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Cation radicals of xanthophylls

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Abstract

Carotenes and xanthophylls are well known to act as electron donors in redox processes. This ability is thought to be associated with the inhibition of oxidative reactions in reaction centers and light-harvesting pigment–protein complexes of photosystem II (PSII). In this work, cation radicals of neoxanthin, violaxanthin, lutein, zeaxanthin, β-cryptoxanthin, β-carotene, and lycopene were generated in solution using ferric chloride as an oxidant and then studied by absorption spectroscopy. The investigation provides a view toward understanding the molecular features that determine the spectral properties of cation radicals of carotenoids. The absorption spectral data reveal a shift to longer wavelength with increasing π-chain length. However, zeaxanthin and β-cryptoxanthin exhibit cation radical spectra blue-shifted compared to that of β-carotene, despite all of these molecules having 11 conjugated carbon–carbon double bonds. CIS molecular orbital theory quantum computations interpret this effect as due to the hydroxyl groups in the terminal rings selectively stabilizing the highest occupied molecular orbitals of preferentially populated s-trans-isomers. The data are expected to be useful in the analysis of spectral results from PSII pigment–protein complexes seeking to understand the role of carotene and xanthophyll cation radicals in regulating excited state energy flow, in protecting PSII reaction centers against photoinhibition, and in dissipating excess light energy absorbed by photosynthetic organisms but not used for photosynthesis.

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Abbreviations

CIS:

Configuration interaction singles

DDQ:

2,3-dicyano-5,6-dichloro-parabenzoquinone

HOMO:

Highest occupied molecular orbital

HPLC:

High-performance liquid chromatography

LUMO:

Lowest unoccupied molecular orbital

NIR:

Near-infrared

PSII:

Photosystem II

TCNQ:

7′,8,8′-tetracyanoquinodimethide

THF:

Tetrahydrofuran

References

  • Adams RN (1969) Anodic oxidation pathways of aromatic hydrocarbons and amines. Acc Chem Res 2:175–180

    Article  CAS  Google Scholar 

  • Amarie S, Standfuss J, Barros T, Külbrandt W, Dreuw A, Wachtveitl J (2007) Carotenoid radical cations as a probe for the molecular mechanism of nonphotochemical quenching in oxygenic photosynthesis. J Phys Chem B 111:3481–3487

    Article  CAS  PubMed  Google Scholar 

  • Andrews JR, Hudson BS (1978) Polyene spectroscopy: vibronic evidence for a forbidden transition in deca-2,4,6,8-tetraene. Chem Phys Lett 57:600–604

    Article  CAS  Google Scholar 

  • Bassi R, Caffarri S (2000) Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynth Res 64:243–256

    Article  CAS  PubMed  Google Scholar 

  • Bautista JA, Tracewell CA, Schlodder E, Cunningham FX, Brudvig GW, Diner BA (2005) Construction and characterization of genetically modified Synechocystis sp. PCC 6803 photosystem II core complexes containing carotenoids with shorter π-conjugation than β-carotene. J Biol Chem 280:38839–38850

    Article  CAS  PubMed  Google Scholar 

  • Bensasson RV, Land EJ, Truscott TG (1983) Flash photolysis and pulse radiolysis. Oxford University Press, New York

    Google Scholar 

  • Böhm F, Tinkler JH, Truscott G (1995) Carotenoid protect against cell membrane damage by the nitrogen dioxide radical. Nat Med 1:98–99

    Article  PubMed  Google Scholar 

  • Burton GW, Ingold KU (1984) β-carotene: an unusual type of lipid antioxidant. Science 224:569–573

    Article  CAS  PubMed  Google Scholar 

  • Christensen RL (1999) The electronic states of carotenoids. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids, vol 8. Kluwer Academic Publishers, Dordrecht, pp 137–159

    Chapter  Google Scholar 

  • Christensen RL, Kohler BE (1973) Low resolution optical spectroscopy of retinyl polyenes: low-lying electronic levels and spectral broadness. Photochem Photobiol 18:293–301

    CAS  Google Scholar 

  • Christensen RL, Goyette M, Gallagher L, Duncan J, DeCoster B, Lugtenburg J, Jansen FJ, van der Hoef I (1999) S1 and S2 States of apo- and diapocarotenes. J Phys Chem A 103:2399–2407

