Skip to main content

Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes

Photosynthesis Research volume 127, pages 33–47 (2016)Cite this article

Abstract

Oscillatory features of two-dimensional spectra of photosynthetic pigment–protein complexes during few picoseconds after electronic excitations of chlorophylls in various pigment–proteins were recently related to the coherent nuclear vibrations. It has been also speculated that the vibrations may assist the excitonic energy transfer and charge separation, hence contributing to energy transport and energy conversion efficiency. Here, we consider three theoretical approaches usually used for characterization of the excitation dynamics and charge separation, namely Redfield, Förster, and Marcus model descriptions, regarding this question. We show that two out of the three mechanisms require explicit resonances of excitonic splittings and the nuclear vibration frequencies. However, the third one related to the electron transfer is in principle off resonant.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Abramavicius D, Mukamel S (2010) Quantum oscillatory exciton migration in photosynthetic reaction centers. J Chem Phys 133:064510

    Article  PubMed  Google Scholar 

  • Abramavicius D, Mukamel S (2011) Exciton dynamics in chromophore aggregates with correlated environment fluctuations. J Chem Phys 134:174504

    PubMed Central  Article  PubMed  Google Scholar 

  • Abramavicius D, Gulbinas V, Valkunas L (2003) Acceleration of charge separation by oscillations of the environment polarization. Chem Phys Lett 368:480

    Article  CAS  Google Scholar 

  • Abramavicius D, Voronine DV, Mukamel S (2008) Unraveling coherent dynamics and energy dissipation in photosynthetic complexes by 2D spectroscopy. Biophys J 94:3613–3619

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Balevičius V Jr, Gelzinis A, Abramavicius D, Mančal T, Valkunas L (2012) Excitation dynamics and relaxation in a molecular heterodimer. Chem Phys 404:94–102

    Article  Google Scholar 

  • Balevičius V Jr, Gelzinis A, Abramavicius D, Valkunas L (2013) Excitation energy transfer and quenching in a heterodimer: applications to the carotenoid-phthalocyanine dyads. J Phys Chem B 117(38):11031–11041

    Article  PubMed  Google Scholar 

  • Ball P (2011) The dawn of quantum biology. Nature 474:272

    Article  CAS  PubMed  Google Scholar 

  • Barzykin AV, Frantsuzov PA, Seki K, Tachiya M (2002) Solvent effects in nonadiabatic electron-transfer reactions: theoretical aspects. Adv Chem Phys 123:511

    CAS  Google Scholar 

  • Basinskaite E, Butkus V, Abramavicius D, Valkunas L (2014) Vibronic models for nonlinear spectroscopy simulations. Photosynth Res 121:95

    Article  CAS  PubMed  Google Scholar 

  • Bixon M, Jortner J (1997) Electron transfer via bridges. J Chem Phys 107:5154

    Article  CAS  Google Scholar 

  • Breuer H-P, Petruccione F (2002) The theory of open quantum systems. Oxford University Press, New York

    Google Scholar 

  • Butkus V, Valkunas L, Abramavicius D (2011) Semiconductors and semimetals. In: Quantum efficiency in complex systems, part II, chap: interplay of exciton coherence and dissipation in molecular aggregates, vol 85. Academic Press, San Diego, pp 3–46

  • Butkus V, Valkunas L, Abramavicius D (2012) Molecular vibrations-induced quantum beats in two-dimensional electronic spectroscopy. J Chem Phys 137:044513

    Article  PubMed  Google Scholar 

  • Butkus V, Zigmantas D, Valkunas L, Abramavicius D (2012) Vibrational vs. electronic coherences in 2D spectrum of molecular systems. Chem Phys Lett 545:40–43

    Article  CAS  Google Scholar 

  • Butkus V, Zigmantas D, Abramavicius D, Valkunas L (2013) Distinctive character of electronic and vibrational coherences in disordered molecular aggregates. Chem Phys Lett 587:93–98

    Article  CAS  Google Scholar 

  • Butkus V, Valkunas L, Abramavicius D (2014) Vibronic phenomena and exciton-vibrational interference in two-dimensional spectra of molecular aggregates. J Chem Phys 140:034306

