Non-Uniform Excited State Electronic-Vibrational Coupling of Pigment–Protein Complexes

J. Phys. Chem. Lett. 2020, 11, 24, 10388–10395

Photosynthetic organisms exploit interacting quantum degrees of freedom, namely intrapigment electron-vibrational (vibronic) and interpigment dipolar couplings (J-coupling), to rapidly and efficiently convert light into chemical energy. These interactions result in wave function configurations that delocalize excitation between pigments and pigment vibrations. Our study uses multidimensional spectroscopy to compare two model photosynthetic proteins, the Fenna–Matthews Olson (FMO) complex and light harvesting 2 (LH2), and confirm that long-lived excited state coherences originate from the vibrational modes of the pigment. Within this framework, the J-coupling of vibronic pigments should have a cascading effect in modifying the structured spectral density of excitonic states. We show that FMO effectively couples all of its excitations to a uniform set of vibrations while in LH2, its two chromophore rings each couple to a unique vibrational environment. We simulate energy transfer in a simple model system with non-uniform vibrational coupling to demonstrate how modification of the vibronic coupling strength can modulate energy transfer. Because increasing vibronic coupling increases internal relaxation, strongly coupled vibronic states can act as an energy funnel, which can potentially benefit energy transport.

Pubs on arXiv

Articles submitted but not yet accepted for publication can be found on the arXiv.


49. S. Irgen-Gioro, K. Gururangan, A. Spencer, E. Harel, 'Non-Uniform Excited State Electronic-Vibrational Coupling of Pigment–Protein Complexes', J. Phys. Chem. Lett. 11, 24, 10388-10395 Read Here

48. S. Irgen-Gioro, P. Roy, S. Padgaonkar, E. Harel, 'Non-Resonant 2 Color 2-Dimensional Electronic Spectroscopy Reveals Ground State Coherences of Light Harvesting Complex II', The 22nd International Conference on Ultrafast Phenomena 2020. Read Here

47. X. Li, Y. Fu, L. Pedesseau, P. Guo, S. Cuthriell, I. Hadar, J. Even, C. Katan, C.C. Stoumpos, R.D. Schaller, E. Harel, M.G. Kanatzidis, 'Negative Pressure Engineering with Large Cage Cations in 2D Halide Perovskites Causes Lattice Softening', J. Am. Chem. Soc. 142, 11486-11496 (2020). Read Here

46. X. Jiang, S. Jun, J, Hoffman, M.G. Kanatzidis, E. Harel, 'Global Analysis for Time and Spectrally Resolved Multidimensional Microscopy: Application to CH3NH3PbI3 Perovskite Thin Films', J. Phys. Chem. A, 124, 4837-4847 (2020). Read Here

45. Y. Fu, X. Jiang, X. Li, B. Traore, I. Spanopoulos, C. Katan, J. Even, M.G. Kanatzidis, E. Harel, 'Cation Engineering in Two-Dimensional Ruddlesden–Popper Lead Iodide Perovskites with Mixed Large A-Site Cations in the Cages', J. Am. Chem. Soc. 142, 4008-4021 (2020). Read Here

44. S. Irgen-Gioro, P. Roy, S. Padgaonkar, E. Harel, 'Low Energy Excited State Vibrations Revealed in Conjugated Copolymer PCDTBT', J. Chem. Phys. 152, 044201 (2020). Read Here

43. X. Jiang, J. Hoffman, C. C. Stoumpos, M. G. Kanatzidis, E. Harel, ‘Transient Sub-Band-Gap States at Grain Boundaries of CH3NH3PbI3 Perovskite Act as Fast Temperature Relaxation Centers’, ACS Energy Lett. 2019, 4, 7, 1741-1747 (2019). Read Here

42. K. Gururangan, E. Harel, ‘Coherent and Dissipative Quantum Process Tensor Reconstruction in Two-Dimensional Electronic Spectroscopy’, J. Chem. Phys. 150, 164127 (2019). Read Here

41. A. P. Spencer, E. Harel, ‘Four-Dimensional Spectroscopy of Complex Molecular Systems in Solution’, J. Phys. Chem. C., 123, 6303 (2019) (cover article), Read Here

40. S. Irgen-Gioro, A. P. Spencer, W. O. Hutson, E. Harel, ‘Coherences of Bacteriochlorophyll a Uncovered Using 3D-Electronic Spectroscopy’, J. Phys. Chem. Lett., 9, 6077-6081 (2018). Read Here

39. E. Harel, ‘Zooming in on Vibronic Structure by Lowest-Value Projection Reconstruction 4D Coherent Spectroscopy’, J. Chem. Phys. 148, 194201 (2018). Read Here

