Photosynthesis Research

, Volume 131, Issue 1, pp 105–117 | Cite as

Ultrafast spectroscopy tracks carotenoid configurations in the orange and red carotenoid proteins from cyanobacteria

  • Václav Šlouf
  • Valentyna Kuznetsova
  • Marcel Fuciman
  • Céline Bourcier de Carbon
  • Adjélé Wilson
  • Diana Kirilovsky
  • Tomáš Polívka
Original Article

Abstract

A quenching mechanism mediated by the orange carotenoid protein (OCP) is one of the ways cyanobacteria protect themselves against photooxidative stress. Here, we present a femtosecond spectroscopic study comparing OCP and RCP (red carotenoid protein) samples binding different carotenoids. We confirmed significant changes in carotenoid configuration upon OCP activation reported by Leverenz et al. (Science 348:1463–1466. doi: 10.1126/science.aaa7234, 2015) by comparing the transient spectra of OCP and RCP. The most important marker of these changes was the magnitude of the transient signal associated with the carotenoid intramolecular charge-transfer (ICT) state. While OCP with canthaxanthin exhibited a weak ICT signal, it increased significantly for canthaxanthin bound to RCP. On the contrary, a strong ICT signal was recorded in OCP binding echinenone excited at the red edge of the absorption spectrum. Because the carbonyl oxygen responsible for the appearance of the ICT signal is located at the end rings of both carotenoids, the magnitude of the ICT signal can be used to estimate the torsion angles of the end rings. Application of two different excitation wavelengths to study OCP demonstrated that the OCP sample contains two spectroscopically distinct populations, none of which is corresponding to the photoactivated product of OCP.

Keywords

Orange carotenoid protein Red carotenoid protein Non-photochemical quenching Intramolecular charge-transfer state Ultrafast spectroscopy 

Supplementary material

11120_2016_302_MOESM1_ESM.pdf (261 kb)
Supplementary material 1 (PDF 260 kb)

