A vibronic-exciton model is applied to investigate the recently proposed mechanism of enhancement of coherent oscillations due to mixing of electronic and nuclear degrees of freedom. We study a dimer system to elucidate the role of resonance coupling, site energies, vibrational frequency and energy disorder in the enhancement of vibronic-exciton and ground-state vibrational coherences, and to identify regimes where this enhancement is significant. For a heterodimer representing two coupled bachteriochloropylls of the FMO complex, long-lived vibronic coherences are found to be generated only when the frequency of the mode is in the vicinity of the electronic energy difference. Although the vibronic-exciton coherences exhibit a larger initial amplitude compared to the ground-state vibrational coherences, we conclude that, due to the dephasing of the former, both type of coherences have a similar magnitude at longer population time.

Faculty of Mathematics and Physics Charles University Prague Prague 2 Czech Republic

Zobrazit více v PubMed

Engel G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782 (2007). PubMed

Prokhorenko V. I., Holzwarth A. R., Nowak F. R. & Aartsma T. J. Growing-In of Optical Coherence in the FMO antenna complexes. J. Phys. Chem. B 106, 9923–9933 (2002).

Savikhin S., Buck D. R. & Struve W. S. Oscillating anisotropies in a bacteriochlorophyll protein: Evidence for quantum beating between exciton levels. J. Chem. Phys. 223, 303–312 (1997).

Lee H., Cheng Y.-C. & Fleming G. Coherence dynamics in photosynthesis: Protein protection of excitonic coherence. Science 316, 1462–1465 (2007). PubMed

Caram J. R., Lewis N. H. C., Fidler A. F. & Engel G. S. Signatures of correlated excitonic dynamics in two-dimensional spectroscopy of the fenna-matthew-olson photosynthetic complex. J. Chem. Phys. 136, 104505 (2012). PubMed

Kreisbeck C. & Kramer T. Long-lived electronic coherence in dissipative exciton dynamics of light-harvesting complexes. J. Phys. Chem. Lett. 3, 2828 (2012).

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

Ishizaki A. & Fleming G. R. Quantum superpositions in photosynthetic light harvesting: delocalization and entanglement. New J. Phys. 12, 055004 (2010).

Hayes D. et al. Dynamics of electronic dephasing in the Fenna-Matthews-Olson complex. New J. Phys. 12, 065042 (2010).

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

Caycedo-Soler F., Chin A. W., Almeida J., Huelga S. F. & Plenio M. B. The nature of the low energy band of the Fenna-Matthews-Olson complex: Vibronic signatures. J. Chem. Phys. 136, 155102 (2012). PubMed

Fidler A. F., Harel E., Long P. D. & Engel G. S. Two-dimensional spectroscopy can distinguish between decoherence and dephasing of zero-quantum coherences. J. Phys. Chem. A 116, 282–289 (2012). PubMed

Olbrich C. et al. From atomistic modeling to excitation transfer and two-dimensional spectra of the FMO light-harvesting complex. J. Phys. Chem. B 115, 8609–8621 (2011). PubMed PMC

Shim S., Rebentrost P., Valleau S. & Aspuru-Guzik A. Atomistic Study of the Long-Lived Quantum Coherences in the Fenna-Matthews-Olson Complex. Biophys. J. 102, 649–660 (2012). PubMed PMC

Wu J., Liu F., Shen Y., Cao J. & Silbey R. J. Efficient energy transfer in light-harvesting systems, I: Optimal temperature, reorganization energy and spatial-temporal correlations. New J. Phys. 12, 105012 (2010).

Cho M. H., Vaswani H. M., Brixner T., Stenger J. & Fleming G. R. Exciton analysis in 2D electronic spectroscopy. J. Phys. Chem. B 109, 10542 (2005). PubMed

Blankenship R. E. Molecular Mechanism of Photosynthesis (Blackwell Science, Oxford, 2002).

Cheng Y.-C. & Fleming G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241 (2009). PubMed

Jiang X.-P. & Brumer P. Creation and dynamics of molecular states prepared with coherent vs partially coherent pulsed light. J. Chem. Phys. 94, 5833 (1991).

