Protein Configuration Landscape Fluctuations Revealed by Exciton Transition Polarizations in Single Light Harvesting Complexes

Abstract

Protein is a flexible material with broad distribution of conformations forming an energy landscape of quasi-stationary states. Disentangling the system dynamics along this landscape is the key for understanding the functioning of the protein. Here we studied a photosynthetic antenna pigment-protein complex LH2 with single molecule two-dimensional polarization imaging. Modeling based on the Redfield relaxation theory well describes the observed polarization properties of LH2 fluorescence and fluorescence excitation, strongly suggesting that at 77 K the conformational subspace of the LH2 is limited to about three configurations with relatively frequent switching among each other. At room temperature the next level of fluctuations determines the conformational dynamics. The results support the multitier model of the energy landscape of proteins and demonstrate the potential of the method for the studies of structural dynamics in proteins.

Preprocess dependence of optical properties of ensembles and single siphonaxanthin-containing major antenna from the marine green alga Codium fragile

“…In contrast, studying the complexes individually provides information about the distributions of parameters rather than only about their moments, which allows to identify subpopulations that would be obscured otherwise. In the past, single-molecule spectroscopy has been applied extensively to the antennae complexes of purple bacteria [11][12][13][14][15][16][17][18][19][20] and to the light-harvesting systems associated with plant photosystems I and II [21][22][23][24][25][26][27][28][29] for obtaining information about the energetics and dynamics both at cryogenic temperatures as well as under ambient conditions, recently excellently reviewed in 30 . At low temperatures thermal motions of the nuclei are frozen out and the electronic transition energies that serve as input for structure-based modelling can be detected with enhanced spectral resolution.…”

Robust light harvesting by a noisy antenna

“… 39 , 51 This approach has been previously successfully used to describe the ultrafast intra-ring transfer. 17 , 45 The energy transfer between the strongly coupled blocks of pigments, i.e. between the B800 and B850 rings, is well described by the generalized multi-chromophoric Förster theory.…”

“…Some temperature dependent measurements suggest a heterogeneity/anharmonicity of the protein potential energy surface (PES). 17 , 60 At the same time, for most of the ambient temperature experiments, including the SMS studies, the disorder was successfully described by a normal distribution. 16 , 31 , 32 , 36 The argument for this description is based on many relevant protein degrees of freedom, leading to a Gaussian distribution of the energies thanks to the central limit theorem.…”

“…Furthermore, previous work has shown that at cryogenic temperatures, the protein fluctuations become anharmonic, adopting multiple possible configurations. 17 , 60 Comparison of low ambient and low temperature measurement could therefore provide interesting information on the nature of the protein fluctuations and the related pigment energetic disorder.…”