Local protein solvation drives direct down-conversion in phycobiliprotein PC645 via incoherent vibronic transport

Abstract

SignificanceTo harness sunlight for growth, plants and algae rapidly convey absorbed excitation energy from antennae pigments to a reaction center, where the excitations convert to chemical energy. In deep water environments, cryptophyte algae survive by using the molecular motion of phycobiliprotein antennae to funnel excitations to low-energy pigments. The mechanism of down-conversion in phycobiliproteins remains controversial: Could specific vibrations resonant with pigment energy gaps support coherence between excited states and thereby enhance the rate of transport by transient delocalization? Here, we demonstrate that down-conversion in a specific phycobiliprotein, PC645, is both incoherent and enhanced by a broad range of high-frequency vibrations. We suggest that a similar incoherent mechanism is appropriate across phycobiliproteins.

Dissipation-Assisted Matrix Product Factorization

“…It is notable that numerically exact simulations with N ≥ 10 sites and Q ≥ 100 local modes and moderate Huang-Rhys factors are possible with DAMPF, which brings the actual dynamics of interesting natural molecular aggregates [1,3,54,55] within the realm of exact simulations. This will facilitate the investigation of the role of highly structured vibrational environments of photosynthetic complexes [10,11,[56][57][58][59][60][61][62], which have been severely coarse-grained in previous theoretical studies due to the limited computational power [63]. In addition, DAMPF can be used to compute spectroscopic quantities, such as absorption spectra (see SM), suggesting the possibility to study the connection between spectroscopic observations and underlying energy transfer dynamics, therefore assisting in the identification of physical mechanisms that may lead to diverse observations [63][64][65][66][67][68][69].…”

“…This will facilitate the investigation of the role of highly structured vibrational environments of photosynthetic complexes [10,11,[56][57][58][59][60][61][62], which have been severely coarse-grained in previous theoretical studies due to the limited computational power [63]. In addition, DAMPF can be used to compute spectroscopic quantities, such as absorption spectra (see SM), suggesting the possibility to study the connection between spectroscopic observations and underlying energy transfer dynamics, therefore assisting in the identification of physical mechanisms that may lead to diverse observations [63][64][65][66][67][68][69]. Finally, the non-equilibrium dynamics of underdamped modes can also be monitored, making our approach very suitable for the study of the role of strongly coupled vibrational modes in organic photovoltaics where coherent vibronic coupling has been suggested to promote charge separation [8,9].…”

Electronic energy transfer in biomacromolecules

“…The real equilibrium populations, however, will reflect the mixing with nuclear degrees of freedom, which effectively renormalizes the eigenstates of the full Hamiltonian . Förster and GF theory describe qualitatively well the EET rates even when the electronic couplings are not very small, and predict qualitatively correct populations at equilibrium …”

“…39 The exact exciton dynamics of an exciton system can be described through a series of hierarchically coupled equations of motion (HEOM). The HEOM approach was derived in a reduced form by Ishizaki and Fleming, 132 and is now widely used to consistently describe all ranges of exciton-phonon couplings 121,[135][136][137] and to benchmark the simpler theories. 132,138 From the comparison with HEOM dynamics, it was shown that Redfield-based theories easily give qualitatively incorrect dynamics outside of their range of applicability.…”

“…136,140 Förster and GF theory describe qualitatively well the EET rates even when the electronic couplings are not very small, and predict qualitatively correct populations at equilibrium. 121,132,138,141 To overcome the limitations of the HEOM due to numerical complexity, several implementations have been devised, including massively parallel implementations, 137,141 or stochastic approaches. 142 However, other limitations remain, on the functional form of the SD, and on the number of vibrational modes that can be modeled.…”