Molecular basis of the exciton–phonon interactions in the PE545 light-harvesting complex

Abstract

Long-lived quantum coherences observed in several photosynthetic pigment-protein complexes at low and at room temperatures have generated a heated debate over the impact that the coupling of electronic excitations to molecular vibrations of the relevant actors (pigments, proteins and solvents) has on the excitation energy transfer process. In this work, we use a combined MD and QM/MMPol strategy to investigate the exciton-phonon interactions in the PE545 light-harvesting complex by computing the spectral densities for each pigment and analyzing their consequences in the exciton dynamics. Insights into the origin of relevant peaks, as well as their differences among individual pigments, are provided by correlating them with normal modes obtained from a quasi-harmonic analysis of the motions sampled by the pigments in the complex. Our results indicate that both the protein and the solvent significantly modulate the intramolecular vibrations of the pigments thus playing an important role in promoting or suppressing certain exciton-phonon interactions. We also find that these low-frequency features are largely smoothed out when the spectral density is averaged over the complex, something difficult to avoid in experiments that underscores the need to combine theory and experiment to understand the origin of quantum coherence in photosynthetic light-harvesting.

Limits and potentials of quantum chemical methods in modelling photosynthetic antennae

“…The impact of such modulation is here illustrated for the PE545 complex. 24 Figure 3-top reports the distribution of the vibrational modes of the PEB 82c bilin computed using a normal mode (NMA) analysis of the free pigment and a quasi-harmonic (QH) analysis of the pigment embedded in the protein matrix, respectively. The NMA analysis proves the vibrations around a single minimum, while the QH analysis aims at characterizing the global extent of the configurational space accessible to the system during an MD simulation.…”

Combining classical molecular dynamics and quantum mechanical methods for the description of electronic excitations: The case of carotenoids

“…[3][4][5][6][7][8][9][10] The understanding of the different roles of carotenoids in LH systems was made possible mainly owing to the advances in X-ray diffraction techniques, now able to resolve the crystalline structures of the complexes at a good level of accuracy. [15][16][17][18][19][20][21][22][23][24][25] The MD simulations allow the study of the PPCs in different environments, as well as the realistic simulation of the in vivo conditions, by inserting the complex into a solvated lipid membrane. In parallel, the detailed information on the structural properties of the complexes has allowed the use of computational chemistry techniques to support the experimental findings, and to predict the properties that are not possible to be assessed using the current experimental techniques.…”

“…A common computational strategy used in the study of PPCs is the combination of classical molecular dynamics (MD) simulations with quantum mechanical (QM) calculations of the electronic processes. [16,18,25] It is evident that in all these analyses the quality of the molecular mechanics (MM) force-fields (FF) used to describe the protein backbone, the solvent, and the cofactors (including the pigments) plays a fundamental role. [20][21][22] Typically, the MD trajectories are applied to obtain structural information used in different analyses, such as the calculation of the spatial correlations between the atomic motions and the normal mode analysis.…”

“…A common computational strategy used in the study of PPCs is the combination of classical molecular dynamics (MD) simulations with quantum mechanical (QM) calculations of the electronic processes. [15][16][17][18][19][20][21][22][23][24][25] The MD simulations allow the study of the PPCs in different environments, as well as the realistic simulation of the in vivo conditions, by inserting the complex into a solvated lipid membrane. [20][21][22] Typically, the MD trajectories are applied to obtain structural information used in different analyses, such as the calculation of the spatial correlations between the atomic motions and the normal mode analysis.…”

Modeling DNA electronic circular dichroism by QM/MM methods and Frenkel Hamiltonian

“…Although some more complicated schemes using the coupling between the monomers' excited state density matrices exist [42][43][44], the simplest formalism consists in simply considering the coupling between the monomeric transition dipoles as well as their distances and orientations. However, in the case of chiral aggregates, such as helical arrangements, the two transitions may have different signs of the rotatory strengths and therefore they can be easily differentiated in the spectrum.…”