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

Brumer P. & Shapiro M. Molecular response in one photon absorption: Coherent pulsed laser vs. thermal incoherent source. ArXiv 1109.0026v2 (2011).

Hoki K. & Brumer P. Excitation of biomolecules by coherent vs. incoherent light: Model rhodopsin photoisomerization. In Procedia Chemistry vol. 3, 122–131 (Elsevier, 22nd Solvay Conference on Chemistry, 2011).

Pachón L. A. & Brumer P. Incoherent excitation of thermally equilibrated open quantum systems. ArXiv 1210.6374v1 (2012).

Dostál J. et al. Two-Dimensional Electronic Spectroscopy Reveals Ultrafast Energy Diffusion in Chlorosomes. J. Am. Chem. Soc. 134, 11611–11617 (2012). PubMed

Christensson N., Kauffmann H. F., Pullerits T. & Mančal T. Origin of long lived coherences in light-harvesting complexes. J. Phys. Chem. B 116, 7449 (2012). PubMed PMC

Polyutov S., Kühn O. & Pullerits T. Exciton-vibrational coupling in molecular aggregates: Electronic versus vibronic dimer. Chem. Phys. 394, 21–28 (2012).

Kolli A., O'Reilly E. J., Scholes G. D. & Olaya-Castro A. The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J. Chem. Phys. 137, 174109 (2012). PubMed

Womick J. M. & Moran A. M. Vibronic Enhancement of Exciton Sizes and Energy Transport in Photosynthetic Complexes. J. Phys. Chem. B 115, 1347–1356 (2011). PubMed

Chin A. W. et al. The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment-protein complexes. Nature Physics 9, 113–118 (2013).

Tiwari V., Peters W. K. & Jonas D. M. Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc. Natl. Acad. Sci. U. S. A. 110, 1203–1208 (2013). PubMed PMC

May V. & Kühn O. Charge and Energy Transfer Dynamics in Molecular Systems (Wiley-VCH, Berlin, 2001).

Adolphs J. & Renger T. How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys. J. 91, 2778–2797 (2006). PubMed PMC

Wendling M. et al. 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, 5825–5831 (2000).

Shelly K. R., Carson E. A. & Beck W. F. Vibrational coherence from the dipyridine complex of bacteriochlorophyll a: Intramolecular modes in the 10–220-cm−1 regime, intermolecular solvent modes, and relevance to photosynthesis. J. Am. Chem. Soc. 125, 11810–11811 (2003). PubMed

Parson W. W. Modern optical spectroscopy : with examples from biophysics and biochemistry (Springer, Berlin, 2007).

Demtröder W. Laser Spectroscopy Volume 1: Basic Principles, 4th Edition (Springer, Berlin, 2008).

Demtröder W. Laser Spectroscopy Volume 2: Experimental Techniques, 4th Edition (Springer, Berlin, 2008).

Jonas D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425 (2003). PubMed

Pisliakov A. V., Mančal T. & Fleming G. R. Two-dimensional optical three-pulse photon echo spectroscopy. II. signatures of coherent electronic motion and exciton population transfer in dimer two-dimensional spectra. J. Chem. Phys. 124, 234505 (2006). PubMed

Cho M. Coherent two-dimensional optical spectroscopy. Chem. Rev. 108, 1331 (2008). PubMed

Mukamel S. Principles of nonlinear spectroscopy (Oxford University Press, Oxford, 1995).

Hochstrasser R. M. Two-dimensional ir-spectroscopy: polarization anisotropy effects. Chem. Phys. 266, 273 (2001).

Tronrud D., Wen J., Gay L. & Blankenship R. The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth. Res. 100, 79–87 (2009). PubMed

Philpott M. R. Theory of coupling of electronic and vibrational excitations in molecular crystals and helical polymers. J. Chem. Phys. 55, 2039 (1971).

