Structure-Function Relationship in Peridinin-Chlorophyll Proteins

  • Tomáš PolívkaEmail author
  • Eckhard Hofmann
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)


An important component of the photosynthetic apparatus is a light-harvesting system that captures light energy and transfers it efficiently to the reaction center. Depending on environmental conditions, photosynthetic antennas have adopted various strategies for this function. The water soluble antenna complex of dinoflagellates, peridinin–chlorophyll a protein (PCP), represents a unique light-harvesting strategy because, unlike other antenna systems which have a preponderance of chlorophyll, the carotenoid peridinin serves in PCP as the major light-harvesting pigment. The key structural feature of peridinin is a conjugated carbonyl group which makes the spectroscopic properties of peridinin very sensitive to its local environment. This property is a crucial factor for maintaining the high efficiency of energy transfer between peridinin and Chl a in PCP. PCP is also amenable to site-directed mutagenesis and reconstitution with different pigments, allowing to study effects of both pigment and amino acid exchange on energy transfer pathways within the complex. Since high resolution structures of native, reconstituted and mutated PCP complexes are now available, this knowledge provides an ideal platform to relate structural motifs to energy transfer pathways and efficiencies in PCP. This Chapter summarizes results of structural and spectroscopic investigations of PCP and related proteins, emphasizing the specific light-harvesting strategy developed by dinoflagellates.


Energy Transfer Intramolecular Charge Transfer Energy Transfer Efficiency Transient Absorption Spectrum Energy Transfer Rate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



– Bacteriochlorophyll;


– Circular dichroism;


– Chlorophyll;


– Electron nuclear double resonance;


– Electron paramagnetic resonance;


– Fucoxanthin chlorophyll protein;


– High salt PCP;


– Intramolecular charge transfer;


– Linear dichroism;


– Light harvesting complex;


– Main form PCP used when needed to distinguish from other forms;


– Modified neglect of differential overlap with partial single and double configuration interaction;


– Near infra red;


– Peridinin chlorophyll protein;


– Peridinin;


– Refolded PCP construct equivalent to the N-terminal domain of MFPCP;


– Visible



The authors thank Roger Hiller and Harry Frank for many years of collaboration on research described in this chapter. Harry Frank is greatly acknowledged for providing data for Fig. 3.12. TP thanks the Czech Science Foundation (P205/11/1164) for financial support. EH acknowledges support by the collaborative research center SFB480 (project C6) of the Deutsche Forschungsgemeinschaft.


