Photosynthesis Research

, Volume 135, Issue 1–3, pp 55–64 | Cite as

Effects of tunable excitation in carotenoids explained by the vibrational energy relaxation approach

  • Vytautas BalevičiusJr
  • Craig N. Lincoln
  • Daniele Viola
  • Giulio Cerullo
  • Jürgen Hauer
  • Darius AbramaviciusEmail author
Original Article


Carotenoids are fundamental building blocks of natural light harvesters with convoluted and ultrafast energy deactivation networks. In order to disentangle such complex relaxation dynamics, several studies focused on transient absorption measurements and their dependence on the pump wavelength. However, such findings are inconclusive and sometimes contradictory. In this study, we compare internal conversion dynamics in \(\beta\)-carotene, pumped at the first, second, and third vibronic progression peak. Instead of employing data fitting algorithms based on global analysis of the transient absorption spectra, we apply a fully quantum mechanical model to treat the high-frequency symmetric carbon–carbon (C=C and C–C) stretching modes explicitly. This model successfully describes observed population dynamics as well as spectral line shapes in their time-dependence and allows us to reach two conclusions: Firstly, the broadening of the induced absorption upon excess excitation is an effect of vibrational cooling in the first excited state (\(S_{1}\)). Secondly, the internal conversion rate between the second excited state (\(S_{2}\)) and \(S_{1}\) crucially depends on the relative curve displacement. The latter point serves as a new perspective on solvent- and excitation wavelength-dependent experiments and lifts contradictions between several studies found in literature.


Internal conversion \(\beta\)-carotene Transient absorption spectroscopy Vibrational cooling 



V. B. acknowledges funding by the Leverhulme Trust Research Project Grant RPG-2015-337. J. H. and C. N. L. acknowledge funding by the Austrian Science Fund (FWF): START project Y 631-N27. D. A. acknowledges support by the Research Council of Lithuania (No MIP-090/2015). G. C. acknowledges support by the European Research Council Advanced Grant STRATUS (ERC-2011-AdG No. 291198). G. C. and J. H. acknowledge funding by Laserlab-Europe (EU-H2020 654148).