References

  1. Bautista JA, Connors RE, Raju BB et al (1999) 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 103:8751–8758. doi:10.1021/jp9916135 CrossRefGoogle Scholar
  2. Berera R, van Stokkum IHM, Gwizdala M et al (2012) The photophysics of the orange carotenoid protein, a light-powered molecular switch. J Phys Chem B 116:2568–2574. doi:10.1021/jp2108329 CrossRefPubMedGoogle Scholar
  3. Berera R, Gwizdala M, van Stokkum IHM et al (2013) Excited states of the inactive and active forms of the orange carotenoid protein. J Phys Chem B 117:9121–9128. doi:10.1021/jp307420p CrossRefPubMedGoogle Scholar
  4. Billsten HH, Bhosale P, Yemelyanov A et al (2003) Photophysical properties of xanthophylls in carotenoproteins from human retinas. Photochem Photobiol 78:138–145. doi:10.1562/0031-8655(2003)0780138PPOXIC2.0.CO2 CrossRefPubMedGoogle Scholar
  5. Billsten HH, Pan J, Sinha S et al (2005) Excited-state processes in the carotenoid zeaxanthin after excess energy excitation. J Phys Chem A 109:6852–6859. doi:10.1021/jp052227s CrossRefPubMedGoogle Scholar
  6. Bode S, Quentmeier CC, Liao P-N et al (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci U S A 106:12311–12316. doi:10.1073/pnas.0903536106 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Britton G, Liaaen-Jensen S, Pfander H (2004) Carotenoids: handbook. Birkhäuser, BaselCrossRefGoogle Scholar
  8. Chábera P, Fuciman M, Hříbek P, Polívka T (2009) Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids. Phys Chem Chem Phys 11:8795–8803. doi:10.1039/b909924g CrossRefPubMedGoogle Scholar
  9. Chábera P, Durchan M, Shih PM et al (2011) Excited-state properties of the 16 kDa red carotenoid protein from Arthrospira maxima. Biochim Biophys Acta Bioenerg 1807:30–35. doi:10.1016/j.bbabio.2010.08.013 CrossRefGoogle Scholar
  10. De Carbon CB, Thurotte A, Wilson A et al (2015) Biosynthesis of soluble carotenoid holoproteins in Escherichia coli. Sci Rep 5:9085. doi:10.1038/srep09085 CrossRefPubMedCentralGoogle Scholar
  11. Dreuw A (2006) Influence of geometry relaxation on the energies of the S1 and S2 states of violaxanthin, zeaxanthin, and lutein. J Phys Chem A 110:4592–4599. doi:10.1021/jp057385y CrossRefPubMedGoogle Scholar
  12. Durchan M, Fuciman M, Šlouf V et al (2012) Excited-state dynamics of monomeric and aggregated carotenoid 8′-apo-β-carotenal. J Phys Chem A 116:12330–12338. doi:10.1021/jp310140k CrossRefPubMedGoogle Scholar
  13. Enriquez MM, Fuciman M, Lafountain AM et al (2010) The intramolecular charge transfer state in carbonyl-containing polyenes and carotenoids. J Phys Chem B 114:12416–12426. doi:10.1021/jp106113h CrossRefPubMedPubMedCentralGoogle Scholar
  14. Frank HA, Bautista JA, Josue J et al (2000) Effect of the solvent environment on the spectroscopic properties and dynamics of the lowest excited states of carotenoids. J Phys Chem B 104:4569–4577. doi:10.1021/jp000079u CrossRefGoogle Scholar
  15. Fuciman M, Keşan G, LaFountain AM et al (2015) Tuning the spectroscopic properties of aryl carotenoids by slight changes in structure. J Phys Chem B 119:1457–1467. doi:10.1021/jp512354r CrossRefPubMedGoogle Scholar
  16. Gildenhoff N, Amarie S, Gundermann K et al (2010) Oligomerization and pigmentation dependent excitation energy transfer in fucoxanthin-chlorophyll proteins. Biochim Biophys Acta Bioenerg 1797:543–549. doi:10.1016/j.bbabio.2010.01.024 CrossRefGoogle Scholar
  17. Gupta S, Guttman M, Leverenz RL et al (2015) Local and global structural drivers for the photoactivation of the orange carotenoid protein. Proc Natl Acad Sci U S A 112:E5567–E5574. doi:10.1073/pnas.1512240112 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Holt TK, Krogmann DW (1981) A carotenoid-protein from cyanobacteria. Biochim Biophys Acta Bioenerg 637:408–414. doi:10.1016/0005-2728(81)90045-1 CrossRefGoogle Scholar
  19. Holt NE, Zigmantas D, Valkunas L et al (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436. doi:10.1126/science.1105833 CrossRefPubMedGoogle Scholar