  1. Alexandre MTA, Luhrs DC, van Stokkum IHM, Hiller R, Groot ML, Kennis JTM, van Grondelle R (2007) Triplet state dynamics in peridinin-chlorophyll a-protein: a new pathway of photoprotection in LHCs? Biophys J 93:2118–2128PubMedCentralPubMedCrossRefGoogle Scholar
  2. Bautista JA, Hiller RG, Sharples FP, Gosztola D, Wasielewski MR, Frank HA (1999a) Singlet and triplet energy transfer in the peridinin-chlorophyll a protein from Amphidinium carterae. J Phys Chem A 103:2267–2273CrossRefGoogle Scholar
  3. Bautista JA, Connors RE, Raju BB, Hiller RG, Sharples FP, Gosztola D, Wasielewski MR, Frank HA (1999b) Excited state properties of peridinin: observation of a solvent dependence of the lowest excited singlet state lifetime and spectral behavior unique among carotenoids. J Phys Chem B 103:8751–8758CrossRefGoogle Scholar
  4. Bonetti C, Alexandre MTA, Hiller RG, Kennis JTM, Grondelle R (2009) Chl a triplet quenching by peridinin in H-PCP and organic solvent revealed by step-scan FTIR time-resolved spectroscopy. Chem Phys 357:63–69CrossRefGoogle Scholar
  5. Bonetti C, Alexandre MTA, van Stokkum IHM, Hiller RG, Groot ML, van Grondelle R, Kennis JTM (2010) Identification of excited-state energy transfer and relaxation pathways in the peridinin-chlorophyll complex: an ultrafast mid-infrared study. Phys Chem Chem Phys 12:9256–9266PubMedCrossRefGoogle Scholar
  6. Brotosudarmo THP, Hofmann E, Hiller RG, Wormke S, Mackowski S, Zumbusch A, Brauchle C, Scheer H (2006) Peridinin-chlorophyll-protein reconstituted with chlorophyll mixtures: preparation, bulk and single molecule spectroscopy. FEBS Lett 580:5257–5262PubMedCrossRefGoogle Scholar
  7. Carbonera D, Giacometti G, Segre U, Hofmann E, Hiller RG (1999) Structure-based calculations of the optical spectra of the light-harvesting peridinin-chlorophyll-protein complexes from Amphidinium carterae and Heterocapsa pygmaea. J Phys Chem B 103:6349–6356CrossRefGoogle Scholar
  8. Damjanovic A, Ritz T, Schulten K (2000) Excitation transfer in the peridinin-chlorophyll-protein of Amphidinium carterae. Biophys J 79:1695–1705PubMedCentralPubMedCrossRefGoogle Scholar
  9. Debreczeny MP, Wasielewski MR, Shinoda S, Osuka A (1997) Singlet-singlet energy transfer mechanisms in covalently-linked fucoxanthin- and zeaxanthin-pyropheophorbide molecules. J Am Chem Soc 119:6407–6414CrossRefGoogle Scholar
  10. Di Valentin M, Ceola S, Salvadori E, Agostini G, Carbonera D (2008a) Identification by time-resolved EPR of the peridinins directly involved in chlorophyll triplet quenching in the peridinin-chlorophyll a-protein from Amphidinium carterae. Biochim Biophys Acta 1777:186–195PubMedCrossRefGoogle Scholar
  11. Di Valentin M, Ceola S, Agostini G, Giacometti GM, Angerhofer A, Crescenzi O, Barone V, Carbonera D (2008b) Pulse ENDOR and density functional theory on the peridinin triplet state involved in the photo-protective mechanism in the peridinin-chlorophyll a-protein from Amphidinium carterae. Biochim Biophys Acta 1777:295–307PubMedCrossRefGoogle Scholar
  12. Di Valentin M, Salvadori E, Agostini G, Biasibetti F, Ceola S, Hiller R, Giacometti GM, Carbonera D (2010) Triplet-triplet energy transfer in the major intrinsic light-harvesting complex of Amphidinium carterae as revealed by ODMR and EPR spectroscopies. Biochim Biophys Acta 1797:1759–1767PubMedCrossRefGoogle Scholar
  13. Förster T (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys 437:55–75CrossRefGoogle Scholar
  14. Frank HA, Bautista JA, Josue J, Pendon Z, Hiller RG, Sharples FP, Gosztola D, Wasielewski MR (2000) Effect of the solvent environment on the spectroscopic properties and dynamics of the lowest excited states of carotenoids. J Phys Chem B 104:4569–4577CrossRefGoogle Scholar
  15. Gildenhoff N, Herz J, Gundermann K, Büchel C, Wachtveitl J (2010) The excitation energy transfer in the trimeric fucoxanthin-chlorophyll protein from Cyclotella meneghiniana analyzed by polarized transient absorption spectroscopy. Chem Phys 373:104–109CrossRefGoogle Scholar
  16. Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Chem 14:47–77CrossRefGoogle Scholar
  17. Govind N, Roman S, Iglesias-Prieto R, Trench R, Triplett E, Prezelin BB (1990) An analysis of the light-harvesting peridinin-chlorophyll a-proteins from dinoflagellates by immunoblotting techniques. Proc R Soc Lond B Biol Sci 240:187–195CrossRefGoogle Scholar
