Enhancement of Vibronic and Ground-State Vibrational Coherences in 2D Spectra of Photosynthetic Complexes
10.1038/srep02029
Crossref journal-article
Springer Science and Business Media LLC
Scientific Reports (297)
Abstract

AbstractA 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.

Bibliography

Chenu, A., Christensson, N., Kauffmann, H. F., & Mančal, T. (2013). Enhancement of Vibronic and Ground-State Vibrational Coherences in 2D Spectra of Photosynthetic Complexes. Scientific Reports, 3(1).

Authors 4
  1. Aurélia Chenu (first)
  2. Niklas Christensson (additional)
  3. Harald F. Kauffmann (additional)
  4. Tomáš Mančal (additional)
References 63 Referenced 155
  1. Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782 (2007). (10.1038/nature05678) / Nature by GS Engel (2007)
  2. 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). (10.1021/jp025758e) / J. Phys. Chem. B by VI Prokhorenko (2002)
  3. 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). / J. Chem. Phys. by S Savikhin (1997)
  4. Lee, H., Cheng, Y.-C. & Fleming, G. Coherence dynamics in photosynthesis: Protein protection of excitonic coherence. Science 316, 1462–1465 (2007). (10.1126/science.1142188) / Science by H Lee (2007)
  5. 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). (10.1063/1.3690498) / J. Chem. Phys. by JR Caram (2012)
  6. Kreisbeck, C. & Kramer, T. Long-lived electronic coherence in dissipative exciton dynamics of light-harvesting complexes. J. Phys. Chem. Lett. 3, 2828 (2012). (10.1021/jz3012029) / J. Phys. Chem. Lett. by C Kreisbeck (2012)
  7. Rebentrost, P., Mohseni, M., Kassal, I., Lloyd, S. & Aspuru-Guzik, A. Environment-assisted quantum transport. New J. Phys. 11, 033003 (2009). (10.1088/1367-2630/11/3/033003) / New J. Phys. by P Rebentrost (2009)
  8. Ishizaki, A. & Fleming, G. R. Quantum superpositions in photosynthetic light harvesting: delocalization and entanglement. New J. Phys. 12, 055004 (2010). (10.1088/1367-2630/12/5/055004) / New J. Phys. by A Ishizaki (2010)
  9. Hayes, D. et al. Dynamics of electronic dephasing in the Fenna-Matthews-Olson complex. New J. Phys. 12, 065042 (2010). (10.1088/1367-2630/12/6/065042) / New J. Phys. by D Hayes (2010)
  10. Abramavicius, D. & Mukamel, S. Exciton dynamics in chromophore aggregates with correlated environment fluctuations. J. Chem. Phys. 134, 174504 (2011). (10.1063/1.3579455) / J. Chem. Phys. by D Abramavicius (2011)
  11. 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). (10.1063/1.3703504) / J. Chem. Phys. by F Caycedo-Soler (2012)
  12. 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). (10.1021/jp2088109) / J. Phys. Chem. A by AF Fidler (2012)
  13. 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). (10.1021/jp202619a) / J. Phys. Chem. B by C Olbrich (2011)
  14. 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). (10.1016/j.bpj.2011.12.021) / Biophys. J. by S Shim (2012)
  15. 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). (10.1088/1367-2630/12/10/105012) / New J. Phys. by J Wu (2010)
  16. 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). (10.1021/jp050788d) / J. Phys. Chem. B by MH Cho (2005)
  17. Blankenship, R. E. Molecular Mechanism of Photosynthesis (Blackwell Science, Oxford, 2002). (10.1002/9780470758472)
  18. Cheng, Y.-C. & Fleming, G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241 (2009). (10.1146/annurev.physchem.040808.090259) / Annu. Rev. Phys. Chem. by Y-C Cheng (2009)
  19. 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). (10.1063/1.460467) / J. Chem. Phys. by X-P Jiang (1991)
  20. Mančal, T. & Valkunas, L. Exciton dynamics in photosynthetic complexes: excitation by coherent and incoherent light. New J. Phys. 12, 065044 (2010). (10.1088/1367-2630/12/6/065044) / New J. Phys. by T Mančal (2010)
  21. Brumer, P. & Shapiro, M. Molecular response in one photon absorption: Coherent pulsed laser vs. thermal incoherent source. ArXiv 1109.0026v2 (2011).
  22. 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). / Procedia Chemistry by K Hoki (2011)
  23. Pachón, L. A. & Brumer, P. Incoherent excitation of thermally equilibrated open quantum systems. ArXiv 1210.6374v1 (2012).
  24. Dostál, J. et al. Two-Dimensional Electronic Spectroscopy Reveals Ultrafast Energy Diffusion in Chlorosomes. J. Am. Chem. Soc. 134, 11611–11617 (2012). (10.1021/ja3025627) / J. Am. Chem. Soc. by J Dostál (2012)
  25. 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). (10.1021/jp304649c) / J. Phys. Chem. B by N Christensson (2012)
  26. Polyutov, S., Kühn, O. & Pullerits, T. Exciton-vibrational coupling in molecular aggregates: Electronic versus vibronic dimer. Chem. Phys. 394, 21–28 (2012). (10.1016/j.chemphys.2011.12.006) / Chem. Phys. by S Polyutov (2012)
  27. 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). (10.1063/1.4764100) / J. Chem. Phys. by A Kolli (2012)
  28. 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). (10.1021/jp106713q) / J. Phys. Chem. B by JM Womick (2011)
  29. 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). (10.1038/nphys2515) / Nature Physics by AW Chin (2013)
  30. 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). (10.1073/pnas.1211157110) / Proc. Natl. Acad. Sci. U. S. A. by V Tiwari (2013)
  31. May, V. & Kühn, O. Charge and Energy Transfer Dynamics in Molecular Systems (Wiley-VCH, Berlin, 2001).
