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Quenching of chlorophyll triplet states by carotenoids in algal light-harvesting complexes related to fucoxanthin-chlorophyll protein

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Abstract

We have used time-resolved absorption and fluorescence spectroscopy with nanosecond resolution to study triplet energy transfer from chlorophylls to carotenoids in a protective process that prevents the formation of reactive singlet oxygen. The light-harvesting complexes studied were isolated from Chromera velia, belonging to a group Alveolata, and Xanthonema debile and Nannochloropsis oceanica, both from Stramenopiles. All three light-harvesting complexes are related to fucoxanthin-chlorophyll protein, but contain only chlorophyll a and no chlorophyll c. In addition, they differ in the carotenoid content. This composition of the complexes allowed us to study the quenching of chlorophyll a triplet states by different carotenoids in a comparable environment. The triplet states of chlorophylls bound to the light-harvesting complexes were quenched by carotenoids with an efficiency close to 100%. Carotenoid triplet states were observed to rise with a ~5 ns lifetime and were spectrally and kinetically homogeneous. The triplet states were formed predominantly on the red-most chlorophylls and were quenched by carotenoids which were further identified or at least spectrally characterized.

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References

  • 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 93:2118–2128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angerhofer A, Bornhauser F, Gall A, Cogdell RJ (1995) Optical and optically detected magnetic-resonance investigation on purple photosynthetic bacterial antenna complexes. Chem Phys 194:259–274

    Article  CAS  Google Scholar 

  • Arellano JB, Melo TB, Borrego CM, Garcia-Gil J, Naqvi KR (2000) Nanosecond laser photolysis studies of chlorosomes and artificial aggregates containing bacteriochlorophyll e: evidence for the proximity of carotenoids and bacteriochlorophyll a in chlorosomes from Chlorobium phaeobacteroides strain CL1401. Photochem Photobiol 72:669–675

    Article  CAS  PubMed  Google Scholar 

  • Basso S, Simionato D, Gerotto C, Segalla A, Giacometti GM, Morosinotto T (2014) Characterization of the photosynthetic apparatus of the Eustigmatophycean Nannochloropsis gaditana: evidence of convergent evolution in the supramolecular organization of photosystem I. BBA-Bioenergetics 1837:306–314

    Article  CAS  PubMed  Google Scholar 

  • Bautista JA, Hiller RG, Sharples FP, Gosztola D, Wasielewski M, Frank HA (1999) Singlet and triplet energy transfer in the peridinin-chlorophyll a protein from Amphidinium carterae. J Phys Chem A 103:2267–2273

    Article  CAS  Google Scholar 

  • Bina D, Gardian Z, Herbstova M, Kotabova E, Konik P, Litvn R, Prasil O, Tichy J, Vacha F (2014) Novel type of red-shifted chlorophyll a antenna complex from Chromera velia: II. Biochemistry and spectroscopy. BBA-Bioenergetics 1837:802–810

    Article  CAS  PubMed  Google Scholar 

  • Blankenship RE (2002) Molecular mechanisms of photosynthesis. Blackwell Science, Oxford

    Book  Google Scholar 

  • Bonetti C, Alexandre MTA, Hiller RG, Kennis JTM, van 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 357:63–69

    Article  CAS  Google Scholar 

  • Buchel C, Naqvi KR, Melo TB (1998) Pigment-pigment interactions in thylakoids and LHCII of chlorophyll a/c containing alga Pleurochloris meiringensis: analysis of fluorescence-excitation and triplet-minus-singlet spectra. Spectrochim Acta A 54:719–726

    Article  Google Scholar 

  • Carbonera D, Giacometti G, Segre U (1996) Carotenoid interactions in peridinin chlorophyll a proteins from dinoflagellates—evidence for optical excitons and triplet migration. J Chem Soc-Faraday Trans 92:989–993