    Article  CAS  Google Scholar 

  • Christensen RL, Faksh A, Meyers JA, Samuel IDW, Wood P, Schrock RR, Hultzsch KC (2004) Optical spectroscopy of long polyenes. J Phys Chem A 108:8229–8236

    Article  CAS  Google Scholar 

  • Cogdell RJ, Gardiner AT, Roszak AW, Law CJ, Southall J, Isaacs NW (2004) Rings, ellipses and horseshoes: how purple bacteria harvest solar energy. Photosynth Res 81:207–214

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Croce R, Muller MG, Caffari S, Bassi R, Holzwarth AR (2003) Energy transfer pathways in the minor antenna complex CP29 of photosystem II: a femtosecond study of carotenoid to chlorophyll transfer in mutant and WT complexes. Biophys J 84:2517–2532

    CAS  PubMed  Google Scholar 

  • Das SK, Frank HA (2002) Pigment compositions, spectral properties, and energy transfer efficiencies between the xanthophylls and chlorophylls in the major and minor pigment-protein complexes of photosystem II. Biochemistry 41:13087–13095

    Article  CAS  PubMed  Google Scholar 

  • Dawe EA, Land EJ (1975) Radical ions derived from photosynthetic polyenes. J Chem Soc Faraday Trans 1 71:2161–2169

    Google Scholar 

  • Deng Y, Gao GQ, He ZF, Kispert LD (2000) Effects of polyene chain length and acceptor substituents on the stability of carotenoid radical cations. J Phys Chem B 104:5651–5656

    Article  CAS  Google Scholar 

  • Desamero RZB, Chynwat V, van der Hoef I, Jansen FJ, Lugtenburg J, Gosztola D, Wasielewski MR, Cua A, Bocian DF, Frank HA (1998) The mechanism of energy transfer from carotenoids to bacteriochlorophyll: light-harvesting by carotenoids having different extents of π-electron conjugation incorporated into the B850 antenna complex from the carotenoidless bacterium Rhodobacter sphaeroides R-26.1. J Phys Chem 102:8151–8162

    CAS  Google Scholar 

  • Ding R, Grant JL, Metzger RM, Kispert LD (1988) Carotenoid cation radicals produced by the interaction of carotenoids with iodine. J Phys Chem 92:4600–4606

    Article  CAS  Google Scholar 

  • Edge R, Land EJ, McGarvey D, Mulroy L, Truscott TG (1998) Relative one-electron reduction potentials of carotenoid radical cations and the interactions of carotenoids with the vitamin E radical cation. J Am Chem Soc 120:4087–4090

    Article  CAS  Google Scholar 

  • Everett SA, Kundu SC, Maddix S, Willson RL (1995) Mechanisms of free radical scavenging by the nutritional antioxidant β-carotene. Biochem Soc Trans 23:230S

    CAS  PubMed  Google Scholar 

  • Everett SA, Dennis MF, Patel KB, Maddix S, Kundu SC, Willson RL (1996) Scavenging of nitrogen dioxide, thiyl, and sulfonyl free radicals by the nutritional antioxidant β-carotene. J Biol Chem 271:3988–3994

    Article  CAS  PubMed  Google Scholar 

  • Frank HA, Brudvig GW (2004) Redox functions of carotenoids in photosynthesis. Biochemistry 43:8607–8615

    Article  CAS  PubMed  Google Scholar 

  • Frank HA, Christensen RL (1995) Singlet energy transfer from carotenoids to bacteriochlorophylls. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria, vol 2. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 373–384

    Chapter  Google Scholar 

  • Gao Y, Kispert LD (2003) Reaction of carotenoids and ferric chloride: equilibiria, isomerization, and products. J Chem Phys B 107:5333–5338

    Article  CAS  Google Scholar 

  • Gao G, Deng Y, Kispert LD (1997) Photoactivated ferric chloride oxidation of carotenoids by near-UV to visible Light. J Phys Chem B 101:7844–7849

    Article  CAS  Google Scholar 

  • Gradinaru CC, van Stokkum IHM, Pascal AA, van Grondelle R, van Amerongen H (2000) Identifying 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