  18. Green RB, Parson WW (eds) (2003) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, DordrechtGoogle Scholar
  19. Haxo FT, Kycia JH, Somers GF, Bennett A, Siegelman HW (1976) Peridinin-chlorophyll a proteins of the dinoflagellate Amphidinium carterae (Plymouth 450). Plant Physiol 57:297–303PubMedCentralPubMedCrossRefGoogle Scholar
  20. Herek JL, Fraser NJ, Pullerits T, Martinsson P, Polívka T, Scheer H, Cogdell RG, Sundström V (2000) B800-B850 energy transfer mechanism in bacterial LH2 complexes investigated by B800 pigment exchange. Biophys J 78:2590–2596PubMedCentralPubMedCrossRefGoogle Scholar
  21. Hiller RG, Wrench PM, Gooley AP, Shoebridge G, Breton J (1993) The major intrinsic light-harvesting protein of Amphidinium: characterization and relation to other light-harvesting proteins. Photochem Photobiol 57:125–131PubMedCrossRefGoogle Scholar
  22. Hiller RG, Wrench PM, Sharples FP (1995) The light-harvesting chlorophyll a-c-binding protein of dinoflagellates: a putative polyprotein. FEBS Lett 363:175–178PubMedCrossRefGoogle Scholar
  23. Hofmann E (1999) Strukturanalyse der Lichtsammler Peridinin-Chlorophyll a-Proteine (PCPs) von Amphidinium carterae und Heterocapsa pygmaea. Doctoral dissertation, University KonstanzGoogle Scholar
  24. Hofmann E, Wrench P, Sharples F, Hiller R, Welte W, Diederichs K (1996) Structural basis of light-harvesting by carotenoids: peridinin-chlorophyll- protein from Amphidinium carterae. Science 272:1788–1791PubMedCrossRefGoogle Scholar
  25. Ilagan RP, Shima S, Melkozernov A, Lin S, Blankenship RE, Sharples FP, Hiller RG, Birge RR, Frank HA (2004) Spectroscopic properties of the main-form and high-salt peridinin-chlorophyll a proteins from Amphidinium carterae. Biochemistry 43:1478–1487PubMedCrossRefGoogle Scholar
  26. Ilagan RP, Koscielecki JF, Hiller RG, Sharples FP, Gibson GN, Birge RR, Frank HA (2006a) Femtosecond time-resolved absorption spectroscopy of main-form and high-salt peridinin-chlorophyll a-proteins at low temperatures. Biochemistry 45:14052–14063PubMedCrossRefGoogle Scholar
  27. Ilagan RP, Chapp TW, Hiller RG, Sharples FP, Polívka T, Frank HA (2006b) Optical spectroscopic studies of light-harvesting by pigment-reconstituted peridinin-chlorophyll-proteins at cryogenic temperatures. Photosynth Res 90:5–15PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kleima FJ, Hofmann E, Gobets B, van Stockum IHM, van Grondelle R, Diederichs K, van Amerongen H (2000a) Förster excitation energy transfer in in peridinin-chlorophyll-a-protein. Biophys J 78:344–353PubMedCentralPubMedCrossRefGoogle Scholar
  29. Kleima FJ, Wendling M, Hofmann E, Peterman EJG, van Grondelle R, van Amerongen H (2000b) Peridinin chlorophyll a protein: relating structure and steady-state spectroscopy. Biochemistry 39:5184–5195PubMedCrossRefGoogle Scholar
  30. Koka P, Song PS (1977) Chromophore topography and binding environment of peridinin-chlorophyll a-protein complexes from marine dinoflagellate algae. Biochim Biophys Acta 495:220–231PubMedCrossRefGoogle Scholar
  31. Krikunova M, Lokstein H, Leupold D, Hiller RG, Voigt B (2006) Pigment-pigment interactions in PCP of Amphidinium carterae investigated by nonlinear polarization spectroscopy in the frequency domain. Biophys J 90:261–271PubMedCentralPubMedCrossRefGoogle Scholar
  32. Krueger BP, Lampoura SS, van Stokkum IHM, Papagiannakis E, Salverda JM, Gradinaru CC, Rutkauskas D, Hiller RG, van Grondelle R (2001) Energy transfer in the peridinin chlorophyll a protein of Amphidinium carterae studied by polarised transient absorption and target analysis. Biophys J 80:2843–2855PubMedCentralPubMedCrossRefGoogle Scholar
  33. Linden PA, Zimmermann J, Brixner T, Holt NE, Vaswani H, Hiller RG, Fleming GR (2004) Transient absorption study of peridinin and peridinin-chlorophyll-a-protein after two photon excitation. J Phys Chem B 108:10340–10345CrossRefGoogle Scholar
  34. Mackowski S, Wormke S, Brotosudarmo THP, Scheer H, Brauchle C (2008) Fluorescence spectroscopy of reconstituted peridinin-chlorophyll-protein complexes. Photosynth Res 95:253–260PubMedCrossRefGoogle Scholar
