Intramolecular charge-transfer state of carotenoids siphonaxanthin and siphonein: function of non-conjugated acyl-oxy group

Abstract

We used ultrafast transient absorption spectroscopy to study excited-state dynamics of two keto-carotenoids, siphonaxanthin and siphonein. These two carotenoids differ in the presence of dodecanoyl-oxy group in siphonein, which is attached to the C19 carbon on the same side of the molecule as the conjugated keto group. We show that this dodecanoyl-oxy group, though not in conjugation, is still capable of modifying excited state properties. While spectroscopic properties of siphonein and siphonaxanthin are nearly identical in a non-polar solvent, they become markedly different in polar solvents. In a polar solvent, siphonein, having the dodecanoyl-oxy moiety, exhibits less pronounced vibrational bands in the absorption spectrum and has significantly enhanced characteristic features of an intramolecular charge-transfer (ICT) state in transient absorption spectra compared to siphonaxanthin. The presence of the dodecanoyl-oxy moiety also alters the lifetimes of the S1/ICT state. For siphonaxanthin, the lifetimes are 60, 20, and 14 ps in n-hexane, acetonitrile, and methanol, whereas for siphonein these lifetimes yield 60, 11, and 10 ps. Thus, we show that even a non-conjugated functional group can affect the charge-transfer character of the S1/ICT state. By comparison with fucoxanthin acyl-oxy derivatives, we show that position of the acyl-oxy group in respect to the conjugated keto group is the key feature determining whether the polarity-dependent behavior is enhanced or suppressed.

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References

  1. Adamec F, Greco JA, LaFountain AM, Magdaong NM, Fuciman M, Birge RR, Polivka T, Frank HA (2016) Spectroscopic investigation of a brightly colored psittacofulvin pigment from parrot feathers. Chem Phys Lett 648:195–199

    CAS  Article  Google Scholar 

  2. Akimoto S, Yamazaki I, Murakami A, Takaichi S, Mimuro M (2004) Ultrafast excitation relaxation dynamics and energy transfer in the siphonaxanthin-containing green alga Codium fragile. Chem Phys Lett 390(1–3):45–49

    CAS  Article  Google Scholar 

  3. Akimoto S, Tomo T, Naitoh Y, Otomo A, Murakami A, Mimuro M (2007) Identification of a new excited state responsible for the in vivo unique absorption band of siphonaxanthin in the green alga Codium fragile. J Phys Chem B 111(31):9179–9181

    CAS  Article  Google Scholar 

  4. Akimoto S, Yokono M, Higuchi M, Tomo T, Takaichi S, Murakami A, Mimuro M (2008) Solvent effects on excitation relaxation dynamics of a keto-carotenoid, siphonaxanthin. Photochem Photobiol Sci 7(10):1206–1209

    CAS  Article  Google Scholar 

  5. Bautista JA, Connors RE, Raju BB, Hiller RG, Sharples FP, Gosztola D, Wasielewski MR, Frank HA (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(41):8751–8758

    CAS  Article  Google Scholar 

  6. Chabera P, Fuciman M, Hribek P, Polivka T (2009) Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids. Phys Chem Chem Phys 11(39):8795–8803

    CAS  Article  Google Scholar 

  7. Enriquez MM, Fuciman M, LaFountain AM, Wagner NL, Birge RR, Frank HA (2010) The intramolecular charge transfer state in carbonyl-containing polyenes and carotenoids. J Phys Chem B 114(38):12416–12426

    CAS  Article  Google Scholar 

  8. Enriquez MM, Hananoki S, Hasegawa S, Kajikawa T, Katsumura S, Wagner NL, Birge RR, Frank HA (2012) Effect of molecular symmetry on the spectra and dynamics of the intramolecular charge transfer (ICT) state of peridinin. J Phys Chem B 116(35):10748–10756

    CAS  Article  Google Scholar 

  9. Fiedor L, Pilch M (2018) Side methyl groups control the conformation and contribute to symmetry breaking of isoprenoid chromophores. Angew Chem Int Ed 57(22):6501–6506

    CAS  Article  Google Scholar 

  10. 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(18):4569–4577

    CAS  Article  Google Scholar 

  11. Garrido JL, Brunet C, Rodriguez F (2016) Pigment variations in Emiliania huxleyi (CCMP370) as a response to changes in light intensity or quality. Environ Microbiol 18(12):4412–4425