    Article  CAS  Google Scholar 

  • Grant JL, Kramer VJ, Ding R, Kispert LD (1988) Carotenoid cation radicals: electrochemical, optical and EPR study. J Am Chem Soc 110:2151–2157

    Article  CAS  Google Scholar 

  • Gust D, Moore TA (1991) Mimicking photosynthetic electron and energy transfer. In: Volman D, Hammond G, Neckers D (eds) Advances in photochemistry, vol 16. John Wiley & Sons, New York, pp 1–63

    Chapter  Google Scholar 

  • Gust D, Moore TA, Moore AL (1993) Molecular mimicry of photosynthetic energy and electron transfer. Acc Chem Res 26:198–205

    Article  CAS  Google Scholar 

  • Hapiot P, Kispert LD, Konovalov VV, Saveant J-M (2001) Single two-electron transfers vs successive one-electron transfers in polyconjugated systems illustrated by the electrochemical oxidation and reduction of carotenoids. J Am Chem Soc 123:6669–6677

    Article  CAS  PubMed  Google Scholar 

  • He Z, Kispert LD (1999a) Effect of electrolytes and temperature on dications and radical cations of carotenoids: electrochemical, optical absorption, and high-performance liquid chromatography studies. J Phys Chem B 103:10524–10531

    Article  CAS  Google Scholar 

  • He Z, Kispert LD (1999b) Electrochemical and optical study of carotenoids in Triton X100 micelles: electron transfer and a large blue shift. J Phys Chem B 103:9038–9043

    Article  CAS  Google Scholar 

  • Hermant RM, Liddell PA, Lin S, Alden RG, Kang HK, Moore AL, Moore TA, Gust D (1993) Mimicking carotenoid quenching of chlorophyll fluorescence. J Am Chem Soc 115:2080–2081

    Article  CAS  Google Scholar 

  • Hill TJ, Land EJ, McGarvey DJ, Schalch W, Tinkler JH, Truscott TG (1995) Interactions between carotenoids and the CCl3O ·2 radical. J Am Chem Soc 117:8322–8326

    Article  CAS  Google Scholar 

  • Holt NE, Zigmantas D, Valkunas L, Li XP, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436

    Article  CAS  PubMed  Google Scholar 

  • Ioffe NT, Engovatov AA, Mairanovskii VG (1976) Electron donor-acceptor properties of carotenoids. II. Spectral study of the interaction of carotenes with electron acceptors. Zh Obshch Khim 46:1638–1644

    CAS  Google Scholar 

  • Isler O (1971) Carotenoids. Birkhauser, Basel

    Google Scholar 

  • Jeevarajan AS, Kispert LD, Wu XG (1994) Spectroelectrochemistry of carotenoids in solution. Chem Phys Lett 219:427–432

    Article  CAS  Google Scholar 

  • Jeevarajan JA, Wei CC, Jeevarajan AS, Kispert LD (1996) Optical absorption spectra of dications of carotenoids. J Phys Chem 100:5637–5641

    Article  CAS  Google Scholar 

  • Josue JS, Frank HA (2002) Direct determination of the S1 excited-state energies of xanthophylls by low-temperature fluorescence spectroscopy. J Phys Chem A 106:4815–4824

    Article  CAS  Google Scholar 

  • Jørgensen K, Skibsted LH (1993) Carotenoid scavenging of radicals. Effect of carotenoid structure and oxygen partial pressure on antioxidative activity. Z Lebensm-Unters Forsch 196:423–429

    Article  PubMed  Google Scholar 

  • Khaled M, Hadjipetrou A, Kispert L (1990) Electrochemical and electron paramagnetic resonance studies of carotenoid cation radicals and dications: effect of deuteration. J Phys Chem 94:5164–5169

    Article  CAS  Google Scholar 

  • Khaled M, Hadjipetrou A, Kispert L, Allendoerfer RD (1991) Simultaenous electrochemical and electron paramagnetic resonance studies of carotenoid cation radicals and dications. J Phys Chem 95:2438–2442

    Article  CAS  Google Scholar 

  • Kohler BE (1990) A simple model for linear polyene electronic structure. J Chem Phys 93:5838–5942

