Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting

Nature Chemistry

Volumn 4, Issue 5, 2012, Pages 396-404

  Wong, Cathy Y ^a   Alvey, Richard M ^b   Turner, Daniel B ^a   Wilk, Krystyna E ^c   Bryant, Donald A ^b   Curmi, Paul M G ^c   Silbey, Robert J ^d   Scholes, Gregory D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGHT HARVESTING SYSTEM; METHODOLOGY; PHOTOSYNTHESIS; RADIATION EXPOSURE; SPECTROSCOPY;

ENERGY TRANSFER; FLUORESCENCE RESONANCE ENERGY TRANSFER; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYNTHESIS; SPECTRUM ANALYSIS;

EID: 84860248499     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.1302     Document Type: Article

References (60)

1. Scholes, G. D., Fleming, G. R., Olaya-Castro, A. & van Grondelle, R. Lessons from nature about solar light harvesting. Nature Chem. 3, 763-774 (2011).
2. van der Meer, B. W., Coker, G. & Chen, S-Y. S. Resonance Energy Transfer: Theory and Data (VCH, 1994).
3. Förster, T. in Modern Quantum Chemistry: Istanbul Lectures. Part III, Action of Light and Organic Crystals (ed. Sinanoglu, O.) 93-137 (Academic Press, 1965).
4. Beljonne, D., Curutchet, C., Scholes, G. D. & Silbey, R. J. Beyond Forster resonance energy transfer in biological and nanoscale systems. J. Phys. Chem. B 113, 6583-6599 (2009).
5. Fleming, G. R. & Scholes, G. D. Physical chemistry-quantum mechanics for plants. Nature 431, 256-257 (2004).
6. Cheng, Y. C. & Fleming, G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241-262 (2009).
7. van Grondelle, R. & Novoderezhkin, V. I. Energy transfer in photosynthesis: Experimental insights and quantitative models. Phys. Chem. Chem. Phys. 8, 793-807 (2006).
8. Novoderezhkin, V. & van Grondelle, R. Physical origins and models of energy transfer in photosynthetic light-harvesting. Phys. Chem. Chem. Phys. 12, 7352-7365 (2010).
9. Collini, E. et al. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644-649 (2010).
10. Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782-786 (2007). (Pubitemid 46582029)
11. Panitchayangkoon, G. et al. Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc. Natl Acad. Sci. USA 107, 12766-12770 (2010).
12. Collini, E. & Scholes, G. D. Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323, 369-373 (2009).
13. Lee, H., Cheng, Y. C. & Fleming, G. R. Coherence dynamics in photosynthesis: Protein protection of excitonic coherence. Science 316, 1462-1465 (2007). (Pubitemid 46906609)
14. Mercer, I. P. et al. Instantaneous mapping of coherently coupled electronic transitions and energy transfers in a photosynthetic complex using angleresolved coherent optical wave-mixing. Phys. Rev. Lett. 102, 057402 (2009).
15. Calhoun, T. R. et al. Quantum coherence enabled determination of the energy landscape in light-harvesting complex II. J. Phys. Chem. B 113, 16291-16295 (2009).
16. Rebentrost, P., Mohseni, M. & Aspuru-Guzik, A. Role of quantum coherence and environmental fluctuations in chromophoric energy transport. J. Phys. Chem. B 113, 9942-9947 (2009).
17. Fassioli, F. & Olaya-Castro, A. Distribution of entanglement in light-harvesting complexes and their quantum efficiency. New J. Phys. 12, 085006 (2010).
18. Ishizaki, A. & Fleming, G. R. Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc. Natl Acad. Sci. USA 106, 17255-17260 (2009).
19. Caruso, F., Chin, A. W., Datta, A., Huelga, S. F. & Plenio, M. B. Entanglement and entangling power of the dynamics in light-harvesting complexes. Phys. Rev. A 81, 062346 (2010).
