New Insights on Persistent Nonphotochemical Hole Burning and Its Application to Photosynthetic Complexes

Abstract

Nonphotochemical hole burning (NPHB) at low temperatures of the electronic absorption bands of molecular chromophores imbedded in amorphous solids (glasses and polymers) and in proteins is a striking manifestation of configurational tunneling triggered by electronic excitation. The current mechanism of NPHB has it due to a hierarchy of relaxation events that begin in the outer shell and involve the intrinsic two-level systems (TLS int ) of the glass and terminate in the inner shell where the rate determining step involving the extrinsic TLS (TLS ext ) occurs. The TLS correspond to asymmetric intermolecular double well potentials. The TLS ext are associated with the chromophore and the inner shell of solvent molecules. The TLS int are intimately associated with the excess free volume of glasses. Their tunneling leads to diffusion of excess free volume. Results for Al-phthalocyanine tetrasulfonate (APT) in hyperquenched glassy water (HGW) and ethanol (HGE) films that provide strong support for the critical role of excess free volume are discussed. Hole spectra of APT/HGW obtained over eight decades of burn fluence reveal that the current mechanism needs to be modified to include multilevel extrinsic systems (MLS ext ) in order to explain why the antihole ("photoproduct" absorption) lies to the blue of the burn frequency for sufficiently high burn fluences, an intriguing up-conversion process. The spectra also reveal, for the first time, that the zero-phonon hole (ZPH) profile is non-Lorentzian. This is shown to be a natural consequence of the interplay between the three distributions that result in dispersive hole growth kinetics. They are associated with the tunnel parameter λ of the TLS ext , the angle R between the laser polarization and transition dipole, and off-resonant absorption of the zero-phonon line (the ω distribution). Theoretical simulations of hole growth data for APT/HGW obtained over six decades of burn fluence show that the λ distribution is of primary importance, describing well the first 80% of the saturated burn. The paper ends with an application of NPHB combined with high pressure and external electric (Stark) fields to the critically important "red" antenna states of photosystem I. The addition of pressure and Stark fields enhances the already impressive selectivity of NPHB. The results show that the linear pressure shift, permanent dipole moment change, and linear electron-phonon coupling are correlated. Of particular importance is that these properties can be used to identify states which involve interacting chlorophyll molecules that possess significant charge transfer character because of electron-exchange coupling. The results also show that the site distribution functions of the antenna states are largely uncorrelated, consistent with the findings for previously studied complexes. This is important because the absence of correlation means that the electronic energy gaps of donor and acceptor states are distributed which, in turn, means that the kinetics can be dispersive under certain ...

Parameters of the Protein Energy Landscapes of Several Light-Harvesting Complexes Probed via Spectral Hole Growth Kinetics Measurements

“…According to 13,34,35,38 , in the absence of the energy transfer (this is the case for this manuscript focusing on the lowest-energy states of the complexes) the time dependence of the absorption spectrum affected by SHB can be described with…”

“…SHB has been applied to explore electronic level structure, electron-phonon coupling and energy and charge transfer processes in a broad variety of complexes [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] , as summarized in a recent review 21 . In terms of low-temperature protein dynamics, the presence of low-energy excitations responsible for the ~T 1.3 dependence of the homogeneous line width, which is characteristic for amorphous solids, was demonstrated for many PS complexes [3][4][5][6][7][8][9][10]12 .…”

“…Both SHB and single molecule spectroscopy have been applied in the research on low-temperature dynamics and energy barrier distributions of glasses and polymers [31][32][33][34][35][36][37] . In particular, hole growth kinetics (HGK) measurements have been employed in 13,[34][35][36][37] . However, until recently the simulations of the hole burning in PS complexes (e.g.…”

Fluorescence hole-burning and site-selective studies of LHCII

“…Photosynthetic pigment-protein complexes, including light-harvesting complex II (LHCII), were successfully studied with the use of absorption hole-burning (AHB; Reinot et al 2001, Ihalainen et al 2003. This wellestablished technique is based on the measurement of the absorption spectra before and after intense illumination of the sample with a spectrally narrow light beam at low temperatures.…”

Introduction to optical methods in photosynthesis

“…This broadening is caused by differences in the local environment leading to a distribution of transition (site) energies. Spectral holeburning (see e.g., Reinot et al 2001) is a technique for resolving the homogeneous absorption lines hidden underneath the inhomogeneously broadened absorption band. The sample is illuminated with a narrow-band laser at very low temperature (\4 K).…”