    Article  CAS  Google Scholar 

  • Carbonera D, Agostini A, Di Valentin M, Gerotto C, Basso S, Giacometti GM, Morosinotto T (2014) Photoprotective sites in the violaxanthin-chlorophyll a binding protein (VCP) from Nannochloropsis gaditana. BBA-Bioenergetics 1837:1235–1246

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Mozzo M, Morosinotto T, Romeo A, Hienerwadel R, Bassi R (2007) Singlet and triplet state transitions of carotenoids in the antenna complexes of higher-plant photosystem I. BioChemistry 46:3846–3855

    Article  CAS  PubMed  Google Scholar 

  • 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. BBA-Bioenergetics 1797:1759–1767

    Article  PubMed  Google Scholar 

  • Di Valentin M, Buchel C, Giacometti GM, Carbonera D (2012) Chlorophyll triplet quenching by fucoxanthin in the fucoxanthin-chlorophyll protein from the diatom Cyclotella meneghiniana. Biochem Biophys Res Commun 427:637–641

    Article  PubMed  Google Scholar 

  • Di Valentin M, Meneghin E, Orian L, Polimeno A, Buchel C, Salvadori E, Kay CWM, Carbonera D (2013) Triplet-triplet energy transfer in fucoxanthin-chlorophyll protein from diatom Cyclotella meneghiniana: insights into the structure of the complex. BBA-Bioenergetics 1827:1226–1234

    Article  PubMed  Google Scholar 

  • Di Valentin M, Dal Farra MG, Galazzo L, Albertini M, Schulte T, Hofmann E, Carbonera D (2016) Distance measurements in peridinin-chlorophyll a-protein by light-induced PELDOR spectroscopy. Analysis of triplet state localization. BBA-Bioenergetics 1857:1909–1916

    Article  PubMed  Google Scholar 

  • Di Valentin M, Ceola S, Agostini G, Giacometti GM, Angerhofer A, Crescenzi O, Barone V, Carbonera D (2008) 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. BBA-Bioenergetics 1777:295–307

    Article  CAS  PubMed  Google Scholar 

  • Di Valentin M, Biasibetti F, Ceola S, Carbonera D (2009) Identification of the sites of chlorophyll triplet quenching in relation to the structure of LHC-II from higher plants. Evidence from EPR spectroscopy. J Phys Chem B 113:13071–13078

    Article  CAS  PubMed  Google Scholar 

  • Dittami SM, Michel G, Collén J, Boyen C, Tonon T (2010) Chlorophyll-binding proteins revisited–a multigenic family of light-harvesting and stress proteins from a brown algal perspective. BMC Evol Biol 10:365–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durchan M, Tichy J, Litvin R, Slouf V, Gardian Z, Hribek P, Vacha F, Polivka T (2012) Role of carotenoids in light-harvesting processes in an antenna protein from the chromophyte Xanthonema debile. J Phys Chem B 116:8880–8889

    Article  CAS  PubMed  Google Scholar 

  • Durchan M, Kesan G, Slouf V, Fuciman M, Staleva H, Tichy J, Litvin R, Bina D, Vacha F, Polivka T (2014) Highly efficient energy transfer from a carbonyl carotenoid to chlorophyll a in the main light harvesting complex of Chromera velia. BBA-Bioenergetics 1837:1748–1755

    Article  CAS  PubMed  Google Scholar 

  • Feng J, Wang Q, Wu YS, Ai XC, Zhang XJ, Huang YG, Zhang XK, Zhang JP (2004) Triplet excitation transfer between carotenoids in the LH2 complex from photosynthetic bacterium Rhodopseudomonas palustris. Photosynth Res 82:83–94

    Article  CAS  PubMed  Google Scholar 

  • Gall A, Berera R, Alexandre MTA, Pascal AA, Bordes L, Mendes-Pinto MM, Andrianambinintsoa S, Stoitchkova KV, Marin A, Valkunas L, Horton P, Kennis JTM, van Grondelle R, Ruban A, Robert B (2011) Molecular adaptation of photoprotection: Triplet states in light-harvesting proteins. Biophys J 101:934–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardian Z, Tichy J, Vacha F (2011) Structure of PSI, PSII and antennae complexes from yellow-green alga Xanthonema debile. Photosynth Res 108:25–32