    Article  CAS  Google Scholar 

  • Kohler BE (1991) Electronic properties of linear polyenes. In: Bredas JL, Silbey R (eds) Conjugated polymers: the novel science and technology of conducting and nonlinear optically active materials. Kluwer Press, Dordrecht, The Netherlands

    Google Scholar 

  • Kohler BE (1995) Electronic structure of carotenoids. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids, vol 1B: spectroscopy. Birkhäuser Verlag AG, Basel, pp 3–12

    Google Scholar 

  • Kramer H, Deinum G, Gardiner AT, Cogdell RJ, Francke C, Aartsma TJ, Amesz J (1995) Energy-transfer in the photosynthetic antenna system of the purple nonsulfur bacterium Rhodopseudomonas–Cryptolactis. Biochim Biophys Acta Bioenerg 1231:33–40

    Article  Google Scholar 

  • Krawczyk S (1998) Absorption and electroabsorption spectra of carotenoid cation radical and dication. Chem Phys Lett 230:297–304

    CAS  Google Scholar 

  • 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 polarized transient absorption and target analysis. Biophys J 80:2843–2855

    Article  CAS  PubMed  Google Scholar 

  • Lafferty J, Roach AC, Sinclair RS, Truscott G, Land EJ (1977) Absorption spectra of radical ions of polyenes of biological interest. J Chem Soc Faraday Trans 1 73:416–429

    Article  CAS  Google Scholar 

  • Land EJ, Lexa D, Bensasson RV, Gust D, Moore TA, Moore AL, Liddell PA, Nemeth GA (1987) Pulse radiolytic and electrochemical investigations of intramolecular electron transfer in carotenoporphyrins and carotenoporphyrin-quinone triads. J Phys Chem 91:4831–4835

    Article  CAS  Google Scholar 

  • Liu D, Kispert LD (1999) Electrochemical aspects of carotenoids. Recent Res Dev Electrochem 2:139–157

    CAS  Google Scholar 

  • Mortensen A, Skibsted LH (1996) Kinetics of parallel electron transfer from β-carotene to phenoxyl radical and adduct formation between phenoxyl radical and β-carotene. Free Rad Res 25:515–523

    Article  CAS  Google Scholar 

  • Mortensen A, Skibsted LH (1997) Importance of carotenoid structure in radical-scavenging reactions. J Agric Food Chem 45:2970–2977

    Article  CAS  Google Scholar 

  • Niedzwiedzki DM, Sullivan JO, Polivka T, Birge RR, Frank HA (2006) Femtosecond time-resolved transient absorption spectroscopy of xanthophylls. J Phys Chem B 110:22872–22885

    Article  CAS  PubMed  Google Scholar 

  • Ohmine I, Karplus M, Schulten K (1978) Renormalized configuration interaction method for electron correlation in the excited states of polyenes. J Chem Phys 68:2298–2318

    Article  CAS  Google Scholar 

  • Palozza P, Krinsky NI (1994) Antioxidant properties of carotenoids. In: Livrea MA, Vidali G (eds) Retinoids: from basic science to clinical applications. Birkhäuser Verlag, Basel, Switzerland

    Google Scholar 

  • Papagiannakis E, Das SK, Gall A, Stokkum IHM, Robert B, van Grondelle R, Frank HA, Kennis JTM (2003) Light harvesting by carotenoids incorporated into the B850 light-harvesting complex from Rhodobacter sphaeroides R-26.1: excited-state relaxation, ultrafast triplet formation, and energy transfer to bacteriochlorophyll. J Phys Chem B 107:5642–5649

    Article  CAS  Google Scholar 

  • Polívka T, Zigmantas D, Herek JL, He Z, Pascher T, Pullerits T, Cogdell RJ, Frank HA, Sundström V (2002) The carotenoid S1 state in LH2 complexes from purple bacteria Rhodobacter sphaeroides and Rhodopseudomonas acidophila: S1 energies, dynamics, and carotenoid radical formation. J Phys Chem B 106:11016–11025

    Article  CAS  Google Scholar 

  • Polívka T, Pullerits T, Frank HA, Cogdell RJ, Sundström V (2004) Ultrafast formation of a carotenoid radical in LH2 antenna complexes of purple bacteria. J Phys Chem B 108:15398–15407