  20. Ihalainen JA, D’Haene S, Yeremenko N et al (2005) Aggregates of the chlorophyll-binding protein IsiA (CP43′) dissipate energy in cyanobacteria. Biochemistry 44:10846–10853. doi:10.1021/bi0510680 CrossRefPubMedGoogle Scholar
  21. Kerfeld CA, Sawaya MR, Brahmandam V et al (2003) The crystal structure of a cyanobacterial water-soluble carotenoid binding protein. Structure 11:55–65. doi:10.1016/S0969-2126(02)00936-X CrossRefPubMedGoogle Scholar
  22. Keşan G, Litvín R, Bína D et al (2016) Efficient light-harvesting using non-carbonyl carotenoids: energy transfer dynamics in the VCP complex from Nannochloropsis oceanica. Biochim Biophys Acta Bioenerg 1857:370–379. doi:10.1016/j.bbabio.2015.12.011 CrossRefGoogle Scholar
  23. Kirilovsky D (2007) Photoprotection in cyanobacteria: the orange carotenoid protein (OCP)-related non-photochemical-quenching mechanism. Photosynth Res 93:7–16. doi:10.1007/s11120-007-9168-y CrossRefPubMedGoogle Scholar
  24. Kish E, Pinto MMM, Kirilovsky D et al (2015) Echinenone vibrational properties: from solvents to the orange carotenoid protein. Biochim Biophys Acta Bioenerg 1847:1044–1054. doi:10.1016/j.bbabio.2015.05.010 CrossRefGoogle Scholar
  25. Leverenz RL, Jallet D, Li M-D et al (2014) Structural and functional modularity of the orange carotenoid protein: distinct roles for the N- and C-terminal domains in cyanobacterial photoprotection. Plant Cell 26:426–437. doi:10.1105/tpc.113.118588 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Leverenz RL, Sutter M, Wilson A et al (2015) A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection. Science 348:1463–1466. doi:10.1126/science.aaa7234 CrossRefPubMedGoogle Scholar
  27. Niedzwiedzki DM, Liu H, Blankenship RE (2014) Excited State Properties of 3′-hydroxyechinenone in solvents and in the orange carotenoid protein from Synechocystis sp. PCC 6803. J Phys Chem B 118:6141–6149. doi:10.1021/jp5041794 CrossRefPubMedGoogle Scholar
  28. Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314. doi:10.1016/j.pbi.2013.03.011 CrossRefPubMedGoogle Scholar
  29. Papagiannakis E, Larsen DS, van Stokkum IHM et al (2004) Resolving the excited state equilibrium of peridinin in solution. Biochemistry 43:15303–15309. doi:10.1021/bi047977r CrossRefPubMedGoogle Scholar
  30. Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 104:2021–2072. doi:10.1021/cr020674n CrossRefPubMedGoogle Scholar
  31. Polívka T, Kerfeld CA, Pascher T, Sundström V (2005) Spectroscopic properties of the carotenoid 3′-hydroxyechinenone in the orange carotenoid protein from the cyanobacterium Arthrospira maxima. Biochemistry 44:3994–4003. doi:10.1021/bi047473t CrossRefPubMedGoogle Scholar
  32. Polívka T, van Stokkum IHM, Zigmantas D et al (2006) Energy transfer in the major intrinsic light-harvesting complex from Amphidinium carterae. Biochemistry 45:8516–8526. doi:10.1021/bi060265b CrossRefPubMedGoogle Scholar
  33. Polívka T, Hiller RG, Frank HA (2007) Spectroscopy of the peridinin-chlorophyll-a protein: insight into light-harvesting strategy of marine algae. Arch Biochem Biophys 458:111–120. doi:10.1016/j.abb.2006.10.006 CrossRefPubMedGoogle Scholar
  34. Polívka T, Chábera P, Kerfeld CA (2013) Carotenoid-protein interaction alters the S1 energy of hydroxyechinenone in the Orange Carotenoid Protein. Biochim Biophys Acta Bioenerg 1827:248–254. doi:10.1016/j.bbabio.2012.10.005 CrossRefGoogle Scholar
  35. Punginelli C, Wilson A, Routaboul J-M, Kirilovsky D (2009) Influence of zeaxanthin and echinenone binding on the activity of the orange carotenoid protein. Biochim Biophys Acta Bioenerg 1787:280–288. doi:10.1016/j.bbabio.2009.01.011 CrossRefGoogle Scholar
  36. Redeckas K, Voiciuk V, Vengris M (2016) Investigation of the S1/ICT equilibrium in fucoxanthin by ultrafast pump–dump–probe and femtosecond stimulated Raman scattering spectroscopy. Photosynth Res 128:169–181. doi:10.1007/s11120-015-0215-9 CrossRefPubMedGoogle Scholar