  32. Adolphs, J. & Renger, T. How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys. J. 91, 2778–2797 (2006). (10.1529/biophysj.105.079483) / Biophys. J. by J Adolphs (2006)
  33. 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). (10.1021/jp000077+) / J. Phys. Chem. B by M Wendling (2000)
  34. 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). (10.1021/ja0366890) / J. Am. Chem. Soc. by KR Shelly (2003)
  35. Parson, W. W. Modern optical spectroscopy : with examples from biophysics and biochemistry (Springer, Berlin, 2007). (10.1007/978-3-540-37542-5) / Modern Optical Spectroscopy by William W. Parson (2007)
  36. Demtröder, W. Laser Spectroscopy Volume 1: Basic Principles, 4th Edition (Springer, Berlin, 2008).
  37. Demtröder, W. Laser Spectroscopy Volume 2: Experimental Techniques, 4th Edition (Springer, Berlin, 2008).
  38. Jonas, D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425 (2003). (10.1146/annurev.physchem.54.011002.103907) / Annu. Rev. Phys. Chem. by DM Jonas (2003)
  39. 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). (10.1063/1.2200705) / J. Chem. Phys. by AV Pisliakov (2006)
  40. Cho, M. Coherent two-dimensional optical spectroscopy. Chem. Rev. 108, 1331 (2008). (10.1021/cr078377b) / Chem. Rev. by M Cho (2008)
  41. Mukamel, S. Principles of nonlinear spectroscopy (Oxford University Press, Oxford, 1995).
  42. Hochstrasser, R. M. Two-dimensional ir-spectroscopy: polarization anisotropy effects. Chem. Phys. 266, 273 (2001). (10.1016/S0301-0104(01)00232-4) / Chem. Phys. by RM Hochstrasser (2001)
  43. 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). (10.1007/s11120-009-9430-6) / Photosynth. Res. by D Tronrud (2009)
  44. Philpott, M. R. Theory of coupling of electronic and vibrational excitations in molecular crystals and helical polymers. J. Chem. Phys. 55, 2039 (1971). (10.1063/1.1676371) / J. Chem. Phys. by MR Philpott (1971)
  45. 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). (10.1063/1.4752107) / J. Chem. Phys. by KA Fransted (2012)
  46. 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). (10.1021/jp109442b) / J. Phys. Chem. B by N Christensson (2011)
  47. 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). (10.1039/c2cp23670b) / Phys. Chem. Chem. Phys. by DB Turner (2012)
  48. 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). (10.1016/j.cplett.2012.07.014) / Chem. Phys. Lett. by V Butkus (2012)
  49. 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). (10.1021/jz300362k) / J. Phys. Chem. Lett. by T Mančal (2012)
  50. 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). (10.1063/1.4725498) / J. Chem. Phys. by J Yuen-Zhou (2012)
  51. 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). (10.1021/ja3065478) / J. Am. Chem. Soc. by S Westenhoff (2012)
  52. 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). (10.1073/pnas.1110642108) / Proc. Natl. Acad. Sci. U. S. A. by J Yuen-Zhou (2011)
  53. 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). (10.1073/pnas.201412998) / Proc. Nat. Am. Soc. by MT Zanni (2001)
  54. Schlau-Cohen, G. S. et al. Elucidation of the timescales and origins of quantum electronic coherence in lhcii. Nature Chemistry 4, 389–395 (2012). (10.1038/nchem.1303) / Nature Chemistry by GS Schlau-Cohen (2012)
  55. 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). (10.1063/1.3518685) / J. Chem. Phys. by M Rätsep (2011)
  56. 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). (10.1021/jp012804m) / J. Phys. Chem. B by V Zazubovich (2001)
  57. Renge, I., Mauring, K. & Avarmaa, R. Site-selection optical spectra of bacteriochlorophyll and bacteriopheophytin in frozen solutions. J. Lumin. 37, 207–214 (1987). (10.1016/0022-2313(87)90161-X) / J. Lumin. by I Renge (1987)
  58. 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). (10.1021/ja00129a042) / J. Am. Chem. Soc. by JR Diers (1995)
  59. 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). (10.1021/bi00015a044) / Biochemistry by NJ Cherepy (1995)
  60. 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). (10.1021/jp963051k) / J. Chem. Phys. B by NJ Cherepy (1997)
  61. 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). (10.1021/ja963281c) / J. Am. Chem. Soc. by K Czarnecki (1997)
  62. 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). (10.1021/jp0018495) / J. Chem. Phys. B by S Matsuzaki (2000)
  63. 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). (10.1016/j.jlumin.2007.02.053) / J. Lumin. by M Rätsep (2007)
Dates
Type When
Created 12 years, 2 months ago (June 19, 2013, 5:05 a.m.)
Deposited 2 years, 7 months ago (Jan. 6, 2023, 12:26 a.m.)
Indexed 1 month, 3 weeks ago (July 11, 2025, 6:17 a.m.)
Issued 12 years, 2 months ago (June 19, 2013)
Published 12 years, 2 months ago (June 19, 2013)
Published Online 12 years, 2 months ago (June 19, 2013)
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@article{Chenu_2013, title={Enhancement of Vibronic and Ground-State Vibrational Coherences in 2D Spectra of Photosynthetic Complexes}, volume={3}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/srep02029}, DOI={10.1038/srep02029}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Chenu, Aurélia and Christensson, Niklas and Kauffmann, Harald F. and Mančal, Tomáš}, year={2013}, month=jun }