  35. Macpherson A, Hiller RG (2003) Light harvesting systems in chlorophyll-c containing algae. In: Green RB, Parson WW (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, Dordrecht, pp 323–352CrossRefGoogle Scholar
  36. Matthews BW, Fenna RE, Bolognesi MC, Schmid MF, Olson JM (1979) Structure of a bacteriochlorophyll a-protein from the green photosynthetic bacterium Prosthecochloris aestuarii. J Mol Biol 131:259–285PubMedCrossRefGoogle Scholar
  37. Miller DJ, Catmull J, Puskeiler R, Tweedale H, Sharples FP, Hiller RG (2005) Reconstitution of the peridinin-chlorophyll a protein (PCP): evidence for functional flexibility in chlorophyll binding. Photosynth Res 86:229–240PubMedCrossRefGoogle Scholar
  38. Mimuro M, Tamai N, Ishimaru T, Yamazaki I (1990) Characteristic fluorescence components in photosynthetic pigment system of a marine dinoflagellate, Protogonyaulax tamarensis, and excitation energy flow among them. Studies by means of steady-state and time-resolved fluorescence spectroscopy. Biochim Biophys Acta 1016:280–287CrossRefGoogle Scholar
  39. Niedzwiedzki DM, Jiang J, Lo CS, Blankenship RE (2013) Spectroscopic properties of the chlorophyll a–chlorophyll c2–peridinin–protein-complex (acpPC) from the coral symbiotic dinoflagellate Symbiodinium. Photosynth Res. doi: 10.1007/s11120-013-9794-5 Google Scholar
  40. Niklas J, Schulte T, Prakash S, van Gastel M, Hofmann E, Lubitz W (2007) Spin-density distribution of the carotenoid triplet state in the peridinin-chlorophyll-protein antenna. A Q-band pulse electron-nuclear double resonance and density functional theory study. J Am Chem Soc 129:15442–15443PubMedCrossRefGoogle Scholar
  41. Osuka A, Kume T (1998) Fucoxanthin- and peridinin-pheophorbide-alpha molecules as a new light-harvesting model. Tetrahedron Lett 39:655–658CrossRefGoogle Scholar
  42. Osuka A, Kume T, Haggquist GW, Jávorfi T, Lima JC, Melo E, Naqvi KR (1999) Photophysical characteristics of two model antenna systems: a fucoxanthin-pyropheoporbide dyad and its peridinin analogue. Chem Phys Lett 313:499–504CrossRefGoogle Scholar
  43. Papagiannakis E, Larsen DS, van Stokkum IHM, Vengris M, Hiller RG, van Grondelle R (2004) Resolving the excited state equilibrium of peridinin in solution. Biochemistry 43:15303–15309PubMedCrossRefGoogle Scholar
  44. Papagiannakis E, van Stokkum IHM, Fey H, Büchel C, van Grondelle R (2005) Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res 86:241–250PubMedCrossRefGoogle Scholar
  45. Papagiannakis E, Vengris M, Larsen DS, van Stokkum IHM, Hiller RG, van Grondelle R (2006) Use of ultrafast dispersed pump-dump-probe and pump-repump-probe spectroscopies to explore the light-induced dynamics of peridinin in solution. J Phys Chem B 110:512–521PubMedCrossRefGoogle Scholar
  46. Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134PubMedCentralPubMedCrossRefGoogle Scholar
  47. Polívka T, Pascher T, Sundström V, Hiller RG (2005) Tuning energy transfer in the peridinin-chlorophyll complex by reconstitution with different chlorophylls. Photosynth Res 86:217–227PubMedCrossRefGoogle Scholar
  48. Polívka T, van Stokkum IHM, Zigmantas D, van Grondelle R, Sundström V, Hiller RG (2006) Energy transfer in the major intrinsic light-harvesting complex from Amphidinium carterae. Biochemistry 45:8516–8526PubMedCrossRefGoogle Scholar
  49. Polívka T, Hiller RG, Frank HA (2007a) Spectroscopy of the peridinin – chlorophyll-a protein: insight into light-harvesting strategy of marine algae. Arch Biochem Biophys 458:111–120PubMedCrossRefGoogle Scholar
  50. Polívka T, Pellnor M, Melo E, Pascher T, Sundström V, Osuka A, Naqvi KR (2007b) Polarity-tuned energy transfer efficiency in artificial light-harvesting antennae containing carbonyl carotenoids peridinin and fucoxanthin. J Phys Chem C 111:467–476CrossRefGoogle Scholar
  51. Polívka T, Pascher T, Hiller RG (2008) Energy transfer in the peridinin-chlorophyll protein complex reconstituted with mixed chlorophyll sites. Biophys J 94:3198–3207PubMedCentralPubMedCrossRefGoogle Scholar
  52. Premvardhan L, Papagiannakis E, Hiller RG, van Grondelle R (2005) The charge-transfer character of the S0-S2 transition in the carotenoid peridinin is revealed by stark spectroscopy. J Phys Chem B 109:15589–15597PubMedCrossRefGoogle Scholar