    Article  CAS  PubMed  Google Scholar 

  • Gelzinis A, Butkus V, Songaila E, Augulis R, Gall A, Buchel C, Robert B, Abramavicius D, Zigmantas D, Valkunas L (2015) Mapping energy transfer channels in fucoxanthin-chlorophyll protein complex. BBA-Bioenergetics 1847:241–247

    Article  CAS  PubMed  Google Scholar 

  • Hendler RW, Shrager RI (1994) Deconvolutions based on singular value decomposition and the pseudoinverse: a guide for beginners. J Biochem Biophys Methods 28:1–33

    Article  CAS  PubMed  Google Scholar 

  • Hoffman GE, Sanchez Puerta MV, Delwiche CF (2011) Evolution of light-harvesting complex proteins from Chl c-containing algae. BMC Evol Biol 11:101–101

    Article  PubMed  PubMed Central  Google Scholar 

  • Javorfi T, Garab G, Naqvi KR (1999) Reinvestigation of the triplet-minus-singlet spectrum of chloroplasts. Spectrochim Acta A 56:211–214

    Article  Google Scholar 

  • Jhutti CS, Javorfi T, Merzlyak MN, Naqvi KR (1998) Triplet-triplet absorption spectra and extinction coefficients of lutein, neoxanthin and violaxanthin. In: Garab G (ed) Photosynthesis: mechanisms and effects, pp 491–494. Springer, Dordrecht

    Chapter  Google Scholar 

  • Jones E, Oliphant T, Peterson P (2001) SciPy: open source scientific tools for Python

  • Kearns DR (1971) Physical and chemical properties of singlet molecular oxygen. Chem Rev 71:395-427-

    Article  Google Scholar 

  • Kesan G, Durchan M, Tichy J, Minofar B, Kuznetsoya V, Fuciman M, Slouf V, Parlak C, Polivka T (2015) Different response of carbonyl carotenoids to solvent proticity helps to estimate structure of the unknown carotenoid from Chromera velia. J Phys Chem B 119:12653–12663

    Article  CAS  PubMed  Google Scholar 

  • Kesan G, Litvin R, Bina D, Durchan M, Slouf V, Polivka T (2016) Efficient light-harvesting using non-carbonyl carotenoids: energy transfer dynamics in the VCP complex from Nannochloropsis oceanica. BBA-Bioenergetics 1857:370–379

    Article  CAS  PubMed  Google Scholar 

  • Kleima FJ, Wendling M, Hofmann E, Peterman EJG, van Grondelle R, van Amerongen H (2000) Peridinin chlorophyll a protein: relating structure and steady-state spectroscopy. BioChemistry 39:5184–5195

    Article  CAS  PubMed  Google Scholar 

  • Koziol AG, Borza T, Ishida KI, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kvicalova Z, Alster J, Hofmann E, Khoroshyy P, Litvin R, Bina D, Polivka T, Psencik J (2016) Triplet-triplet energy transfer from chlorophylls to carotenoids in two antenna complexes from dinoflagellate Amphidinium carterae. BBA-Bioenergetics 1857:341–349

    Article  CAS  PubMed  Google Scholar 

  • Lakowicz JR (2006) Principles of fluorescence spectroscopy. Springer, New York

    Book  Google Scholar 

  • Larkum AW (2003) Light-harvesting systems in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae, pp 277–304. Springer, Dordrecht

    Chapter  Google Scholar 

  • Litvin R, Bina D, Herbstova M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130:137–150

    Article  CAS  PubMed  Google Scholar 

  • Llansola-Portoles MJ, Uragami C, Pascal AA, Bina D, Litvin R, Robert B (2016) Pigment structure in the FCP-like light-harvesting complex from Chromera velia. BBA-Bioenergetics 1857:1759–1765

