Asian Journal of Physics  Vol. 31 No 2, 2022, 227-338

Ultrafast vibrational and electronic relaxation of carotenoids investigated with Femtosecond Stimulated Raman Spectroscopy
E Ragnoni, T M Kardaś, A Lapini, P Foggi, R Righini and M Di Donato


Abstract

This paper reviews the main results obtained by using the technique of Femtosecond Stimulated Raman Spectroscopy (FSRS) to study the photophysics of carotenoids. After a brief presentation of the technique and of its practical implementation, its potentialities in disentangling the very fast relaxation processes occurring upon light absorption in carotenoids are presented. It is shown that the recourse to FSRS allows to clarify the timescale of vibrational energy relaxation in the electronic excited states of these molecules, and to clearly identify the nature of the excited states involved in the photophysics of several naturally occurring pigments, both in solution and when embedded in photosynthetic proteins. © Anita Publications. All rights reserved.
Keywords: Carotenoids, Femtosecond Stimulated Raman Spectroscopy, Internal Vibrational Relaxation.


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Method: Single- anonymous; Screened for Plagiarism? Yes
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References

  1. Enriquez M M, Fuciman M, LaFountain A M, Wagner N L, Birge R R, Frank H A, The Intramolecular Charge Transfer State in Carbonyl-Containing Polyenes and Carotenoids. J Phys Chem B, 114(2010)12416-12426.
  2. Gradinaru C C, Kennis J T M, Papagiannakis E, van Stokkum I H M, Cogdell R J, Fleming G R, Niederman R A, van Grondelle R, 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, 98(2001)2364–2369.
  3. Knecht S, Marian C M, Kongsted J, Mennucci B, On the Photophysics of Carotenoids: A Multireference DFT Study of Peridinin. J Phys Chem B 117(2013)13808–13815.
  4. Polivka T, Sundstrom V, Ultrafast Dynamics of Carotenoid Excited States. From Solution to Natural and Artificial Systems. Chem Rev, 104(2004)2021–2072.
  5. Donato M D, Centellas M S, Lapini A, Lima M, Avila F, Santoro F, Cappelli C, Righini R, Combination of Transient 2D-IR Experiments and Ab Initio Computations Sheds Light on the Formation of the Charge-Transfer State in Photoexcited Carbonyl Carotenoids, J Phys Chem B, 118(2014)9613–9630.
  6. Balevičius V(Jr), Lincoln C N, Viola D, Cerullo G, Hauer J, Abramavicius D, Effects of tunable excitation in carotenoids explained by the vibrational energy relaxation approach, Photosynth Res, 135(2018)55-64.
  7. Tavan P, Schulten K, Electronic excitations in finite and infinite polyenes, Phys Rev B, 36(1987)4337–4358.
  8. Gacek D A, Holleboom C-P, Liao P-N, Negretti M, Croce R, Walla P J, Carotenoid dark state to chlorophyll energy transfer in isolated light-harvesting complexes CP24 and CP29, Photosynth Res, 143(2020)19–30.
  9. Beck W F, Bishop M B, Roscioli J D, Ghosh S, Frank H A, Excited state conformational dynamics in carotenoids: Dark intermediates and excitation energy transfer. Arch Biochem Biophys, 572(2015)175–183.
  10. Hashimoto H, Yanagi K, Yoshizawa M, DarioPolli, Cerullo G, Lanzani G, Silvestri S D, Gardiner A T, Cogdell R J, The very early events following photoexcitation of carotenoids, Biochem Biophys, 430(2004)61–69.
  11. Ragnoni E, Donato M D, Iagatti A, Lapini A, Righini R, Mechanism of the Intramolecular Charge Transfer State Formation in all-trans-β-Apo-8′-carotenal: Influence of Solvent Polarity and Polarizability, J Phys Chem B,119(2015)420–432.
  12. Ehlers F, Wild D A, Lenzer T, Oum K, Investigation of the S1/ICT S0 Internal Conversion Lifetime of 4′-apo-β -caroten-4′-al and 8′-apo-β-caroten-8′-al: Dependence on Conjugation Length and Solvent Polarity, J Phys Chem A, 111(2007)2257–2265.
  13. Kopczynski M, Ehlers F, Lenzer T, Oum K, Evidence for an Intramolecular Charge Transfer State in 12′-Apo-β-caroten-12′-al and 8′-Apo-β-caroten-8′-al: Influence of Solvent Polarity and Temperature, J Phys Chem A, 111(2007)5370–5381.
  14. Zigmantas D, Hiller R G, Yartsev A, Sundström V, Polívka T, Dynamics of Excited States of the Carotenoid Peridinin in Polar Solvents: Dependence on Excitation Wavelength, Viscosity, and Temperature, J Phys Chem B, 107(2003)5339–5348.
  15. Polivka T, Kaligotla S, Chábera P, Frank H A, An intramolecular charge transfer state of carbonyl carotenoids: implications for excited state dynamics of apo-carotenals and retinal, Phys Chem Chem Phys, 13(2011)10787–10796.
  16. Kosumi D, Kajikawa T, Okumura S, Sugisaki M, Sakaguchi K, Katsumura S, Hashimoto H, Elucidation and Control of an Intramolecular Charge Transfer Property of Fucoxanthin by a Modification of Its Polyene Chain Length, J Phys Chem Lett, 5(2014)792–797.