    Article  CAS  Google Scholar 

  • Rivas J, Telfer A, Barber J (1993) Two coupled β-carotene molecules protect P680 from photodamage in isolated photosystem II reaction centers. Biochem Biophys Acta 1142:155–164

    Article  Google Scholar 

  • Schenck CC, Diner BA, Mathis P, Satoh K (1982) Flash-induced carotenoid radical cation formation in photosystem II. Biochim Biophys Acta 680:216–227

    Article  CAS  Google Scholar 

  • Schulten K, Karplus M (1972) On the origin of a low-lying forbidden transition in polyenes and related molecules. Chem Phys Lett 14:305–309

    Article  CAS  Google Scholar 

  • Schulten K, Ohmine I, Karplus M (1976) Correlation effects in the spectra of polyenes. J Chem Phys 64:4422–4441

    Article  CAS  Google Scholar 

  • Serrano-Andrés L, Lindh R, Roos BO, Merchán M (1993) Theoretical study of the electronic spectrum of all-trans-1,3,5,7-octatetraene. J Phys Chem 97:9360–9368

    Article  Google Scholar 

  • Sorenson TS (1965) The preparation and reactions of a homologous series of aliphatic polyenylic cations. J Am Chem Soc 87:5075–5084

    Article  Google Scholar 

  • Starcke JH, Wormit M, Schirmer J, Dreuw A (2006) How much double excitation character do the lowest excited states of linear polyenes have? Chem Phys Lett 329:39–49

    CAS  Google Scholar 

  • Tavan P, Schulten K (1979) The 21Ag–11Bu energy gap in the polyenes: an extended configuration interaction study. J Chem Phys 70:5407–5413

    Article  CAS  Google Scholar 

  • Tavan P, Schulten K (1986) The low-lying electronic excitations in long polyenes: a PPP-MRD-CI study. J Chem Phys 85:6602–6609

    Article  CAS  Google Scholar 

  • Tracewell CA, Brudvig GW (2003) Two redox-active b-carotene molecules in photosystem II. Biochemistry 42:9127–9136

    Article  CAS  PubMed  Google Scholar 

  • Trissl H-W, Law CJ, Cogdell RJ (1999) Uphill energy transfer in LH2-containing purple bacteria at room temperature. Biochim Biophys Acta 1412:149–172

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • van Grondelle R, Dekker JP, Gillbro T, Sundström V (1994) Energy-transfer and trapping in photosynthesis. Biochim Biophys Acta 1187:1–65

    Article  CAS  Google Scholar 

  • Wang X-F, Kakitani Y, Xiang J, Koyama Y, Rondonuwu FS, Nagae H, Sasaki S-i, Tamiaki H (2005) Generation of carotenoid radical cation in the vicinity of a chlorophyll derivative bound to titanium oxide, upon excitation of the chlorophyll derivative to the Qy state, as identified by time-resolved absorption spectroscopy. Chem Phys Lett 416:229–233

    Article  CAS  Google Scholar 

  • Wei C-C, Gao G, Kispert LD (1997) Selected cis/trans isomers of carotenoids formed by bulk electrolysis and iron(III) chloride oxidation. J Chem Soc Perkin Trans 2:783–786

    Google Scholar 

  • Woodall AA, Britton G, Jackson MJ (1996) Dietary supplementation with carotenoids:effects on α-tocopherol levels and susceptibility of tissues to oxiative stress. Br J Nutr 76:307–317

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work is supported in the laboratory of HAF by the National Science Foundation (MCB-0314380) and the University of Connecticut Research Foundation and in the laboratory of RRB by the National Institutes of Health (GM-34548).

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  1. Department of Chemistry, University of Connecticut, U-3060, 55 North Eagleville Road, Storrs, CT, 06269-3060, USA

    Mary Grace I. Galinato, Dariusz Niedzwiedzki, Cailin Deal, Robert R. Birge & Harry A. Frank

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  1. Mary Grace I. Galinato
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  2. Dariusz Niedzwiedzki
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  3. Cailin Deal
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  4. Robert R. Birge
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Correspondence to Harry A. Frank.

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Galinato, M.G.I., Niedzwiedzki, D., Deal, C. et al. Cation radicals of xanthophylls. Photosynth Res 94, 67–78 (2007). https://doi.org/10.1007/s11120-007-9218-5

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