    Article  CAS  PubMed  Google Scholar 

  • Melo TB, Frigaard NU, Matsuura K, Naqvi KR (2000) Electronic energy transfer involving carotenoid pigments in chlorosomes of two green bacteria: Chlorobium tepidum and Chloroflexus aurantiacus. Spectrochim Acta A 56:2001–2010

    Article  Google Scholar 

  • Miloslavina Y, Grouneva I, Lambrev PH, Lepetit B, Goss R, Wilhelm C, Holzwarth AR (2009) Ultrafast fluorescence study on the location and mechanism of non-photochemical quenching in diatoms. Biochim Biophys Acta 1787:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Moore RB, Obornik M, Janouskovec J, Chrudimsky T, Vancova M, Green DH, Wright SW, Davies NW, Bolch CJS, Heimann K, Slapeta J, Hoegh-Guldberg O, Logsdon JM, Carter DA (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–963

    Article  CAS  PubMed  Google Scholar 

  • Mozzo M, Dall’Osto L, Hienerwadel R, Bassi R, Croce R (2008) Photoprotection in the antenna complexes of photosystem II—role of individual xanthophylls in chlorophyll triplet quenching. J Biol Chem 283:6184–6192

    Article  CAS  PubMed  Google Scholar 

  • Naqvi KR, Melo TB, Raju BB, Javorfi T, Simidjiev I, Garab G (1997) Quenching of chlorophyll a singlets and triplets by carotenoids in light-harvesting complex of photosystem II: comparison of aggregates with trimers. Spectrochim Acta A 53:2659–2667

    Article  Google Scholar 

  • Nechushtai R, Thornber JP, Patterson LK, Fessenden RW, Levanon H (1988) Photosensitization of triplet carotenoid in photosynthetic light-harvesting complex of photosystem-II. J Phys Chem 92:1165–1168

    Article  CAS  Google Scholar 

  • Niedzwiedzki DM, Blankenship RE (2010) Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls. Photosynth Res 106:227–238

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Jiang J, Lo CS, Blankenship RE (2013) Low-temperature spectroscopic properties of the peridinin-chlorophyll a-protein (PCP) complex from the coral symbiotic dinoflagellate Symbiodinium. J Phys Chem B 117:11091–11099

    Article  CAS  PubMed  Google Scholar 

  • Niedzwiedzki DM, Jiang J, Lo CS, Blankenship RE (2014) Spectroscopic properties of the chlorophyll a-chlorophyll c2-peridinin-protein-complex (acpPC) from the coral symbiotic dinoflagellate Symbiodinium. Photosynth Res 120:125–139

    Article  CAS  PubMed  Google Scholar 

  • Oliphant TE (2006) A guide to NumPy. Trelgol Publishing, Spanish Fork

    Google Scholar 

  • Owens TG, Gallagher JC, Alberte RS (1987) Photosynthetic light-harvesting function of violaxanthin in Nannochloropsis spp. (Eustigmatophyceae)1. J Phycol 23:79–85

    Article  CAS  Google Scholar 

  • Pascal AA, Liu ZF, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang WR, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137

    Article  CAS  PubMed  Google Scholar 

  • Pessarakli M (2016) Handbook of photosynthesis, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Peterman EJG, Dukker FM, van Grondelle R, van Amerongen H (1995) Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys J 69:2670–2678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Premvardhan L, Robert B, Beer A, Buchel C (2010) Pigment organization in fucoxanthin chlorophyll a/c2 proteins (FCP) based on resonance Raman spectroscopy and sequence analysis. BBA-Bioenergetics 1797:1647–1656

    Article  CAS  PubMed  Google Scholar 

  • Psencik J, Searle GFW, Hala J, Schaafsma TJ (1994) Fluorescence-detected magnetic-resonance (FDMR) of green sulfur photosynthetic bacteria Chlorobium sp. Photosynth Res 40:1–10

