Skip to main content
SpringerLink
Log in

Investigation of the S1/ICT equilibrium in fucoxanthin by ultrafast pump–dump–probe and femtosecond stimulated Raman scattering spectroscopy

  • Original Article
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

An Erratum to this article was published on 26 October 2016

Abstract

Time-resolved multi-pulse spectroscopic methods—pump–dump–probe (PDP) and femtosecond stimulated Raman spectroscopy—were used to investigate the excited state photodynamics of the carbonyl group containing carotenoid fucoxanthin (FX). PDP experiments show that S1 and ICT states in FX are strongly coupled and that the interstate equilibrium is rapidly (<5 ps) reestablished after one of the interacting states is deliberately depopulated. Femtosecond stimulated Raman scattering experiments indicate that S1 and ICT are vibrationally distinct species. Identification of the FSRS modes on the S1 and ICT potential energy surfaces allows us to predict a possible coupling channel for the state interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. Percentages here and further in the text denote the maximal difference between the PP and PDP signals, achieved within the ca. 140 fs cross-correlation period between the dump and probe pulses.

  2. Equations 1 and 2 without the dump pulse.

Abbreviations

AP:

Actinic pump

DP:

Dump pulse

FSRS:

Femtosecond stimulated Raman scattering

FX:

Fucoxanthin

GSB:

Ground state bleaching

GSI:

Ground state intermediate

IA:

Induced absorption

ICT:

Internal charge transfer

IRF:

Instrument response function

OD:

Optical density

PP:

Pump–probe

PDP:

Pump–dump–probe

RP:

Raman pump

SADS:

Species-associated difference spectrum

SE:

Stimulated emission

SNR:

Signal-to-noise ratio

WLSc:

White light supercontinuum

References

  • Ballard LJ, Glasgow LA, Hoskins LC, Krohe T (1989) The resonance Raman excitation profile of fucoxanthin. Spectrochim Acta Mol Biomol Spectrosc 45(12):1235–1238. doi:10.1016/0584-8539(89)80235-1

    Article  Google Scholar 

  • 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. doi:10.1021/jp9916135

    Article  CAS  Google Scholar 

  • Bonetti C, Alexandre MTA, van Stokkum IHM, Hiller RG, Groot ML, van Grondelle R, Kennis JTM (2010) Identification of excited-state energy transfer and relaxation pathways in the peridinin–chlorophyll complex: an ultrafast mid-infrared study. PCCP 12(32):9256–9266. doi:10.1039/B923695C

    Article  CAS  PubMed  Google Scholar 

  • Büchel C (2003) Fucoxanthin–chlorophyll Proteins in diatoms: 18 and 19 kDa subunits assemble into different oligomeric states. Biochemistry 42(44):13027–13034. doi:10.1021/bi0349468

    Article  PubMed  Google Scholar 

  • Creelman M, Kumauchi M, Hoff WD, Mathies RA (2014) Chromophore dynamics in the PYP photocycle from femtosecond stimulated Raman spectroscopy. J Phys Chem B 118(3):659–667. doi:10.1021/jp408584v

    Article  CAS  PubMed  Google Scholar 

  • de Weerd FL, van Stokkum IHM, van Grondelle R (2002) Subpicosecond dynamics in the excited state absorption of all-trans-β-carotene. Chem Phys Lett 354(1–2):38–43. doi:10.1016/S0009-2614(02)00095-7

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1(1):21–26. doi:10.1016/S1360-1385(96)80019-7

    Article  Google Scholar 

  • Di Donato M, Ragnoni E, Lapini A, Foggi P, Hiller RG, Righini R (2015a) Femtosecond transient infrared and stimulated Raman spectroscopy shed light on the relaxation mechanisms of photo-excited peridinin. J Chem Phys 142(21):212409. doi:10.1063/1.4915072

    Article  PubMed  Google Scholar 

  • Di Donato M, Ragnoni E, Lapini A, Kardaś TM, Ratajska-Gadomska B, Foggi P, Righini R (2015b) 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(9):1592–1598. doi:10.1021/acs.jpclett.5b00528

    Article  PubMed  Google Scholar 

  • Falkowski PG, Barber RT, Smetacek V (1998) Biogeochemical controls and feedbacks on ocean primary production. Science 281(5374):200–206. doi:10.1126/science.281.5374.200

    Article  CAS  PubMed  Google Scholar 

  • Ferraro JR, Nakamoto K, Brown CW (2003) Introductory Raman spectroscopy, 2nd edn. Academic Press, Amsterdam

    Google Scholar 

  • Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63(3):257–264. doi:10.1111/j.1751-1097.1996.tb03022.x

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1021/jp000079u

    Article  CAS  Google Scholar 

  • Frontiera RR, Fang C, Dasgupta J, Mathies RA (2012) Probing structural evolution along multidimensional reaction coordinates with femtosecond stimulated Raman spectroscopy. PCCP 14(2):405–414. doi:10.1039/C1CP22767J