38. A.P. Spencer, W.O. Hutson, S. Irgen-Gioro, E. Harel, ‘Exciton-Phonon Spectroscopy of Quantum Dots Below the Single-Particle Homogeneous Linewidth’, J. Phys. Chem. Lett. 9, 1503-1508 (2018) Read Here

37. W.O. Hutson, A.P. Spencer, E. Harel, ‘Ultrafast Four-Dimensional Coherent Spectroscopy by Projection Reconstruction, J. Phys. Chem. Lett. 9, 1034 – 1040 (2018) Read Here

36. S. Nah, B. M. Spokoyny, X. Jiang, C. M. M. Soe, C. C. Stoumpos, M. G. Kanatzidis, E. Harel, Transient Sub-bandgap States in Halide Perovskite Thin Films, Nano Lett., 18, 827-831 (2018) Read Here

35. S. Nah, B. M. Spokoyny, C. M. M. Soe, C. C. Stoumpos, M. G. Kanatzidis, E. Harel, Ultrafast Imaging of Carrier Cooling in Metal Halide Perovskite Thin Films, Nano Lett., 18, 1044-1048 (2018) Read Here

34. E. Harel, A. Spencer, B. Spokoyny, Compressive Sensing for Single-Shot Two-Dimensional Coherent Spectroscopy. Proc. SPIE, 10117 (2017)

33. E. Harel, Four-dimensional Coherent Electronic Raman Spectroscopy, J. Chem. Phys., 146, 154201 (2017) Read Here

32. S. Nah, B. Spokoyny, C. Stoumpos, C. M. M. Soe, M. Kanatzidis, and E. Harel, Spatially segregated free-carrier and exciton populations in individual lead halide perovskite grains, Nat. Photonics., 11, 285-289 (2017). Read Here

31. A.P. Spencer, W.O. Hutson, and E. Harel, Quantum coherence selective 2D Raman-2D electronic spectroscopy, Nat. Commun., 8, 14732 (2017). Read Here (highlighted as a Perspective in Science).

30. W.O. Hutson, A.P. Spencer, and E. Harel, Isolated Ground-State Coherence Measured by Fifth-Order Single-Shot Two-Dimensional Electronic Spectroscopy, J. Phys. Chem. Lett., 7, 3636-3640 (2016). Read Here

29. A.P. Spencer, B. Spokoyny, S. Ray, F. Sarvari, and E. Harel, Mapping Multidimensional electronic structure and ultrafast dynamics with single-element detection and compressive sensing, Nat. Commun., 7, 10434 (2016). Read Here

28. B. Spokoyny, C. J. Koh, and E. Harel, Stable and high-power few cycle supercontinuum for 2D ultrabroadband electronic spectroscopy, Opt. Lett., 40 (6), 1014-1017 (2015). Read Here

27. A. P. Spencer, B. Spokoyny, and E. Harel, Enhanced-Resolution Single-Shot 2DFT Spectroscopy by Spatial Spectral Interferometry, J. Phys. Chem. Lett., 6, 945-950 (2015). Read Here

26. B. Spokoyny, and E. Harel, Mapping the Vibronic Structure of a Molecule by Few-cycle Continuum Two-Dimensional Spectroscopy in a Single Pulse,J. Phys. Chem. Lett., 5, 2808–2814 (2014). Read Here

25. E. Harel, Long Range Excitonic Transpot in a Biomimetic System Inspired by the Bacterial Light-harvesting Apparatus, J. Chem. Phys. 136, 174104-1 (2012) Read Here

Prior Publications

24. N. Ben-Eliezer, E. Solomon, E. Harel, N. Nevo, L. Frydman, Fully Refocused Multi-shot Spatiotemporally Encoded MRI: Robust Imaging in the Presence of Metallic Implants, MAGMA 25, 433-442 (2012) Read Here

23. E. Harel, S.M. Rupich, R.D. Schaller, D.V. Talapin, G.S. Engel, Measurement of Electronic Splitting in PbS Quantum Dots by Two-dimensional Nonlinear Spectroscopy, Phys Rev B 86, 075412 (2012) Read Here

22. E. Harel, G.S. Engel, Quantum Coherence Spectroscopy Reveals Complex Dynamics in Bacterial Light Harvesting Complex 2 (LH2), P Natl Acad Sci USA 109, 706-711(2012) Read Here

21. A. F. Fidler, E. Harel, P. D. Long, G. S. Engel, Two-Dimensional Spectroscopy Can Distinguish Between Decoherence and Dephasing of Zero-Quantum Coherences, J Phys Chem A 116, 282-289 (2011) Read Here