  1. Andersson PO, Gillbro T (1995) Photophysics and dynamics of the lowest excited singlet-state in long susbtituted polyenes with implications to the very long-chain limit. J Chem Phys 103(7):2509–2519CrossRefGoogle Scholar
  2. Balevičius V Jr, Pour AG, Savolainen J, Lincoln CN, Lukeš V, Riedle E, Valkunas L, Abramavicius D, Hauer J (2015) Vibronic energy relaxation approach highlighting deactivation pathways in carotenoids. Phys Chem Phys Chem 17:19491–19499CrossRefGoogle Scholar
  3. Balevičius V Jr, Abramavicius D, Polívka T, Galestian Pour A, Hauer J (2016) A unified picture of S* in carotenoids. J Phys Chem Lett 7:3347–3352CrossRefPubMedPubMedCentralGoogle Scholar
  4. Billsten HH, Zigmantas D, Sundström V, Polívka T (2002) Dynamics of vibrational relaxation in the \({S}_{1}\) state of carotenoids having 11 conjugated C=C bonds. Chem Phys Lett 355:465–470CrossRefGoogle Scholar
  5. Billsten HH, Pan J, Sinha S, Pascher T, Sundström V, Polívka T (2005) Excited-state processes in the carotenoid zeaxanthin after excess energy excitation. J Phys Chem A 109:6852–6859CrossRefPubMedGoogle Scholar
  6. Cerullo G, Silvestri SD (2003) Ultrafast optical parametric amplifiers. Rev Sci Instrum 74(1):1–18CrossRefGoogle Scholar
  7. Chábera P, Fuciman M, Hřibek P, Polívka T (2009) Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids. Phys Chem Chem Phys 11(39):8795–8803CrossRefPubMedGoogle Scholar
  8. Christensson N, Milota F Milota F, Nemeth A, Sperling J, Kauffmann HF, Pullerits T, Hauer J (2009) Two-dimensional electronic spectroscopy of \(\beta\)-carotene. J Phys Chem B 113(51):16409–16419CrossRefPubMedGoogle Scholar
  9. Christensson N, Milota F, Nemeth A, Pugliesi I, Riedle E, Sperling J, To Pullerits, Kauffmann HF, Hauer J (2010) Electronic double-quantum coherences and their impact on ultrafast spectroscopy: the example of \(\beta\)-carotene. J Phys Chem Lett 1:3366–3370CrossRefPubMedPubMedCentralGoogle Scholar
  10. DeCoster B, Christensen RL, Gebhard R, Lugtenburg J, Farhoosh R, Frank HA (1992) Low-lying electronic states of carotenoids. Biochim Biophys Acta Bioenerget 1102(1):107–114CrossRefGoogle Scholar
  11. de Weerd FL, van Stokkum IHM, van Grondelle R (2002) Subpicosecond dynamics in the excited state absorption of all-trans-\(\beta\)-carotene. Chem Phys Lett 354:38–43CrossRefGoogle Scholar
  12. Dilbeck PL, Tang Q, Mothersole DJ, Martin EC, Hunter NC, Bocian DF, Holten D, Niedzwiedzki DM (2016) Quenching capabilities of long-chain carotenoids in light-harvesting-2 complexes from Rhodobacter sphaeroides with an engineered carotenoid synthesis pathway. J Phys Chem B 120:5429–5443CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dobryakov AL, Kovalenko SA (2005) Coherent and sequential contributions to femtosecond transient absorption spectra of a rhodamine dye in solution. J Chem Phys 123(4):44502CrossRefGoogle Scholar
  14. Frank H, Young A, Britton G, Cogdell R (eds) (1999) The Photochemistry of carotenoids, advances in photosynthesis and respiration, vol 8. Springer, DordrechtGoogle Scholar
  15. Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63(3):257–264CrossRefPubMedGoogle Scholar
  16. Fujii R, Onaka K, Kuki M, Koyama Y, Watanabe Y (1998) ) The 2A\(_{g}^{-}\) energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy. Chem Phys Lett 288:847–853CrossRefGoogle Scholar
  17. Hauer J, Maiuri M, Viola D, Lukes V, Henry S, Carey AM, Cogdell RJ, Cerullo G, Polli D (2013) Explaining the temperature dependence of spirilloxanthin’s S* signal by an inhomogeneous ground state model. J Phys Chem A 117:6303–6310CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jailaubekov AE, Vengris M, Song SH, Kusumoto T, Hashimoto H, Larsen DS (2011) Deconstructing the excited-state dynamics of \(\beta\)-carotene in solution. J Phys Chem A 115:3905–3916CrossRefPubMedGoogle Scholar
  19. Kloz M, Pillai S, Kodis G, Gust D, Moore TA, Moore AL, van Grondelle R, Kennis JTM (2012) New light-harvesting roles of hot and forbidden carotenoid states in artificial photosynthetic constructs. Chem Sci 3:2052–2061CrossRefGoogle Scholar
  20. Kosumi D, Yanagi K, Nishio T, Hashimoto H, Yoshizawa M (2005) Excitation energy dependence of excited states dynamics in all-trans-carotenes determined by femtosecond absorption and fluorescence spectroscopy. Chem Phys Lett 408:89–95CrossRefGoogle Scholar
