protein (FCP) complex of the diatom Cyclotella meneghiniana by conducting ultrafast transient absorption measurements. This light harvesting antenna has a distinct pigment composition and binds chlorophyll a (Chl-a), fucoxanthin and chlorophyll c (Chl-c) molecules in a 4:4:1 ratio. We find that upon excitation of fucoxanthin to its S2 state, a significant amount of excitation energy is transferred rapidly to Chl-a. The ensuing dynamics illustrate the presence of a complex energy transfer network that also involves energy transfer from the unrelaxed or ‘hot’ intermediates. Chl-c to Chl-a energy transfer occurs on a timescale of a 100 fs. We observe no significant spectral evolution in the Chl-a region of the spectrum. We have applied global and target analysis to model the measured excited state dynamics and estimate the spectra of the states involved; the energy transfer network is discussed in relation to the pigment organization of the FCP complex.

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Abbreviations

Chl:

chlorophyll

EADS:

evolution-associated difference spectrum

EET:

excitation energy transfer

ESA:

excited-state absorption

FCP:

fucoxanthin–chlorophyll protein

IC:

internal conversion

ICT:

intramolecular charge-transfer

LHC:

light-harvesting complex

PCP:

peridinin–chlorophyll protein

SADS:

species-associated difference spectrum

SE:

stimulated emission

References

  • C Büchel (2003) ArticleTitleFucoxanthin–chlorophyll proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states Biochemistry 42 13027–13034 Occurrence Handle10.1021/bi0349468 Occurrence Handle14596618

    Article  PubMed  Google Scholar 

  • R Croce MG Muller R Bassi AR Holzwarth (2001) ArticleTitleCarotenoid-to-chlorophyll energy transfer in recombinant major light-harvesting complex (LHCII) of higher plants. I. Femtosecond transient absorption measurements Biophys J 80 901–915 Occurrence Handle11159457

    PubMed  Google Scholar 

  • M Eppard E Rhiel (1998) ArticleTitleThe genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family Mol Gen Genet 260 335–345 Occurrence Handle10.1007/s004380050902 Occurrence Handle9870698

    Article  PubMed  Google Scholar 

  • HA Frank RJ Cogdell (1996) ArticleTitleCarotenoids in photosynthesis Photochem Photobiol 63 257–264 Occurrence Handle8881328

    PubMed  Google Scholar 

  • B Gobets JTM Kennis JA Ihalainen M Brazzoli R Croce IHM Stokkum Particlevan R Bassi JP Dekker H Amerongen Particlevan GR Fleming R Grondelle Particlevan (2001) ArticleTitleLight harvesting by chlorophylls and carotenoids in the Photosystem I core complex of Synechococcus elongatus: a fluorescence upconversion study J Phys Chem B 104 4485–4494

    Google Scholar 

  • CC Gradinaru IHM Stokkum Particlevan AA Pascal R Grondelle Particlevan H Amerongen Particlevan (2000) ArticleTitleIdentifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multicolor, femtosecond pump-probe study J Phys Chem B 104 9330–9342 Occurrence Handle10.1021/jp001752i

    Article  Google Scholar 

  • BR Green W Kühlbrandt (1995) ArticleTitleSequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII Photosynth Res 44 139–148 Occurrence Handle10.1007/BF00018304

    Article  Google Scholar 

  • JA Haugan G Englert E Glinz S Liaaenjensen (1992) ArticleTitleAlgal carotenoids. 48. Structural assignments of geometrical-isomers of fucoxanthin Acta Chem Scand 46 389–395

    Google Scholar 

  • JL Herek T Polivka T Pullerits GJS Fowler CN Hunter V Sundström (1998) ArticleTitleUltrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes Biochemistry 37 7057–7061 Occurrence Handle9585514

    PubMed  Google Scholar 

  • E Hofmann PM Wrench FP Sharples RG Hiller W Welte K Diederichs (1996) ArticleTitleStructural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae Science 272 1788–1791

    Google Scholar 

  • AR Holzwarth (1996) Data analysis of time-resolved measurements J Amesz AJ Hoff (Eds) Biophysical Techniques in Photosynthesis Kluwer Academic Publishers Dordrecht, The Netherlands 75–92