    Article  PubMed  Google Scholar 

  • Caruso F, Chin AW, Datta A, Huelga SF, Plenio MB (2009) Highly efficient energy excitation transfer in light-harvesting complexes: the fundamental role of noise-assisted transport. J Chem Phys 131:105106

    Article  Google Scholar 

  • Caycedo-Soler F, Chin AW, Almeida J, Huelga SF, Plenio MB (2012) The nature of the low energy band of the Fenna-Matthews–Olson complex: vibronic signatures. J Chem Phys 136:155102

    Article  PubMed  Google Scholar 

  • Chachisvilis M, Fidder H, Pullerits T, Sundström V (1995) Coherent nuclear motions in light-harvesting pigments and dye molecules, probed by ultrafast spectroscopy. J Raman Spectrosc 26:513–522

    Article  CAS  Google Scholar 

  • Chenu A, Christensson N, Kauffmann HF, Mančal T (2013) Enhancement of vibronic and ground-state vibrational coherences in 2D spectra of photosynthetic complexes. Sci Rep 3:2029

    PubMed Central  Article  PubMed  Google Scholar 

  • Chin AW, Prior J, Rosenbach R, Caycedo-Soler F, Huelga SF, Plenio MB (2013) The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment–protein complexes. Nat Phys 9:113–118

    Article  CAS  Google Scholar 

  • Chorosajev V, Gelzinis A, Valkunas L, Abramavicius D (2014) Dynamics of exciton–polaron transition in molecular assemblies: the variational approach. J Chem Phys 140:244108

    Article  PubMed  Google Scholar 

  • Christensson N, Milota F, Hauer J, Sperling J, Bixner O, Nemeth A, Kauffmann HF (2011) High frequency vibrational modulations in two-dimensional electronic spectra and their resemblance to electronic coherence signatures. J Phys Chem B 115:5383–5391

    Article  CAS  PubMed  Google Scholar 

  • Christensson N, Kauffmann HF, Pullerits T, Mančal T (2012) Origin of long-lived coherences in light-harvesting complexes. J Phys Chem B 116:7449–7454

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Collini E, Scholes GD (2009) Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323:369–373

    Article  CAS  PubMed  Google Scholar 

  • Engel GS, Calhoun TR, Read EL, Ahn TK, Mančal T, Cheng Y-C, Blankenship RE, Fleming GR (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786

    Article  CAS  PubMed  Google Scholar 

  • Fassioli F, Dinshaw R, Arpin PC, Scholes GD (2013) Photosynthetic light harvesting: excitons and coherence. J R Soc Interface 11:20130901

    Article  PubMed  Google Scholar 

  • Ferretti M, Novoderezhkin VI, Romero E, Augulis R, Pandit A, Zigmantas D, van Grondelle R (2014) The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy. Phys Chem Chem Phys 16:9930–9939

    Article  CAS  PubMed  Google Scholar 

  • Förster Th (1948) Zwischenmolekulare energiewanderung und fluoreszenz. Ann Physik 6:55

    Article  Google Scholar 

  • Fuller FD, Pan J, Gelzinis A, Butkus V, Senlik SS, Wilcox DE, Yocum CF, Valkunas L, Abramavicius D, Ogilvie JP (2014) Vibronic coherence in oxygenic photosynthesis. Nat Chem 6:706

    CAS  PubMed  Google Scholar 

  • Gelzinis A, Abramavicius D, Valkunas L (2011) Non-Markovian effects in time-resolved fluorescence spectrum of molecular aggregates: tracing polaron formation. Phys Rev B 84:245430

    Article  Google Scholar 

  • Gelzinis A, Valkunas L, Fuller FD, Ogilvie JP, Mukamel S, Abramavicius D (2013) Tight-binding model of the photosystem ii reaction center: application to two-dimensional electronic spectroscopy. New J Phys 15:075013

    Article  Google Scholar 

  • Harel E, Engel GS (2012) Quantum coherence spectroscopy reveals complex dynamics in bacterial light-harvesting complex 2 (LH2). Proc Natl Acad Sci USA 109:706–711

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Heitele H (1993) Dynamic solvent effects on electron-transfer reactions. Angew Chem Int Ed Eng 32(3):359–377

    Article  Google Scholar 

  • Ishizaki A, Fleming GR (2009a) Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc Natl Acad Sci USA 106:17255–17260