20. Hoyer, S., Sarovar, M. & Whaley, K. B. Limits of quantum speedup in photosynthetic light harvesting. New J. Phys. 12, 065041 (2010).
21. Andrews, D. L., Curutchet, C. & Scholes, G. D. Resonance energy transfer: Beyond the limits. Lasers Photon. Rev. 5, 114-123 (2011).
22. Turner, D. B., Wilk, K. E., Curmi, P. M. G. & Scholes, G. D. Comparison of electronic and vibrational coherence measured by two-dimensional electronic spectroscopy. J. Phys. Chem. Lett. 2, 1904-1911 (2011).
23. Cerino, F. & Zingone, A. in Unravelling the Algae: The Past, Present, and Future of Algal Systematics (eds Brodie, J. & Lewis, J.) Ch. 11, 197 (CRC Press, 2007).
24. Wedemayer, G. J., Kidd, D. G. & Glazer, A. N. Cryptomonad biliproteins: Bilin types and locations. Photosynth. Res. 48, 163-170 (1996). (Pubitemid 26367869)
25. Wilk, K. E. et al. Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: Crystal structure of a cryptophyte phycoerythrin at 1.63-ångstrom resolution. Proc. Natl Acad. Sci. USA 96, 8901-8906 (1999). (Pubitemid 29374680)
26. MacColl, R. Cyanobacterial phycobilisomes. J. Struct. Biol. 124, 311-334 (1998). (Pubitemid 29143068)
27. Faust, M. A. & Gantt, E. Effect of light-intensity and glycerol on growth, pigment composition, and ultrastructure of Chroomonas sp. J. Phycol. 9, 489-495 (1973).
28. Frauenfelder, H. & Wolynes, P. G. Rate theories and puzzles of hemeprotein kinetics. Science 229, 337-345 (1985). (Pubitemid 15073081)
29. Jonas, D. M. Two-dimensional femtosecond spectroscopy. Annu. Rev. Phys. Chem. 54, 425-463 (2003).
30. Cho, M. H., Brixner, T., Stiopkin, I., Vaswani, H. & Fleming, G. R. Two dimensional electronic spectroscopy of molecular complexes. J. Chin. Chem. Soc. 53, 15-24 (2006).
31. Abramavicius, D., Palmieri, B., Voronine, D. V., Sanda, F. & Mukamel, S. Coherent multidimensional optical spectroscopy of excitons in molecular aggregates; quasiparticle versus supermolecule perspectives. Chem. Rev. 109, 2350-2408 (2009).
32. Milota, F., Sperling, J., Nemeth, A., Mancal, T. & Kaufmann, H. F. Twodimensional electronic spectroscopy of molecular excitons. Acc. Chem. Res. 42, 1364-1374 (2009).
33. Hochstrasser, R. M. Two-dimensional spectroscopy at infrared and optical frequencies. Proc. Natl Acad. Sci. USA 104, 14190-14196 (2007). (Pubitemid 350003239)
34. Gallagher Fader, S. M. & Jonas, D. M. Two-dimensional electronic correlation and relaxation spectra: Theory and model calculations. J. Phys. Chem. A 1999, 10489-10505 (1999). (Pubitemid 129571337)
35. Novoderezhkin, V. I., Doust, A. B., Curutchet, C., Scholes, G. D. & van Grondelle, R. Excitation dynamics in phycoerythrin 545: Modeling of steadystate spectra and transient absorption with modified Redfield theory. Biophys. J. 99, 344-352 (2010).
36. Roberts, S. T., Loparo, J. J. & Tokmakoff, A. Characterization of spectral diffusion from two-dimensional line shapes. J. Chem. Phys. 125, 084502 (2006).
37. Christensson, N. et al. High frequency vibrational modulations in twodimensional electronic spectra and their resemblance to electronic coherence signatures. J. Phys. Chem. B 115, 5383-5391 (2011).
38. Alvey, R. M., Biswas, A., Schluchter, W. M. & Bryant, D. A. Effects of modified phycobilin biosynthesis in the cyanobacterium Synechococcus sp. strain PCC 7002. J. Bacteriol. 193, 1663-1671 (2011).
39. Duerring, M., Schmidt, G. B. & Huber, R. Isolation, crystalization, crystal structure analysis and refinement of constitutive C-phycocyanin from the chromatically adapting cyanobacterium Fremyella diplosiphon at 1.66 A resolution. J. Mol. Biol. 217, 577-592 (1991). (Pubitemid 121003303)