    CAS  Article  Google Scholar 

  12. Gradinaru CC, Kennis JTM, Papagiannakis E, van Stokkum IHM, Cogdell RJ, Fleming GR, Niederman RA, van Grondelle R (2001) An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna. Proc Natl Acad Sci USA 98(5):2364–2369

    CAS  Article  Google Scholar 

  13. Guillard RR, Ryther JH (1962) Studies of marine planktonic diatoms. 1. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8(2):229–239

    CAS  Article  Google Scholar 

  14. Hashimoto H, Uragami C, Yukihira N, Gardiner AT, Cogdell RJ (2018) Understanding/unravelling carotenoid excited singlet states. J R Soc Interface. https://doi.org/10.1098/rsif.2018.0026

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jeffrey SW, Mantoura RFC, Wright SW (2005) Phytoplankton Pigments in Oceanography: Guidelines to Modern Methods, vol 10. Monographs on Oceanographic Methodology. UNESCO Publishing, Paris

  16. 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(39):12653–12663

    CAS  Article  Google Scholar 

  17. Kopczynski M, Ehlers F, Lenzer T, Oum K (2007) Evidence for an intramolecular charge transfer state in 12‘-apo-beta-caroten-12‘-al and 8‘-apo-beta-caroten-8‘-al: influence of solvent polarity and temperature. J Phys Chem A 111(25):5370–5381

    CAS  Article  Google Scholar 

  18. Kosumi D, Kajikawa T, Okumura S, Sugisaki M, Sakaguchi K, Katsumura S, Hashimoto H (2014a) Elucidation and control of an intramolecular charge transfer property of fucoxanthin by a modification of its polyene chain length. J Phys Chem Lett 5(5):792–797

    CAS  Article  Google Scholar 

  19. Kosumi D, Kajikawa T, Yano K, Okumura S, Sugisaki M, Sakaguchi K, Katsumura S, Hashimoto H (2014b) Roles of allene-group in an intramolecular charge transfer character of a short fucoxanthin homolog as revealed by femtosecond pump-probe spectroscopy. Chem Phys Lett 602:75–79

    CAS  Article  Google Scholar 

  20. Li L, Hu F, Chang YQ, Zhou Y, Wang P, Zhang JP (2015) Triplet excitation dynamics of two keto-carotenoids in n-hexane and in methanol as studied by ns flash photolysis spectroscopy. Chem Phys Lett 633:114–119

    CAS  Article  Google Scholar 

  21. Litvin R, Bina D, Herbstova M, Gardian Z (2016) Architecture of the light-harvesting apparatus of the eustigmatophyte alga Nannochloropsis oceanica. Photosynth Res 130(1–3):137–150

    CAS  Article  Google Scholar 

  22. Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee Scholes GD (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117(2):249–293

    CAS  Article  Google Scholar 

  23. Niedzwiedzki D, Koscielecki JF, Cong H, Sullivan JO, Gibson GN, Birge RR, Frank HA (2007) Ultrafast dynamics and excited state spectra of open-chain carotenoids at room and low temperatures. J Phys Chem B 111(21):5984–5998

    CAS  Article  Google Scholar 

  24. Niedzwiedzki DM, Chatterjee N, Enriquez MM, Kajikawa T, Hasegawa S, Katsumura S, Frank HA (2009) Spectroscopic investigation of peridinin analogues having different pi-electron conjugated chain lengths: exploring the nature of the intramolecular charge transfer state. J Phys Chem B 113(41):13604–13612

    CAS  Article  Google Scholar 

  25. Niedzwiedzki DM, Kajikawa T, Aoki K, Katsumura S, Frank HA (2013) Excited states energies and dynamics of peridinin analogues and the nature of the intramolecular charge transfer state in carbonyl-containing carotenoids. J Phys Chem B 117(23):6874–6887

    CAS  Article  Google Scholar 

  26. Papagiannakis E, van Stokkum IHM, Fey H, Buchel C, van Grondelle R (2005) Spectroscopic characterization of the excitation energy transfer in the fucoxanthin-chlorophyll protein of diatoms. Photosynth Res 86(1–2):241–250

    CAS  Article  Google Scholar 

  27. Polivka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43(8):1125–1134

    CAS  Article  Google Scholar 

  28. Polivka T, Sundstrom V (2004) Ultrafast dynamics of carotenoid excited states—from solution to natural and artificial systems. Chem Rev 104(4):2021–2071