    PubMed Central  Article  PubMed  Google Scholar 

  • Ishizaki A, Fleming GR (2009b) Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: reduced hierarchy equation approach. J Chem Phys 130:234111

    Article  PubMed  Google Scholar 

  • Jang S, Newton MD, Silbey RJ (2004) Multichromophoric förster resonance energy transfer. Phys Rev Lett 92:218301

    Article  PubMed  Google Scholar 

  • Jankowiak R, Reppert M, Zazubovich V, Pieper J, Reinot T (2011) Site selective and single complex laser-based spectroscopies: a window on excited state electronic structure, excitation energy transfer, and electron phonon coupling of selected photosynthetic complexes. Chem Rev 111:4546

    Article  CAS  PubMed  Google Scholar 

  • Kell A, Feng X, Reppert M, Jankowiak RJ (2013) On the shape of the phonon spectral density in photosynthetic complexes. J Phys Chem B 117:7317–7323

    Article  CAS  PubMed  Google Scholar 

  • Kolli A, O’Reilly EJ, Scholes GD, Olaya-Castro A (2012) The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J Chem Phys 137:174109

    Article  PubMed  Google Scholar 

  • Lee H, Cheng Y-C, Fleming GR (2007) Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316:1462–1465

    Article  CAS  PubMed  Google Scholar 

  • Lewis KLM, Fuller FD, Myers JA, Yocum CF, Mukamel S, Abramavicius D, Ogilvie JP (2013) Simulations of the two-dimensional electronic spectroscopy of the photosystem II reaction center. J Phys Chem A 117(1):34–41

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Loudon R (2000) Quantum theory of light, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Mančal T, Valkunas L (2010) Exciton dynamics in photosynthetic complexes: excitation by coherent and incoherent light. New J Phys 12(6):065044

    Article  Google Scholar 

  • Mančal T, Valkunas L, Read EL, Engel GS, Calhoun TR, Fleming GR (2008) Electronic coherence transfer in photosynthetic complexes and its signatures in optical spectroscopy. Spectroscopy 22:199–211

    Article  Google Scholar 

  • Mančal T, Balevičius Jr. V, Valkunas L (2011) Decoherence in weakly coupled excitonic complexes. J Phys Chem A 115:3845–3858

    Article  PubMed  Google Scholar 

  • Marcus RA (1963) On the theory of oxidation-reduction reactions involving electron transfer. V. Comparison and properties of electrochemical and chemical rate constants. J Phys Chem 67:853–857

    Article  CAS  Google Scholar 

  • Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811(3):265–322

    Article  CAS  Google Scholar 

  • May V, Kühn O (2011) Charge and energy transfer dynamics in molecular systems. Wiley-VCH, Weinheim

    Book  Google Scholar 

  • Milota F, Sperling J, Nemeth A, Kauffmann HF (2009) Two-dimensional electronic photon echoes of a double band J-aggregate: quantum oscillatory motion versus exciton relaxation. Chem Phys 357(1–3):45–53

    Article  CAS  Google Scholar 

  • Mohseni M, Omar Y, Engel GS, Plenio MB (eds) (2014) Quantum effects in biology. Cambridge University Press, Cambridge

  • Novoderezhkin V, Palacios MA (2005) Exciton dynamics in the LHCII complex of higher plants: modelling based on the 2.72 Å crystal structure. J Phys Chem B 109:10493–10504

    Article  CAS  PubMed  Google Scholar 

  • Novoderezhkin VI, Andrizhiyevskaya EG, Dekker JP, van Grondelle R (2005) Pathways and timescales of primary charge separation in the photosystem II reaction center as revealed by a simultaneous fit of time-resolved fluorescence and transient absorption. Biophys J 89:1464–1481

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Novoderezhkin V, Dekker JP, van Amerongen H, van Grondelle R (2007) Mixing of exciton and charge-transfer states in photosystem II reaction centers: modeling of Stark spectra with modified Redfield theory. Biophys J 93:1293–1311

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Novoderezhkin VI, Romero E, Dekker JP, van Grondelle R (2011) Multiple charge-separation pathways in photosystem II: modeling of transient absorption kinetics. ChemPhysChem 12(3):681–688

