Vibronic Enhancement of Exciton Sizes and Energy Transport in Photosynthetic Complexes

Abstract

Transport processes and spectroscopic phenomena in light harvesting proteins depend sensitively on the characteristics of electron-phonon couplings. Decoherence imposed by low-frequency nuclear motion generally suppresses the delocalization of electronic states, whereas the Franck-Condon progressions of high-frequency intramolecular modes underpin a hierarchy of vibronic Coulombic interactions between pigments. This Article investigates the impact of vibronic couplings on the electronic structures and relaxation mechanisms of two cyanobacterial light-harvesting proteins, allophycocyanin (APC) and C-phycocyanin (CPC). Both APC and CPC possess three pairs of pigments (i.e., dimers) that undergo electronic relaxation on the subpicosecond time scale. Electronic relaxation is ~10 times faster in APC than in CPC despite the nearly identical structures of their pigment dimers. We suggest that the distinct behaviors of these closely related proteins are understood on the same footing only in a basis of joint electronic-nuclear states (i.e., vibronic excitons). A vibronic exciton model predicts well-defined rate enhancements in APC at realistic values of the site reorganization energies, whereas a purely electronic exciton model points to faster dynamics in CPC. Calculated exciton sizes (i.e., participation ratios) show that wave function delocalization underlies the rate enhancement predicted by the vibronic exciton model. Strong vibronic coupling and heterogeneity in the pigment sites are the key ingredients of the vibronic delocalization mechanism. In contrast, commonly employed purely electronic exciton models see heterogeneity as only a localizing influence. This work raises the possibility that similar vibronic effects, which are often neglected, may generally have a significant influence on energy transport in molecular aggregates and photosynthetic complexes.

Coherence and population dynamics of chlorophyll excitations in FCP complex: Two-dimensional spectroscopy study

“…Second, vibrations-assisted energy transfer enhancement might be significant for the Chl c-Chl a energy transfer. The energy gap of 715 cm −1 is close to the strongest vibrational Chl a mode of 745 cm −1 , thus allowing for electronic-vibrational resonance [55][56][57] . Recently, specific vibrational modes were suggested to speed up the initial charge transfer step in the photosystem II (PS II) reaction center 16,17 .…”

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

“…[16][17][18][19] In addition to the (often low frequency) continuum, the environmental spectral densities of pigment-protein complexes are generally structured; that is, there are specific underdamped vibrational modes of the environment that couple strongly to the excitonic degrees of freedom. 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.…”

“…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.…”

Ultrafast energy transfer with competing channels: Non-equilibrium Förster and Modified Redfield theories

“…Despite current attention to fine effects of underdamped intramolecular vibrational modes [24][25][26][27][28] and to details of spectral density shapes [29], and despite recent efforts to introduce a paradigm shift in understanding of the origin of the photosynthetic EET efficiency [30][31][32], the overall picture of this process, as drawn by the master equations of the Förster and Redfield types, remains valid [33] (see e. g. [34] for quantitative results). Recent theoretical advances enabling exact numerical solutions of some types of energy transfer problems e.g.…”