  21. Larsen DS, Papagiannakis E, Stokkum IHM, Vengris M, Kennis JTM, van Grondelle R (2003) Excited state dynamics of \(\beta\)-carotene explored with dispersed multi-pulse transient absorption. Chem Phys Lett 381:733–742CrossRefGoogle Scholar
  22. Lukeš V, Christensson N, Milota F, Kauffmann HF, Hauer J (2011) Electronic ground state conformers of \(\beta\)-carotene and their role in ultrafast spectroscopy. Chem Phys Lett 506(1–3):122–127Google Scholar
  23. May V, Kühn O (2004) Charge and energy transfer in molecular systems. Wiley, WeinheimGoogle Scholar
  24. Nakamura R, Fujii R, Nagae H, Koyama Y, Kanematsu Y (2004) Vibrational relaxation in the \(1{B}_{u}^{+}\) state of carotenoids as determined by Kerr-gate fluorescence spectroscopy. Chem Phys Lett 400:7–14CrossRefGoogle Scholar
  25. Nakamura R, Wang P, Fujii R, Koyama Y, Hashimoto H, Kanematsu Y (2006) Vibrational relaxation pathways in the electronic excited state of carotenoid. J Lumin 119–120:442–447CrossRefGoogle Scholar
  26. Niedzwiedzki DM, Hunter CN, Blankenship RE (2016) Evaluating the nature of so-called S*-state feature in transient absorption of carotenoids in light-harvesting complex 2 (LH2) from purple photosynthetic bacteria. J Phys Chem B 120(43):11123–11131CrossRefPubMedPubMedCentralGoogle Scholar
  27. Papagiannakis E, van Stokkum IHM, Vengris M, Cogdell RJ, van Grondelle R, Larsen DS (2006) Excited-state dynamics of carotenoids in light-harvesting complexes. 1. exploring the relationship between the S1 and S* state. J Phys Chem B 110(11):5727–5736CrossRefPubMedGoogle Scholar
  28. Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states—from solution to natural and artificial systems. Chem Rev 104:2021–2071CrossRefPubMedGoogle Scholar
  29. Polívka T, Sundström V (2009) Dark excited states of carotenoids: consensus and controversy. Chem Phys Lett 477:1–11CrossRefGoogle Scholar
  30. Polívka T, Zigmantas D, Frank HA, Bautista JA, Herek JL, Koyama Y, Fujii R, Sundström V (2001) Near-infrared time-resolved study of the \({S}_{1}\) state dynamics of the carotenoid spheroidene. J Phys Chem B 105:1072–1080CrossRefGoogle Scholar
  31. Staleva H H, Zeeshan M, Chábera P, Partali V, Sliwka HR, Polívka T (2015) Ultrafast dynamics of long homologues of carotenoid zeaxanthin. J Phys Chem A 119(46):11304–11312CrossRefPubMedGoogle Scholar
  32. Takaya T, Iwata K (2014) Relaxation mechanism of \(\beta\)-carotene from \(S_{2}\) \((1B_{u}^{+})\) state to \(S_{1}\) \((2A_{g}^{-})\) state: femtosecond time-resolved near-IR absorption and stimulated resonance Raman studies in 900–1550 nm region. J Phys Chem A 118(23):4071–4078CrossRefPubMedGoogle Scholar
  33. Valkunas L, Abramavicius D, Mančal T (2013) Molecular excitation dynamics and relaxation. Wiley, WeinheimCrossRefGoogle Scholar
  34. van Amerongen H, Valkunas L, van Grondelle R (2000) Photosynthetic excitons. World Scientific, SingaporeCrossRefGoogle Scholar
  35. Wendling M, Pullerits T, Przyjalgowski MA, Vulto SIE, Aartsma TJ, van Grondelle R, van Amerongen H (2000) Electron-vibrational coupling in the Fenna–Matthews–Olson complex of Prosthecochloris aestuarii determined by temperature-dependent absorption and fluorescence line-narrowing measurements. J Phys Chem B 104:5825–5831CrossRefGoogle Scholar
  36. Young AJ, Britton G (eds) (1993) Carotenoids in photosynthesis. Chapman & Hall, LondonGoogle Scholar
  37. Zhang JP, Skibsted LH, Fujii R, Koyama Y (2001) Transient absorption from the 1B\(_u^{+}\) state of all-trans-\(\beta\)-carotene newly identified in the near-infrared region. Photochem Photobiol 73(3):219–222CrossRefPubMedGoogle Scholar
  38. Zuo P, Sutresno A, Li C, Koyama Y, Nagae H (2007) Vibrational relaxation on the mixed vibronic levels of the \(1{B}_{u}^{+}\) and \(1{B}_{u}^{-}\) states in all-trans-neurosporene as revealed by subpicosecond time-resolved, stimulated emission and transient absorption spectroscopy. Chem Phys Lett 440:360–366CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Vytautas BalevičiusJr
    • 2
  • Craig N. Lincoln
    • 3
  • Daniele Viola
    • 4
  • Giulio Cerullo
    • 4
  • Jürgen Hauer
    • 3
  • Darius Abramavicius
    • 1
    Email author
  1. 1.Department of Theoretical PhysicsVilnius UniversityVilniusLithuania
  2. 2.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK
  3. 3.Photonics InstituteTU WienViennaAustria
  4. 4.IFN-CNR, Dipartimento di FisicaPolitecnico di MilanoMilanItaly

Personalised recommendations