    Article  CAS  PubMed  Google Scholar 

  • Panitchayangkoon G, Voronine DV, Abramavicius D, Caram JR, Lewis NHC, Mukamel S, Engel GS (2011) Direct evidence of quantum transport in photosynthetic light-harvesting complexes. Proc Natl Acad Sci USA 108:20908–20912

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Pope M, Swenberg CE (1999) Electronic processes in organic crystals and polymers, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Prior J, Chin AW, Huelga SF, Plenio MB (2010) Efficient simulation of strong system–environment interactions. Phys Rev Lett 105:050404

    Article  PubMed  Google Scholar 

  • Rancova O, Sulskus J, Abramavicius D (2012) Insight into the structure of photosynthetic LH2 aggregate from spectroscopy simulations. J Phys Chem B 116:7803–7814

    Article  CAS  PubMed  Google Scholar 

  • Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130:4431–4446

    Article  CAS  PubMed  Google Scholar 

  • Raszewski G, Saenger W, Renger T (2005) Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J 88:986–998

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Raszewski G, Diner BA, Schlodder E, Renger T (2008) Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys J 95:105–119

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Rebentrost P, Mohseni M, Kassal I, Lloyd S, Aspuru-Guzik A (2009) Environment-assisted quantum transport. New J Phys 11:033003

    Article  Google Scholar 

  • Redfield AG (1957) On the theory of relaxation processes. IBM J Res Dev 1:19–31

    Article  Google Scholar 

  • Renger T, Marcus RA (2002) On the relation of protein dynamics and exciton relaxation in pigment-protein complexes: an estimation of the spectral density and a theory for the calculation of optical spectra. J Chem Phys 116(22):9997–10019

    Article  CAS  Google Scholar 

  • Renger T, Schlodder E (2011) Optical properties, excitation energy and primary charge transfer in photosystem II: theory meets experiment. J Photochem Photobiol B 104:126–141

    Article  CAS  PubMed  Google Scholar 

  • Romero E, Augulis R, Novoderezhkin VI, Ferretti M, Thieme J, Zigmantas D, van Grondelle R (2014) Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat Phys 10:676

    Article  CAS  Google Scholar 

  • Ryu IS, Dong H, Fleming GR (2014) Role of electronic-vibrational mixing in enhancing vibrational coherences in the ground electronic states of photosynthetic bacterial reaction center. J Phys Chem B 118(5):1381–1388

    Article  CAS  PubMed  Google Scholar 

  • Savikhin S, Buck DR, Struve WS (1997) Oscillating anisotropies in a bacteriochlorophyll protein: evidence for quantum beating between exciton levels. Chem Phys 223:303–312

    Article  CAS  Google Scholar 

  • Schlau-Cohen GS, Calhoun TR, Ginsberg NS, Read EL, Ballottari M, Bassi R, van Grondelle R, Fleming GR (2009) Pathways of energy flow in LHCII from two-dimensional electronic spectroscopy. J Phys Chem B 113:15352–15363

    Article  CAS  PubMed  Google Scholar 

  • Schlau-Cohen GS, Ishizaki A, Fleming GR (2011) Two-dimensional electronic spectroscopy and photosynthesis: fundamentals and applications to photosynthetic light-harvesting. Chem Phys 386:1–22

    Article  CAS  Google Scholar 

  • Schlösshauer MA (2007) Decoherence and the quantum-to-classical transition. The frontiers collection. Springer, Berlin

    Google Scholar 

  • Scholes GD, Fleming GR, Olaya-Castro A, van Grondelle R (2011) Lessons from nature about solar light harvesting. Nat Chem 3:763–774

    Article  CAS  PubMed  Google Scholar 

  • Schulze J, Torbjörnsson M, Kühn O, Pullerits T (2014) Exciton coupling induces vibronic hyperchromism in light-harvesting complexes. New J Phys 16:045010

    Article  Google Scholar 

  • Seibt J, Pullerits T (2013) Beating signals in 2D spectroscopy: electronic or nuclear coherences? Application to a quantum dot model system. J Phys Chem B 117:18728–18737

    Article  CAS  Google Scholar 

  • Seibt J, Hansen T, Pullerits T (2013) 3D spectroscopy of vibrational coherences in quantum dots: theory. J Phys Chem B 117:11124–11133

    Article  CAS  PubMed  Google Scholar 

  • Song A, Williams R (1993) Self-trapped excitons, vol 105. Springer series in solid-state sciences. Springer, Berlin