Fransted K. A., Caram J. R., Hayes D. & Engel G. S. Two-dimensional electronic spectroscopy of bacteriochlorophyll a in solution: Elucidating the coherence dynamics of the Fenna-Matthews-Olson complex using its chromophore as a control. J. Chem. Phys. 137, 125101 (2012). PubMed

Christensson N. et al. High frequency vibrational modulations in two-dimensional electronic spectra and their resemblance to electronic coherence signatures. J. Phys. Chem. B 115, 5383–5391 (2011). PubMed

Turner D. B. et al. Quantitative investigations of quantum coherence for a light-harvesting protein at conditions simulating photosynthesis. Phys. Chem. Chem. Phys. 14, 4857–4874 (2012). PubMed

Butkus V., Zigmantas D., Valkunas L. & Abramavičius D. Vibrational vs. electronic coherences in 2D spectrum of molecular systems. Chem. Phys. Lett. 515, 40–43 (2012).

Mančal T. et al. System-Dependent Signatures of Electronic and Vibrational Coherences in Electronic Two-Dimensional Spectra. J. Phys. Chem. Lett. 3, 1497–1502 (2012). PubMed

Yuen-Zhou J., Krich J. J. & Aspuru-Guzik A. A witness for coherent electronic vs vibronic-only oscillations in ultrafast spectroscopy. J. Chem. Phys. 136, 234501 (2012). PubMed

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

Yuen-Zhou J., Krich J. J., Mohseni M. & Aspuru-Guzik A. Quantum state and process tomography of energy transfer systems via ultrafast spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 108, 17615 (2011). PubMed PMC

Zanni M. T., Ge N., Kim Y. S. & Hochstrasser R. M. Two-dimensional IR spectroscopy can be designed to eliminate the diagonal peaks and expose only the crosspeaks needed for structure determination. Proc. Nat. Am. Soc. 98, 11265–11270 (2001). PubMed PMC

Schlau-Cohen G. S. et al. Elucidation of the timescales and origins of quantum electronic coherence in lhcii. Nature Chemistry 4, 389–395 (2012). PubMed

Rätsep M., Cai Z., Reimers J. R. & Freiberg A. Demonstration and interpretation of significant asymmetry in the low-resolution and high-resolution Qy fluorescence and absorption spectra of bacteriochlorophyll a. J. Chem. Phys. 134, 024506 (2011). PubMed

Zazubovich V., Tibe I. & Small G. J. Bacteriochlorophyll a Franck-Condon factors for the s0 → s1 (Qy) Transition. J. Phys. Chem. B 105, 12410–12417 (2001).

Renge I., Mauring K. & Avarmaa R. Site-selection optical spectra of bacteriochlorophyll and bacteriopheophytin in frozen solutions. J. Lumin. 37, 207–214 (1987).

Diers J. R. & Bocian D. F. Qy-Excitation Resonance Raman Spectra of Bacteriochlorophyll Observed under Fluorescence-Free Conditions. Implications for Cofactor Structure in Photosynthetic Proteins. J. Am. Chem. Soc. 117, 6629–6630 (1995).

Cherepy N. J., Holzwarth A. R. & Mathies R. A. Near-infrared resonance Raman spectra of Chloroflexus aurantiacus photosynthetic reaction centers. Biochemistry 34, 5288–5293 (1995). PubMed

Cherepy N. J., Shreve A. P., Moore L. J., Boxer S. G. & Mathies R. A. Electronic and Nuclear Dynamics of the Accessory Bacteriochlorophylls in Bacterial Photosynthetic Reaction Centers from Resonance Raman Intensities. J. Chem. Phys. B 101, 3250–3260 (1997).

Czarnecki K. et al. Characterization of the strongly coupled, low-frequency vibrational modes of the special pair of photosynthetic reaction centers via isotopic labeling of the cofactors. J. Am. Chem. Soc. 119, 415–426 (1997).

Matsuzaki S., Zazubovich V., Rätsep M., Hayes J. M. & Small G. J. Energy Transfer Kinetics and Low Energy Vibrational Structure of the Three Lowest Energy Qy-States of the Fenna-Matthews-Olson Antenna Complex. J. Chem. Phys. B 104, 9564–9572 (2000).

Rätsep M. & Freiberg A. Electron-phonon and vibronic couplings in the fmo bacteriochlorophyll a antenna complex studied by difference fluorescence line narrowing. J. Lumin. 127, 251–259 (2007).

Hidden vibronic and excitonic structure and vibronic coherence transfer in the bacterial reaction center

The Role of Resonant Vibrations in Electronic Energy Transfer