  17. Kardaś T M, Ratajska-Gadomska B, Lapini A, Ragnoni E, Righini R, Donato M D, Foggi P, Gadomski W, Dynamics of the time-resolved stimulated Raman scattering spectrum in presence of transient vibronic inversion of population on the example of optically excited trans-β-apo-8′-carotenal, J Chem Phys, 140(2014)204312; doi.org/10.1063/1.4879060.
  18. Donato M D, Ragnoni E, Lapini A, Kardaś T M, Ratajska-Gadomska B, Foggi P, Righin R, Identification of the Excited-State C═C and C═O Modes of trans-β-Apo-8′-carotenal with Transient 2D-IR-EXSY and Femtosecond Stimulated Raman Spectroscopy. J Phys Chem Lett, 6(2015)1592–1598.
  19. Siebert T, Engel V, Materny A, Kiefer W, Schmitt M, Probing the Kinetics of a Nonadiabatic Transition Initiating Out of Vibrationally Excited as Well as Ground State Modes with Femtosecond Time-Resolved Transient Gratings, J Phys Chem A, 107(2003)8355–8362.
  20. Siebert T, Maksimenka R, Materny A, Engel V, Kiefer W, Schmitt M, The role of specific normal modes during non-Born-Oppenheimer dynamics: the S1→S0 internal conversion of β-carotene interrogated on a femtosecond time-scale with coherent anti-Stokes Raman scattering, J Raman Spectrosc, 33(2002)844–854.
  21. Siebert T, Schmitt M, Engel V, Materny A, Kiefer W, Population Dynamics in Vibrational Modes during Non-Born-Oppenheimer Processes: CARS Spectroscopy Used as a Mode-Selective Filter, J Am Chem Soc,124(2002) 6242-6243.
  22. McCamant D W, Kim J E, Mathies R A, Vibrational Relaxation in β-Carotene Probed by Picosecond Stokes and Anti-Stokes Resonance Raman Spectroscopy, J Phys Chem A, 106(2002)6030–6038.
  23. McCamant D W, Kukura P, Mathies R A, Femtosecond Time-Resolved Stimulated Raman Spectroscopy:  Application to the Ultrafast Internal Conversion in β-Carotene, J Phys Chem A, 107(2003)8208–8214.
  24. Yoshizawa M, Kurosawa M, Femtosecond time-resolved Raman spectroscopy using stimulated Raman scattering. Phys Rev A, 61(1999)013808; doi.org/10.1103/PhysRevA.61.013808.
  25. Frontiera R R. Mathies R A, Femtosecond stimulated Raman spectroscopy, Laser & Photonics Rev, 5(2011)102–113.
  26. Yoshizawa M, Hattori Y, Kobayashi T, Femtosecond time-resolved resonance Raman gain spectroscopy in polydiacetylene, Phys Rev B, 49(1994)13259–13262.
  27. Yoshizawa M, Aoki H, Hashimoto H, Vibrational relaxation of the 2Ag excited state in all-trans-β-carotene obtained by femtosecond time-resolved Raman spectroscopy, Phys Rev B, 63(2001)180301; doi.org/10.1103/PhysRevB.63.180301.
  28. Kukura P, McCamant D W, Mathies R A, Femtosecond Stimulated Raman Spectroscopy, Annu Rev Phys Chem, 58(2007)461–488.
  29. Dietze D R. Mathies R A, Femtosecond Stimulated Raman Spectroscopy. ChemPhysChem, 17(2016)1224–1251.
  30. Han F, Liu W, Fang C, Excited-state proton transfer of photoexcited pyranine in water observed by femtosecond stimulated Raman spectroscopy. Chem Phys, 422(2013)204–219.
  31. Mallick B, Lakhsmanna A, Umapathy S, Ultrafast Raman loss spectroscopy (URLS): instrumentation and principle. J Raman Spectrosc, 42(2011)1883–1890.
  32. Noguchi T, Hayashi H, Tasumi M, Atkinson G H, Solvent effects on the carbon-carbon double bond stretching mode in the 1Ag excited state of β-carotene and two derivatives: picosecond time-resolved resonance Raman spectroscopy, J Phys Chem, 95(1991)3167–3172.
  33. Kukura P, McCamant D W, Mathies R A, Femtosecond Time-Resolved Stimulated Raman Spectroscopy of the S2 (1Bu+) Excited State of β-Carotene. J Phys Chem A, 108(2004)5921–5925.
  34. Donato, M D, Ragnoni E, Lapini A, Foggi P, Hiller R G, Righini R, Femtosecond transient infrared and stimulated Raman spectroscopy shed light on the relaxation mechanisms of photo-excited peridinin, J Chem Phys, 142(2015)212409; doi.org/10.1063/1.4915072.
  35. Bonetti C, Alexandre M T A, van Stokkum I H M, Hiller R G, Groot M L, van Grondellea R, and John T M. Kennis J T, Identification of excited-state energy transfer and relaxation pathways in the peridinin-chlorophyll complex: an ultrafast mid-infrared study, Phys Chem Chem Phys, 12(2010)9256–9266.
  36. Frank H A, Cogdell R J, Carotenoids in Photosynthesis. Photochem Photobiol, 63(1996)257–264.
  37. Papagiannakis E, van Stokkum I H M, Vengris M, Cogdell R J, van Grondelle R, Larsen D S, Excited-State Dynamics of Carotenoids in Light-Harvesting Complexes. 1. Exploring the Relationship between the S1 and S* States, J Phys Chem B, 110(2006)5727–5736.
  38. Redeckas K, Voiciuk V, Vengris M, Investigation of the S1/ICT equilibrium in fucoxanthin by ultrafast pump–dump–probe and femtosecond stimulated Raman scattering spectroscopy, Photosynt Res, 128(2016)169–181.
  39. Vivancos J M A, van Stokkum I H M, Saccon F, Hontani Y, Kloz M, Ruban A, van Grondelle R, Kennis J T M, Unraveling the Excited-State Dynamics and Light-Harvesting Functions of Xanthophylls in Light-Harvesting Complex II Using Femtosecond Stimulated Raman Spectroscopy, J Am Chem Soc, 142(2020)17346–17355.

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