  • Spano FC (2010) The spectral signatures of Frenkel polarons in H- and J-aggregates. Acc Chem Res 43:429–439

    Article  CAS  PubMed  Google Scholar 

  • Spano FC, Silvestri L (2010) Multiple mode exciton-vibrational coupling in H-aggregates: synergistic enhancement of the quantum yield. J Chem Phys 132:094704

    Article  CAS  PubMed  Google Scholar 

  • Spano FC, Clark J, Silva C, Friend RH (2009) Determining exciton coherence from the photoluminescence spectral line shape in poly(3-hexylthiophene) thin films. J Chem Phys 130:074904

    Article  PubMed  Google Scholar 

  • Sumi H, Marcus RA (1986) Dynamical effects in electron transfer reactions. J Chem Phys 84(9):4894–4914

    Article  CAS  Google Scholar 

  • Sundström V, Pullerits T, van Grondelle R (1999) Photosynthetic light-harvesting: reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J Phys Chem B 103:2327–2346

    Article  Google Scholar 

  • Tanimura Y (2006) Stochastic Liouville, Langevin, Fokker-Planck, and master equation approaches to quantum dissipative systems. J Phys Soc Jpn 75:082001

    Article  Google Scholar 

  • Timpmann K, Rätsep M, Hunter CN, Freiberg A (2004) Emitting excitonic polaron states in core LH1 and peripheral LH2 bacterial light-harvesting complexes. J Phys Chem B 108(29):10581–10588

    Article  CAS  Google Scholar 

  • Tiwari V, Peters WK, Jonas DM (2013) Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc Natl Acad Sci USA 110:1203–1208

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Valkunas L, Abramavicius D, Mančal T (2013) Molecular excitation dynamics and relaxation. Wiley-VCH, Weinheim

    Book  Google Scholar 

  • van Amerogen H, Valkunas L, van Grondelle R (2000) Photosynthetic excitons. World Scientific, Singapore

    Book  Google Scholar 

  • van Kampen NG (2007) Stochastic processes in physics and chemistry, 3rd edn. North Holland, Amsterdam

  • Warshel A, Parson WW (2001) Dynamics of biochemical and biophysical reactions: insight from computer simulations. Q Rev Biophys 34:563

    Article  CAS  PubMed  Google Scholar 

  • Westenhoff S, Paleček D, Edlund P, Smith P, Zigmantas D (2012) Coherent picosecond exciton dynamics in a photosynthetic reaction center. J Am Chem Soc 134:16484–16487

    Article  CAS  PubMed  Google Scholar 

  • Womick JM, Moran AM (2011) Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes. J Phys Chem B 115:1347–1356

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Fleming GR (2002) Influence of phonons on exciton transfer dynamics: comparison of the Redfield, Förster, and modified Redfield equations. Chem Phys 275:355–372

    Article  CAS  Google Scholar 

  • Zhang WM, Meier T, Chernyak V, Mukamel S (1998) Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J Chem Phys 108:7763–7774

    Article  CAS  Google Scholar 

  • Zhu J, Kais S, Rebentrost P, Aspuru-Guzik A (2011) Modified scaled hierarchical equation of motion approach for the study of quantum coherence in photosynthetic complexes. J Phys Chem B 115:1531–1537

    Article  CAS  PubMed  Google Scholar 

  • Zigmantas D, Read EL, Mančal T, Brixner T, Gardiner AT, Cogdell RJ, Fleming GR (2006) Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex. Proc Natl Acad Sci USA 103:12672–12677

    PubMed Central  Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Theoretical Physics, Vilnius University, Sauletekio al. 9-III, 10222, Vilnius, Lithuania

    Darius Abramavicius & Leonas Valkunas

  2. Center for Physical Sciences and Technology, A. Gostauto 11, 01108, Vilnius, Lithuania

    Leonas Valkunas

Authors
  1. Darius Abramavicius
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leonas Valkunas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leonas Valkunas.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abramavicius, D., Valkunas, L. Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes. Photosynth Res 127, 33–47 (2016). https://doi.org/10.1007/s11120-015-0080-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-015-0080-6

Keywords

  • Vibrational coherence
  • Electronic coherence
  • Electron transfer
  • Energy transfer