    Google Scholar 

  • SW Jeffrey (1972) ArticleTitlePreparation and some properties of crystalline chlorophyll-C1 and C2 from marine algae Biochim Biophys Acta 279 15–33 Occurrence Handle4652559

    PubMed  Google Scholar 

  • JE Johansen WA Svec S Liaaenje FT Haxo (1974) ArticleTitleAlgal carotenoids. 10. Carotenoids of Dinophyceae Phytochemistry 13 2261–2271 Occurrence Handle10.1016/0031-9422(74)85038-7

    Article  Google Scholar 

  • BP Krueger J Yom PJ Walla GR Fleming (1999) ArticleTitleObservation of the S1 state of spheroidene in LH2 by two-photon fluorescence excitation Chem Phys Lett 310 57–64 Occurrence Handle10.1016/S0009-2614(99)00729-0

    Article  Google Scholar 

  • BP Krueger SS Lampoura IHM Stokkum Particlevan E Papagiannakis JM Salverda CC Gradinaru D Rutkauskas RG Hiller R Grondelle Particlevan (2001) ArticleTitleEnergy transfer in the peridinin chlorophyll-a protein of Amphidinium carterae studied by polarized transient absorption and target analysis Biophys J 80 2843–2855 Occurrence Handle11371458

    PubMed  Google Scholar 

  • DS Larsen M Vengris IHM Stokkum Particlevan M Horst Particlevan der FL Weerd Particlede KJ Hellingwerf R Grondelle Particlevan (2004) ArticleTitlePhotoisomerization and photoionization of the photoactive yellow protein chromophore in solution Biophys J 86 2538–2550 Occurrence Handle15041690

    PubMed  Google Scholar 

  • HK Lichtenthaler (1987) ArticleTitleChlorophylls and carotenoids – pigments of photosynthetic biomembranes Meth Enzymol 148 350–382

    Google Scholar 

  • ZF Liu HC Yan KB Wang TY Kuang JP Zhang LL Gui XM An WR Chang (2004) ArticleTitleCrystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 287–292 Occurrence Handle15029188

    PubMed  Google Scholar 

  • VI Novoderezhkin MA Palacios H Amerongen Particlevan R Grondelle Particlevan (2004) ArticleTitleEnergy-transfer dynamics in the LHCII complex of higher plants: modified redfield approach J Phys Chem B 108 10363–10375 Occurrence Handle10.1021/jp0496001

    Article  Google Scholar 

  • A Osuka T Kume GW Haggquist T Javorfi JC Lima E Melo KR Naqvi (1999) ArticleTitlePhotophysical characteristics of two model antenna systems: a fucoxanthin-pyropheoporbide dyad and its peridinin analogue Chem Phys Lett 313 499–504 Occurrence Handle10.1016/S0009-2614(99)01098-2

    Article  Google Scholar 

  • E Papagiannakis JTM Kennis IHM Stokkum Particlevan RJ Cogdell R Grondelle Particlevan (2002) ArticleTitleAn alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting Proc Natl Acad Sci USA 99 6017–6022 Occurrence Handle10.1073/pnas.092626599 Occurrence Handle11972067

    Article  PubMed  Google Scholar 

  • E Papagiannakis IHM Stokkum Particlevan R Grondelle Particlevan RA Niederman D Zigmantas V Sundström T Polívka (2003) ArticleTitleA near-infrared transient absorption study of the excited-state dynamics of the carotenoid spirilloxanthin in solution and in the LH1 complex of Rhodospirillum rubrum J Phys Chem B 107 11216–11223 Occurrence Handle10.1021/jp034931j

    Article  Google Scholar 

  • E Papagiannakis DS Larsen IHM Stokkum Particlevan M Vengris R Hiller R Grondelle Particlevan (2004) ArticleTitleResolving the excited state equilibrium of peridinin in solution Biochemistry 43 15303–15309 Occurrence Handle10.1021/bi047977r Occurrence Handle15581342

    Article  PubMed  Google Scholar 

  • EJG Peterman FM Dukker R Grondelle Particlevan H Amerongen Particlevan (1995) ArticleTitleChlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants Biophys J 69 2670–2678 Occurrence Handle8599673

    PubMed  Google Scholar 

  • EJG Peterman R Monshouwer IHM Stokkum Particlevan R Grondelle Particlevan H Amerongen Particlevan (1997) ArticleTitleUltrafast singlet excitation transfer from carotenoids to chlorophylls via different pathways in light-harvesting complex II of higher plants Chem Phys Lett 264 279–284 Occurrence Handle10.1016/S0009-2614(96)01334-6