40. Doust, A. B. et al. Developing a structure-function model for the cryptophyte phycoerythrin 545 using ultrahigh resolution crystallography and ultrafast laser spectroscopy. J. Mol. Biol. 344, 135-153 (2004). (Pubitemid 39422379)
41. Huo, P. & Coker, D. F. Theoretical study of coherent excitation energy transfer in cryptophyte phycocyanin 645 at physiological temperature. J. Phys. Chem. Lett. 2, 825-833 (2011).
42. Hanna, G. & Kapral, R. Nonadiabatic dynamics of condensed phase rate processes. Acc. Chem. Res. 39, 21-27 (2006).
43. Fenimore, P. W., Frauenfelder, H., McMahon, B. H. & Parak, F. G. Slaving: Solvent fluctuations dominate protein dynamics and functions. Proc. Natl Acad. Sci. USA 99, 16047-16051 (2002). (Pubitemid 35462746)
44. Sergi, A., Mac Kernan, D., Ciccotti, G. & Kapral, R. Simulating quantum dynamics in classical environments. Theor. Chem. Acc. 110, 49-58 (2003). (Pubitemid 37229639)
45. Nandi, N., Bhattacharyya, K. & Bagchi, B. Dielectric relaxation and solvation dynamics of water in complex chemical and biological systems. Chem. Rev. 100, 2013-2045 (2000).
46. Olbrich, C., Strümpfer, J., Schulten, K. & Kleinekathöfer, U. Quest for spatially correlated fluctuations in the FMO light-harvesting complex. J. Phys. Chem. B 115, 758-764 (2011).
47. Peng, J., Castonguay, T. C., Coker, D. F. & Ziegler, L. D. Ultrafast H2 and D2 rotational Raman responses in near critical CO2: An experimental and theoretical study of anisotropic solvation dynamics. J. Chem. Phys. 131, 054501 (2009).
48. Warshel, A. & Parson, W. W. Computer simulations of electron-transfer reactions in solution and in photosynthetic reaction centers. Annu. Rev. Phys. Chem. 42, 279-309 (1991).
49. Scholes, G. D. & Rumbles, G. Excitons in nanoscale systems. Nature Mater. 5, 683-696 (2006). (Pubitemid 44320320)
50. Simpson, W. T. & Peterson, D. L. Coupling strength for resonance force transfer of electronic energy in van der Waals solids. J. Chem. Phys. 26, 588-593 (1957).
51. Craig, D. P. & Walmsley, S. H. Excitons in Molecular Crystals (Benjamin, 1968).
52. Jang, S., Cheng, Y-C., Reichman, D. R. & Eaves, J. D. Theory of coherent resonance energy transfer. J. Chem. Phys. 129, 101104 (2008).
53. Cheng, Y-C. & Silbey, R. J. Coherence in the B800 ring of purple bacteria LH2. Phys. Rev. Lett. 96, 028103 (2006).
54. Khalil, M., Demirdoven, N. & Tokmakoff, A. Obtaining absorptive line shapes in two-dimensional infrared vibrational correlation spectra. Phys. Rev. Lett. 90, 047401 (2003).
55. Knapp, E. W. Lineshapes of molecular aggregates. Exchange narrowing and intersite correlation. Chem. Phys. 85, 73-82 (1984).
56. Heijs, D. J., Malyshev, V. A. & Knoester, J. Decoherence of excitons in multichromophore systems: Thermal line broadening and destruction of superradiant emission. Phys Rev. Lett. 95, 177402 (2005).
57. Xiao, L. & Coker, D. F. The influence of nonadiabatic rotational transitions on the line shapes of the rotational Raman sepctrum of H2 in liquid argon. J. Chem. Phys. 100, 8646-8655 (1994).
58. Miller, W. H. Quantum dynamics of complex molecular systems. Proc. Natl Acad. Sci. USA 102, 6660-6664 (2005). (Pubitemid 40675373)
59. Onuchic, J. N. & Wolynes, P. G. Classical and quantum pictures of reaction dynamics in condensed matter: Resonances, dephasing, and all that. J. Phys. Chem. 92, 6495-6503 (1988).
60. Onuchic, J. N., Beratan, D. N. & Hopfield, J. J. Some aspects of electron-transfer reaction dynamics. J. Phys. Chem. 90, 3707-3721 (1986).