    Article  CAS  PubMed  Google Scholar 

  • Fujisawa T, Creelman M, Mathies RA (2012) Structural dynamics of a noncovalent charge transfer complex from femtosecond stimulated Raman spectroscopy. J Phys Chem B 116(35):10453–10460. doi:10.1021/jp3001306

    Article  CAS  PubMed  Google Scholar 

  • Hörvin Billsten H, Zigmantas D, Sundström V, Polívka T (2002) Dynamics of vibrational relaxation in the S1 state of carotenoids having 11 conjugated C=C bonds. Chem Phys Lett 355(5–6):465–470. doi:10.1016/S0009-2614(02)00268-3

    Article  Google Scholar 

  • Kardaś TM, Ratajska-Gadomska B, Lapini A, Ragnoni E, Righini R, Di Donato M, Foggi P, Gadomski W (2014) 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(20):204312. doi:10.1063/1.4879060

    Article  PubMed  Google Scholar 

  • Kennis JTM, Larsen DS, van Stokkum IHM, Vengris M, van Thor JJ, van Grondelle R (2004) Uncovering the hidden ground state of green fluorescent protein. PNAS 101(52):17988–17993. doi:10.1073/pnas.0404262102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kloz M, Rv Grondelle, Kennis JTM (2011) Wavelength-modulated femtosecond stimulated raman spectroscopy-approach towards automatic data processing. PCCP 13(40):18123–18133. doi:10.1039/C1CP21650C

    Article  CAS  PubMed  Google Scholar 

  • Kosumi D, Kusumoto T, Fujii R, Sugisaki M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Frank HA, Hashimoto H (2009) One- and two-photon pump–probe optical spectroscopic measurements reveal the S1 and intramolecular charge transfer states are distinct in fucoxanthin. Chem Phys Lett 483(1–3):95–100. doi:10.1016/j.cplett.2009.10.077

    Article  CAS  Google Scholar 

  • Kosumi D, Kusumoto T, Fujii R, Sugisaki M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Frank HA, Hashimoto H (2011a) Ultrafast excited state dynamics of fucoxanthin: excitation energy dependent intramolecular charge transfer dynamics. PCCP 13(22):10762–10770. doi:10.1039/C0CP02568B

    Article  CAS  PubMed  Google Scholar 

  • Kosumi D, Kusumoto T, Fujii R, Sugisaki M, Iinuma Y, Oka N, Takaesu Y, Taira T, Iha M, Frank HA, Hashimoto H (2011b) Ultrafast S1 and ICT state dynamics of a marine carotenoid probed by femtosecond one- and two-photon pump–probe spectroscopy. J Lumin 131(3):515–518. doi:10.1016/j.jlumin.2010.09.018

    Article  CAS  Google Scholar 

  • Kosumi D, Fujii R, Sugisaki M, Oka N, Iha M, Hashimoto H (2014a) Characterization of the intramolecular transfer state of marine carotenoid fucoxanthin by femtosecond pump–probe spectroscopy. Photosynth Res 121(1):61–68. doi:10.1007/s11120-014-9995-6

    Article  CAS  PubMed  Google Scholar 

  • Kosumi D, Kajikawa T, Okumura S, Sugisaki M, Sakaguchi K, Katsumura S, Hashimoto H (2014b) 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. doi:10.1021/jz5000287

    Article  CAS  PubMed  Google Scholar 

  • Koyama Y, Kuki M, Andersson PO, Gillbro T (1996) Singlet excited states and the light-harvesting function of carotenoids in bacterial photosynthesis. Photochem Photobiol 63(3):243–256. doi:10.1111/j.1751-1097.1996.tb03021.x

    Article  CAS  Google Scholar 

  • Kukura P, McCamant DW, Mathies RA (2004) Femtosecond time-resolved stimulated raman spectroscopy of the S(2) (1B(u)(+)) excited state of β-carotene. J Phys Chem A 108(28):5921–5925. doi:10.1021/jp0482971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kukura P, McCamant DW, Mathies RA (2007) Femtosecond stimulated Raman spectroscopy. Annu Rev Phys Chem 58(1):461–488. doi:10.1146/annurev.physchem.58.032806.104456

    Article  CAS  PubMed  Google Scholar 

  • Kuramochi H, Takeuchi S, Tahara T (2012) Ultrafast structural evolution of photoactive yellow protein chromophore revealed by ultraviolet resonance femtosecond stimulated Raman spectroscopy. J Phys Chem Lett 3(15):2025–2029. doi:10.1021/jz300542f

    Article  CAS  Google Scholar 

  • Larsen DS, van Stokkum IHM, Vengris M, van der Horst MA, de Weerd FL, Hellingwerf KJ, van Grondelle R (2004) Incoherent manipulation of the photoactive yellow protein photocycle with dispersed pump–dump–probe spectroscopy. Biophys J 87(3):1858–1872. doi:10.1529/biophysj.104.043794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macpherson AN, Gillbro T (1998) Solvent dependence of the ultrafast S2–S1 internal conversion rate of β-carotene. J Phys Chem A 102(26):5049–5058. doi:10.1021/jp980979z