    Article  CAS  PubMed  Google Scholar 

  • Schodel R, Irrgang KD, Voigt J, Renger G (1998) Rate of carotenoid triplet formation in solubilized light-harvesting complex II (LHCII) from spinach. Biophys J 75:3143–3153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrager RI, Hendler W (1998) Some pitfalls in curve-fitting and how to avoid them: a case in point. J Biochem Biophys Methods 36:157–173

    Article  CAS  PubMed  Google Scholar 

  • Straume M, Johnson ML (1992) Monte Carlo method for determining complete confidence probability distributions of estimated model parameters. Methods Enzymol 210:117–129

    Article  CAS  PubMed  Google Scholar 

  • Tichy J, Gardian Z, Bina D, Konik P, Litvin R, Herbstova M, Pain A, Vacha F (2013) Light harvesting complexes of Chromera velia, photosynthetic relative of apicomplexan parasites. BBA-Bioenergetics 1827:723–729

    Article  CAS  PubMed  Google Scholar 

  • Truscott TG, Land EJ, Sykes A (1973) In-vitro photochemistry of biological molecules. 3. Absorption-spectra, lifetimes and rates of oxygen quenching of triplet-states of beta-carotene, retinal and related polyenes. Photochem Photobiol 17:43–51

    Article  CAS  PubMed  Google Scholar 

  • van Stokkum IHM, Larsen DS, van Grondelle R (2004) Global and target analysis of time-resolved spectra. BBA-Bioenergetics 1657:82–104

    Article  PubMed  Google Scholar 

  • van der Vos R, Carbonera D, Hoff AJ (1991) Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHCII of spinach. Appl Magn Reson 2:179–202

    Article  Google Scholar 

  • Vieler A, Wu GX, Tsai CH, Bullard B, Cornish AJ, Harvey C, Reca IB, Thornburg C, Achawanantakun R, Buehl CJ, Campbell MS, Cavalier D, Childs KL, Clark TJ, Deshpande R, Erickson E, Ferguson AA, Handee W, Kong Q, Li X, Liu B, Lundback S, Peng C, Roston RL, Sanjaya, Simpson JP, TerBush A, Warakanont J, Zauner S, Farre EM, Hegg EL, Jiang N, Kuo MH, Lu Y, Niyogi KK, Ohlrogge J, Osteryoung KW, Shachar-Hill Y, Sears BB, Sun Y, Takahashi H, Yandell M, Shiu SH, Benning C (2012) Genome, functional gene annotation, and nuclear transformation of the Heterokont Oleaginous alga Nannochloropsis oceanica CCMP1779. PLoS Genet 8:e1003064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by Czech Science Foundation projects P501/12/G055 and 14-01377P and by institutional funding RVO:60077344. Discussions with Prof. Herbert van Amerongen from the Wageningen University are greatly appreciated. We are indebted to Dr. Sarah Henry from Glasgow University for careful proofreading of the manuscript.

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  1. Department of Chemical Physics and Optics, Faculty of Mathematics and Physics, Charles University, 121 16, Prague 2, Czech Republic

    Petro Khoroshyy, Jan Alster & Jakub Pšenčík

  2. Biological Centre, Czech Academy of Sciences, 370 05, České Budějovice, Czech Republic

    David Bína, Zdenko Gardian & Radek Litvín

  3. Faculty of Science, University of South Bohemia, 370 05, České Budějovice, Czech Republic

    David Bína, Zdenko Gardian & Radek Litvín

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  1. Petro Khoroshyy
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  2. David Bína
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Correspondence to Jakub Pšenčík.

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Khoroshyy, P., Bína, D., Gardian, Z. et al. Quenching of chlorophyll triplet states by carotenoids in algal light-harvesting complexes related to fucoxanthin-chlorophyll protein. Photosynth Res 135, 213–225 (2018). https://doi.org/10.1007/s11120-017-0416-5

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