  37. Ruban AV, Berera R, Ilioaia C et al (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578. doi:10.1038/nature06262 CrossRefPubMedGoogle Scholar
  38. Shima S, Ilagan RP, Gillespie N et al (2003) Two-photon and fluorescence spectroscopy and the effect of environment on the photochemical properties of peridinin in solution and in the peridinin-chlorophyll-protein from amphidinium carterae. J Phys Chem A 107:8052–8066. doi:10.1021/jp022648z CrossRefGoogle Scholar
  39. Šlouf V, Chábera P, Olsen JD et al (2012) Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties. Proc Natl Acad Sci U S A 109:8570–8575. doi:10.1073/pnas.1201413109 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Staleva H, Komenda J, Shukla MK et al (2015) Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins. Nat Chem Biol 11:287–291. doi:10.1038/nchembio.1755 CrossRefPubMedGoogle Scholar
  41. Sutter M, Wilson A, Leverenz RL et al (2013) Crystal structure of the FRP and identification of the active site for modulation of OCP-mediated photoprotection in cyanobacteria. Proc Natl Acad Sci U S A 110:10022–10027. doi:10.1073/pnas.1303673110 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Tian L, van Stokkum IHM, Koehorst RBM et al (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133:18304–18311. doi:10.1021/ja206414m CrossRefPubMedGoogle Scholar
  43. Wagner NL, Greco JA, Enriquez MM et al (2013) The nature of the intramolecular charge transfer state in peridinin. Biophys J 104:1314–1325. doi:10.1016/j.bpj.2013.01.045 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Wilson A, Ajlani G, Verbavatz J et al (2006) A soluble carotenoid protein involved in phycobilisome-related energy dissipation in cyanobacteria. Plant Cell 18:992–1007. doi:10.1105/tpc.105.040121.1981 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Wilson A, Punginelli C, Gall A et al (2008) A photoactive carotenoid protein acting as light intensity sensor. Proc Natl Acad Sci U S A 105:12075–12080. doi:10.1073/pnas.0804636105 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wilson A, Kinney JN, Zwart PH et al (2010) Structural determinants underlying photoprotection in the photoactive orange carotenoid protein of cyanobacteria. J Biol Chem 285:18364–18375. doi:10.1074/jbc.M110.115709 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wilson A, Punginelli C, Couturier M et al (2011) Essential role of two tyrosines and two tryptophans on the photoprotection activity of the orange carotenoid protein. Biochim Biophys Acta Bioenerg 1807:293–301. doi:10.1016/j.bbabio.2010.12.009 CrossRefGoogle Scholar
  48. Yeremenko N, Kouřil R, Ihalainen JA et al (2004) Supramolecular organization and dual function of the IsiA chlorophyll-binding protein in cyanobacteria. Biochemistry 43:10308–10313. doi:10.1021/bi048772l CrossRefPubMedGoogle Scholar
  49. Young AJ, Phillip DM, Hashimoto H (2002) Ring-to-chain conformation may be a determining factor in the ability of xanthophylls to bind to the bulk light-harvesting complex of plants. J Mol Struct 642:137–145. doi:10.1016/S0022-2860(02)00444-1 CrossRefGoogle Scholar
  50. Zigmantas D, Hiller RG, Sundström V, Polívka T (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 99:16760–16765. doi:10.1073/pnas.262537599 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Zigmantas D, Hiller RG, Sharples FP et al (2004) Effect of a conjugated carbonyl group on the photophysical properties of carotenoids. Phys Chem Chem Phys 6:3009–3016. doi:10.1039/b315786e CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institute of Physics and Biophysics, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Institute for Integrative Biology of the Cell (I2BC), CEA, CNRSUniversité Paris-Sud, Université Paris-SaclayGif-sur-YvetteFrance
  3. 3.Institut de Biologie et Technologies de Saclay (iBiTec-S)Commissariat à l’Energie Atomique (CEA)Gif-sur-YvetteFrance
  4. 4.Institute of Plant Molecular Biology, Biological CentreCzech Academy of SciencesČeské BudějoviceCzech Republic

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