    Article  CAS  Google Scholar 

  • McCamant DW, Kim JE, Mathies RA (2002) Vibrational relaxation in β-carotene probed by picosecond stokes and anti-stokes resonance Raman spectroscopy. J Phys Chem A 106(25):6030–6038. doi:10.1021/jp0203595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCamant DW, Kukura P, Mathies RA (2003a) Femtosecond broadband stimulated Raman: a new approach for high-performance vibrational spectroscopy. Appl Spectrosc 57(11):1317–1323. doi:10.1366/000370203322554455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCamant DW, Kukura P, Mathies RA (2003b) Femtosecond time-resolved stimulated Raman spectroscopy: application to the ultrafast internal conversion in β-carotene. J Phys Chem A 107(40):8208–8214. doi:10.1021/jp030147n

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCamant DW, Kukura P, Yoon S, Mathies RA (2004) Femtosecond broadband stimulated Raman spectroscopy: apparatus and methods. Rev Sci Instrum 75(11):4971–4980. doi:10.1063/1.1807566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCamant DW, Kukura P, Mathies RA (2005) Femtosecond stimulated Raman study of excited-state evolution in bacteriorhodopsin. J Phys Chem B 109(20):10449–10457. doi:10.1021/jp050095x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papagiannakis E, Larsen DS, van Stokkum IHM, Vengris M, Hiller RG, van Grondelle R (2004) Resolving the excited state equilibrium of peridinin in solution. Biochemistry 43(49):15303–15309. doi:10.1021/bi047977r

    Article  CAS  PubMed  Google Scholar 

  • Papagiannakis E, Vengris M, Larsen DS, van Stokkum IHM, Hiller RG, van Grondelle R (2006) Use of ultrafast dispersed pump–dump–probe and pump–repump–probe spectroscopies to explore the light-induced dynamics of peridinin in solution. J Phys Chem B 110(1):512–521. doi:10.1021/jp053094d

    Article  CAS  PubMed  Google Scholar 

  • Premvardhan L, Bordes L, Beer A, Büchel C, Robert B (2009) Carotenoid structures and environments in trimeric and oligomeric fucoxanthin chlorophyll a/c2 proteins from resonance Raman spectroscopy. J Phys Chem B 113(37):12565–12574. doi:10.1021/jp903029g

    Article  CAS  PubMed  Google Scholar 

  • Redeckas K, Voiciuk V, Steponavičiūtė R, Martynaitis V, Šačkus A, Vengris M (2014) Optically Controlled molecular switching of an indolobenzoxazine-type photochromic compound. J Phys Chem A 118(30):5642–5651. doi:10.1021/jp505723q

    Article  CAS  PubMed  Google Scholar 

  • Ricci M, Bradforth SE, Jimenez R, Fleming GR (1996) Internal conversion and energy transfer dynamics of spheroidene in solution and in the LH-1 and LH-2 light-harvesting complexes. Chem Phys Lett 259(3–4):381–390. doi:10.1016/0009-2614(96)00832-9

    Article  CAS  Google Scholar 

  • Shim S, Mathies RA (2008) Development of a tunable femtosecond stimulated Raman apparatus and its application to β-carotene. J Phys Chem B 112(15):4826–4832. doi:10.1021/jp710518y

    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(2–3):82–104. doi:10.1016/j.bbabio.2004.04.011

    Article  PubMed  Google Scholar 

  • Vengris M, van Stokkum IHM, He X, Bell AF, Tonge PJ, van Grondelle R, Larsen DS (2004) Ultrafast excited and ground-state dynamics of the green fluorescent protein chromophore in solution. J Phys Chem A 108(21):4587–4598. doi:10.1021/jp037902h

    Article  CAS  Google Scholar 

  • Zigmantas D, Polívka T, Hiller RG, Yartsev A, Sundström V (2001) Spectroscopic and dynamic properties of the peridinin lowest singlet excited states. J Phys Chem A 105(45):10296–10306. doi:10.1021/jp010022n

    Article  CAS  Google Scholar 

  • 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. PCCP 6(11):3009–3016. doi:10.1039/B315786E

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Quantum Electronics, Faculty of Physics, Vilnius University, Saulėtekio AV. 10, 10223, Vilnius, Lithuania

    Kipras Redeckas, Vladislava Voiciuk & Mikas Vengris

Authors
  1. Kipras Redeckas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladislava Voiciuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mikas Vengris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kipras Redeckas.

Additional information

An erratum to this article can be found at http://dx.doi.org/10.1007/s11120-016-0321-3.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 754 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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. Photosynth Res 128, 169–181 (2016). https://doi.org/10.1007/s11120-015-0215-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0215-9

Keywords

Search

Navigation