  53. Prézelin BB, Haxo FT (1976) Purification and characterization of peridinin-chlorophyll a-proteins from the marine dinoflagellates Glenodinium sp. and Gonyaulax polyedra. Planta 128:133–141PubMedCrossRefGoogle Scholar
  54. Scholes GD (2003) Long-range resonance energy transfer in molecular systems. Annu Rev Phys Chem 54:57–87PubMedCrossRefGoogle Scholar
  55. Schulte T, Niedzwiedzki DM, Birge RR, Hiller RG, Polívka T, Hofmann E, Frank HA (2009a) Identification of a single peridinin sensing Chl a excitation in reconstituted PCP by crystallography and spectroscopy. Proc Natl Acad Sci U S A 106:20764–20769PubMedCentralPubMedCrossRefGoogle Scholar
  56. Schulte T, Sharples FP, Hiller RG, Hofmann E (2009b) X-ray structure of the high-salt form of the peridinin-chlorophyll-a protein from the dinoflagellate Amphidinium carterae: modulation of the spectral properties of pigments by the protein environment. Biochemistry 48:4466–4475PubMedCrossRefGoogle Scholar
  57. Schulte T, Hiller RG, Hofmann E (2010) X-ray structures of the peridinin-chlorophyll-protein reconstituted with different chlorophylls. FEBS Lett 584:973–978PubMedCrossRefGoogle Scholar
  58. Sharples FP, Wrench PM, Ou KL, Hiller RG (1996) Two distinct forms of the peridinin-chlorophyll alpha-protein from Amphidinium carterae. Biochim Biophys Acta 1276:117–123PubMedCrossRefGoogle Scholar
  59. Shinoda S, Osuka A, Nishimura Y, Yamazaki I (1995) Synthesis of natural carotenoid-modified pyropheophorbide dyads for investigation of carotenoid-chlorophyll excited state interactions. Chem Lett 12:1139–1140CrossRefGoogle Scholar
  60. Šlouf V, Fuciman M, Johanning S, Hofmann E, Frank HA, Polívka T (2013) Low temperature time-resolved spectroscopic study of the major light-harvesting complex of Amphidinium carterae. Photosynth Res 117:257–265PubMedCrossRefGoogle Scholar
  61. Song PS, Koka P, Berzelin BB, Haxo FT (1976) Molecular topology of photosynthetic light-harvesting pigment complex, peridinin-chlorophyll-a-protein, from marine dinoflagellates. Biochemistry 15:4422–4427PubMedCrossRefGoogle Scholar
  62. Tronrud DE, Wen J, Gay L, Blankenship RE (2009) The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosyn Res 100:79–87PubMedCrossRefGoogle Scholar
  63. van Stokkum IHM, Papagiannakis E, Vengris M, Salverda JM, Polívka T, Zigmantas D, Larsen DS, Lampoura SS, Hiller RG, van Grondelle R (2009) Inter-pigment interactions in the peridinin chlorophyll protein studied by global and target analysis of time resolved absorption spectra. Chem Phys 357:70–78CrossRefGoogle Scholar
  64. van Tassle AJ, Prantil MA, Hiller RG, Fleming GR (2007) Excited state structural dynamics of the charge transfer state of peridinin. Isr J Chem 47:17–24CrossRefGoogle Scholar
  65. Wormke S, Mackowski S, Brotosudarmo THP, Jung C, Zurnbusch A, Ehrl M, Scheer H, Hofmann E, Hiller RG, Brauchle C (2007) Monitoring fluorescence of individual chromophores in peridinin chlorophyll-protein complex using single molecule spectroscopy. Biochim Biophys Acta 1767:956–964PubMedCrossRefGoogle Scholar
  66. Zigmantas D, Polívka T, Hiller RG, Yartsev A, Sundström V (2001) Spectroscopic and dynamic properties of the peridinin lowest singlet excited states. J Phys Chem A 105:10296–10306CrossRefGoogle Scholar
  67. Zigmantas D, Hiller RG, Polívka T, Sundström V (2002) Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc Natl Acad Sci U S A 99:16760–16765PubMedCentralPubMedCrossRefGoogle Scholar
  68. Zigmantas D, Hiller RG, Yartsev A, Sundström V, Polívka T (2003) Dynamics of excited states of the carotenoid peridinin in polar solvents: dependence on excitation wavelength, viscosity, and temperature. J Phys Chem B 107:5339–5348CrossRefGoogle Scholar
  69. Zigmantas D, Hiller RG, Sharples FP, Frank HA, Sundström V, Polívka T (2004) Effect of a conjugated carbonyl group on the photophysical properties of carotenoids. Phys Chem Chem Phys 6:3009–3016CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  1. 1.Faculty of Science, Department of Physics and BiophysicsUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Faculty of Biology and Biotechnology, Department of BiophysicsRuhr-University BochumBochumGermany

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