20. E. Harel, P. D. Long, G. S. Engel, Single-shot ultrabroadband two-dimensional electronic spectroscopy of the light-harvesting complex LH2. Opt Lett 36, 1665 (2011) Read Here

19. E. Harel, A. F. Fidler, G. S. Engel, Single-Shot Gradient-Assisted Photon Echo Electronic Spectroscopy. J Phys Chem A115, 3787 ( 2011) Read Here

18. G. Panitchayangkoon, D. Hayes, K. A. Fransted, J. R. Caram, E. Harel, J. Z. Wen, . . . G. S. Engel, Long-lived quantum coherence in photosynthetic complexes at physiological temperature. P Natl Acad Sci USA 107, 12766 (2010).Read Here

17. E. Harel, A. F. Fidler, G. S. Engel, Real-time mapping of electronic structure with single-shot two-dimensional electronic spectroscopy. P Natl Acad Sci USA 107, 16444 (2010) Read Here

16. E. Harel, Lab-on-a-chip detection by magnetic resonance methods. Prog Nucl Mag Res Sp 57, 293 (2010) Read Here

15. A. F. Fidler, E. Harel, G. S. Engel, Dissecting Hidden Couplings Using Fifth-Order Three-Dimensional Electronic Spectroscopy. J Phys Chem Lett 1, 2876 (2010) Read Here

14. V. S. Bajaj, J. Paulsen, E. Harel, A. Pines, Zooming In on Microscopic Flow by Remotely Detected MRI. Science 330, 1078 (2010). Read Here

13. E. Harel, Magnetic resonance detection: spectroscopy and imaging of lab-on-a-chip. Lab Chip 9, 17 (2009). Read Here

12. S. J. Xu, E. Harel, D. J. Michalak, C. W. Crawford, D. Budker, A. Pines, Flow in Porous Metallic Materials: A Magnetic Resonance Imaging Study. J Magn Reson Imaging 28, 1299 (2008). Read Here

11. E. Harel, L. Schroder, S. J. Xu, Novel Detection Schemes of Nuclear Magnetic Resonance and Magnetic Resonance Imaging: Applications from Analytical Chemistry to Molecular Sensors. Annu Rev Anal Chem 1, 133 (2008).Read Here

10. E. Harel, A. Pines, Spectrally resolved flow imaging of fluids inside a microfluidic chip with ultrahigh time resolution. J Magn Reson 193, 199 (2008) COVER. Read Here

9. V. V. Telkki, C. Hilty, S. Garcia, E. Harel, A. Pines, Quantifying the diffusion of a fluid through membranes by double phase encoded remote detection magnetic resonance imaging. J Phys Chem B 111, 13929 (2007) COVER. Read Here

8. E. Harel, C. Hilty, K. Koen, E. E. McDonnell, A. Pines, Time-of-flight flow imaging of two-component flow inside a microfluidic chip. Phys Rev Lett 98, (2007). Read Here

7. J. Granwehr, E. Harel, C. Hilty, S. Garcia, L. Chavez, A. Pines, . . . Y. Q. Song, Dispersion measurements using time-of-flight remote detection MRI. Magn Reson Imaging 25, 449 (2007). Read Here

6. E. Harel, J. Granwehr, J. A. Seeley, A. Pines, Multiphase imaging of gas flow in a nanoporous material using remote-detection NMR. Nat Mater 5, 321 (2006). Read Here

5. E. Harel, H. Cho, A general numerical analysis of time-domain NQR experiments. J Magn Reson 183, 308 (Dec, 2006). Read Here

4. V. G. Stavros, E. Harel, S. R. Leone, The influence of intense control laser pulses on homodyne-detected rotational wave packet dynamics in O-2 by degenerate four-wave mixing. J Chem Phys 122, (2005). Read Here

3. E. Harel, S. E. Meltzer, A. A. G. Requicha, M. E. Thompson, B. E. Koel, Fabrication of polystyrene latex nanostructures by nanomanipulation and thermal processing. Nano Lett 5, 2624 (2005). Read Here

2. J. Granwehr, E. Harel, S. Han, S. Garcia, A. Pines, P. N. Sen, Y. Q. Song, Time-of-flight flow imaging using NMR remote detection. Phys Rev Lett 95, (2005). Read Here

1. S. A. Maier, P. G. Kik, H. A. Atwater, S. Meltzer, E. Harel, B. E. Koel, A. A. G. Requicha, Local detection of electromagnetic energy transport below the diffraction limit in metal nanoparticle plasmon waveguides. Nat Mater 2, 229 (2003) COVER. Read Here