    CAS  Article  Google Scholar 

  29. Polivka T, Sundstrom V (2009) Dark excited states of carotenoids: consensus and controversy. Chem Phys Lett 477(1–3):1–11

    CAS  Article  Google Scholar 

  30. Polivka T, Frank HA, Enriquez MM, Niedzwiedzki DM, Liaaen-Jensen S, Hemming J, Helliwell JR, Helliwell M (2010) X-ray crystal structure and time-resolved spectroscopy of the blue carotenoid violerythrin. J Phys Chem B 114(26):8760–8769

    CAS  Article  Google Scholar 

  31. Raniello R, Lorenti M, Brunet C, Buia MC (2006) Photoacclimation of the invasive alga Caulerpa racemosa var. cylindracea to depth and daylight patterns and a putative new role for siphonaxanthin. Mar Ecol Evol Persp 27(1):20–30

    CAS  Article  Google Scholar 

  32. Redeckas K, Voiciuk V, Zigmantas D, Hiller RG, Vengris M (2017) Unveiling the excited state energy transfer pathways in peridinin-chlorophyll a-protein by ultrafast multi-pulse transient absorption spectroscopy. BBA 1858(4):297–307

    CAS  Google Scholar 

  33. 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(2):169–181

    CAS  Article  Google Scholar 

  34. Staleva-Musto H, Kuznetsova V, West RG, Kesan G, Minofar B, Fuciman M, Bina D, Litvin R, Polivka T (2018) Nonconjugated acyloxy group deactivates the intramolecular charge-transfer state in the carotenoid fucoxanthin. J Phys Chem B 122(11):2922–2930

    CAS  Article  Google Scholar 

  35. Tejeda-Ferrari ME, Brown CL, Coutinho GCCC, de Sa GAG, Palma JL, Llansola-Portoles MJ, Kodis G, Mujica V, Ho J, Gust D, Moore TA, Moore AL (2019) Electronic structure and triplet-triplet energy transfer in artificial photosynthetic antennas. Photochem Photobiol 95(1):211–219

    CAS  Article  Google Scholar 

  36. Wang WA, Qin XC, Sang M, Chen DQ, Wang KB, Lin RC, Lu CM, Shen JR, Kuang TY (2013) Spectral and functional studies on siphonaxanthin-type light-harvesting complex of photosystem II from Bryopsis corticulans. Photosynth Res 117(1–3):267–279

    CAS  Article  Google Scholar 

  37. West RG, Bina D, Fuciman M, Kuznetsova V, Litvin R, Polivka T (2018a) Ultrafast multi-pulse transient absorption spectroscopy of fucoxanthin chlorophyll a protein from Phaeodactylum tricornutum. BBA 1859(5):357–365

    CAS  Google Scholar 

  38. West RG, Fuciman M, Staleva-Musto H, Sebelik V, Bina D, Durchan M, Kuznetsova V, Polivka T (2018b) Equilibration dependence of fucoxanthin S1 and ICT signatures on polarity, proticity, and temperature by multipulse femtosecond absorption spectroscopy. J Phys Chem B 122(29):7264–7276

    CAS  Article  Google Scholar 

  39. Zigmantas D, Hiller RG, Sundstrom V, Polivka T (2002) Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state. Proc Natl Acad Sci USA 99(26):16760–16765

    CAS  Article  Google Scholar 

  40. Zigmantas D, Hiller RG, Yartsev A, Sundstrom V, Polivka 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(22):5339–5348

    CAS  Article  Google Scholar 

  41. Zigmantas D, Hiller RG, Sharples FP, Frank HA, Sundstrom V, Polivka T (2004) Effect of a conjugated carbonyl group on the photophysical properties of carotenoids. Phys Chem Chem Phys 6(11):3009–3016

    CAS  Article  Google Scholar 

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Acknowledgements

The authors thank the Czech Science Foundation (16-10417S and 19-28323X) for financial support. Institutional support RVO:60077344 is also acknowledged.

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Correspondence to Tomáš Polívka.

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Staleva-Musto, H., Kuznetsova, V., Bína, D. et al. Intramolecular charge-transfer state of carotenoids siphonaxanthin and siphonein: function of non-conjugated acyl-oxy group. Photosynth Res 144, 127–135 (2020). https://doi.org/10.1007/s11120-019-00694-x

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Keywords

  • Carotenoid
  • Excited-state dynamics
  • Ultrafast spectroscopy
  • Charge-transfer state