Exciton Coherence and Energy Transport in the Light-Harvesting Dimers of Allophycocyanin

Abstract

Femtosecond transient grating and photon echo spectroscopies with a sub-20 fs time resolution are applied to allophycocyanin (APC), a protein located at the base of the phycobilisome antenna of cyanobacteria. Coupling between pairs of phycocyanobilin pigments with nondegenerate energy levels gives rise to the four-level exciton electronic structure of APC. Spectroscopic signals obtained in multiple experiments (e.g., linear absorption, fluorescence, transient grating, 2D Fourier transform photon echo) are used to constrain the parameters of a Frenkel exciton Hamiltonian. Comparison between experiment and theory yields a robust microscopic understanding of the electronic and nuclear relaxation dynamics. In agreement with previous work, transient absorption anisotropy establishes that internal conversion between the exciton states of the dimer occurs with time constants of 35, 220, and 280 fs. The sub-100 fs dynamics are decomposed into three distinct relaxation processes: electronic population transfer, intramolecular vibrational energy redistribution, and the dephasing of electronic and nuclear coherences. Model calculations show that the sub-100 fs red-shift in the transient absorption signal spectrum reflects interference between stimulated emission (ESE) and excited state absorption (ESA) signal components. It is also established that the pigment fluctuations in the dimer are not well-correlated, although further experiments will be required to precisely quantify the amount of correlation. The findings of this paper suggest that the light harvesting function of APC is enhanced by nondegeneracy of the pigments comprising the dimer and strong vibronic coupling of intramolecular modes on the phycocyanobilins. We find that the exciton states are 96% localized to the individual molecular sites within a particular dimer. Localization of the transition densities, in turn, is suggested to promote significant vibronic coupling which serves to both broaden the absorption line shape and open channels for fast internal conversion. The dominant internal conversion channel is assigned to a promoting mode near 800 cm(-1) involving hydrogen out-of-plane (HOOP) wagging motion similar to that observed in phytochrome and retinal. This rate enhancement ensures that all photoexcitations quickly and efficiently relax to the electronic origin of the lower energy exciton state from which energy transfer to the reaction center occurs.

Quantum state and process tomography of energy transfer systems via ultrafast spectroscopy

“…The excitonic part of the Hamiltonian, describing the system with the environment frozen in place, is given by (4,8,18):…”

“…excitation energy transfer | nonlinear spectroscopy | quantum information processing | open quantum systems | quantum biology E xcitonic systems and the processes triggered upon their interaction with electromagnetic radiation are of fundamental physical and chemical interest (1)(2)(3)(4)(5)(6). In nonlinear optical spectroscopy (NLOS), a series of ultrafast femtosecond pulses induces coherent vibrational and electronic dynamics in a molecule or nanomaterial, and the nonlinear polarization of the excitonic system is monitored both in the time and frequency domains (7,8).…”

Energy transfer in structured and unstructured environments: Master equations beyond the Born-Markov approximations

“…There is now increasing evidence to suggest that these underdamped modes are an important contributing factor to the long-lived coherences observed in photosynthetic systems, [20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35][36][37][38] as well as links between the quantum mechanical nature of these vibrational modes and enhanced transfer rates. 25,37,39,40 A multitude of powerful computational methods have been developed to deal with the difficulties faced in modelling strongly dissipative quantum systems. Examples include the hierarchical equations of motion (HEOM), [41][42][43][44][45][46] density matrix renormalisation group (and related) techniques, 25,36,47,48 and those based on the path integral formalism.…”

Probing weak dipole-dipole interaction using phase-modulated nonlinear spectroscopy

“…Refs. [11][12][13][14][15][16]). The model of our measurement results effectively in a one-body measurement operator (number of detected photons).…”