    Article  Google Scholar 

  • T Polívka V Sundström (2004) ArticleTitleUltrafast dynamics of carotenoid excited states. From solution to natural and artificial systems Chem Rev 104 2021–2071 Occurrence Handle15080720

    PubMed  Google Scholar 

  • JM Salverda (2003) Interacting pigments in light-harvesting complexes studied with nonlinear spectroscopy Vrije Universiteit Amsterdam

    Google Scholar 

  • H Amerongen Particlevan R Grondelle Particlevan (2001) ArticleTitleUnderstanding the energy transfer function of LHCII, the major light-harvesting complex of green plants J Phys Chem B 105 604–617 Occurrence Handle10.1021/jp0028406

    Article  Google Scholar 

  • R Grondelle Particlevan (1985) ArticleTitleExcitation energy transfer, trapping and annihilation in photosynthetic systems Biochim Biophys Acta 811 147–195

    Google Scholar 

  • R Grondelle Particlevan JP Dekker T Gillbro V Sundström (1994) ArticleTitleEnergy-transfer and trapping in photosynthesis Biochim Biophys Acta 1187 1–65 Occurrence Handle10.1016/0005-2728(94)90166-X

    Article  Google Scholar 

  • IHM Stokkum Particlevan DS Larsen R Grondelle Particlevan (2004a) ArticleTitleGlobal and target analysis of time-resolved spectra Biochim Biophys Acta 1657 82–104

    Google Scholar 

  • IHM Stokkum Particlevan DS Larsen R Grondelle Particlevan (2004b) ArticleTitleErratum to “Global and target analysis of time-resolved spectra” Biochim Biophys Acta 1658 82–104

    Google Scholar 

  • PJ Walla PA Linden K Ohta GR Fleming (2002) ArticleTitleExcited-state kinetics of the carotenoid S1 state in LHC II and two-photon excitation spectra of lutein and beta-carotene in solution: efficient car S1→Chl electronic energy transfer via hot S1 states? J Phys Chem A 106 1909–1916 Occurrence Handle10.1021/jp011495x

    Article  Google Scholar 

  • JP Zhang LH Skibsted R Fujii Y Koyama (2001) ArticleTitleTransient absorption from the 1B − u state of all-trans-beta-carotene newly identified in the near-infrared region Photochem Photobiol 73 219–222 Occurrence Handle10.1562/0031-8655(2001)073<0219:TAFTUS>2.0.CO;2 Occurrence Handle11281016

    Article  PubMed  Google Scholar 

  • D Zigmantas RG Hiller FP Sharples HA Frank V Sundstrom T Polívka (2004) ArticleTitleEffect of a conjugated carbonyl group on the photophysical properties of carotenoids Phys Chem Chem Phys 6 3009–3016 Occurrence Handle10.1039/b315786e

    Article  Google Scholar 

  • D Zigmantas RG Hiller V Sundström T Polívka (2002) ArticleTitleCarotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state Proc Natl Acad Sci USA 99 16760–16765 Occurrence Handle10.1073/pnas.262537599 Occurrence Handle12486228

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Physics and Astronomy, Faculty of Sciences, Vrije Universiteit, De Boelelaan 1081, 1081, HV, Amsterdam, The Netherlands

    Emmanouil Papagiannakis, Ivo H.M. van Stokkum & Rienk van Grondelle

  2. Institute of Botany, University of Frankfurt, Siesmayerstrasse 70, 60323, Frankfurt, Germany

    Holger Fey & Claudia Büchel

Authors
  1. Emmanouil Papagiannakis
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  2. Ivo H.M. van Stokkum
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  3. Holger Fey
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  4. Claudia Büchel
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  5. Rienk van Grondelle
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Correspondence to Emmanouil Papagiannakis.

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Papagiannakis, E., H.M. van Stokkum, I., Fey, H. et al. Spectroscopic Characterization of the Excitation Energy Transfer in the Fucoxanthin–Chlorophyll Protein of Diatoms. Photosynth Res 86, 241–250 (2005). https://doi.org/10.1007/s11120-005-1003-8

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  • DOI: https://doi.org/10.1007/s11120-005-1003-8

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