How fine-tuned for energy transfer is the environmental noise produced by proteins around biological chromophores?

Abstract

We investigate the role of the local protein environment on the energy transfer processes in biological molecules, excluding from the analysis the effect of intra-chromophore nuclear motions, and focussing on the exciton-phonon coupling. We studied three different proteins (FMO and two variants of the WSCP protein) with different biological functions but similar chromophores, to understand whether a classification of chromophores based on the details of the environment would be possible, and whether specific environments enhance or suppress the coupling between exciton and protein dynamics. Our results show that despite the different biological role, there is no significant difference in the influence of the environment on the properties of the chromophores. Additionally, we show that the main role in influencing molecular properties is played by solvent molecules: the interaction occurs on a medium-range scale, and the solvent is kept in place by a strong H-bond network being free to rotate, suggesting a dipole-dipole interaction mechanism. Steric hindrance exerted by other moieties can help modulating the interactions and tuning the energy transfer process. Overall, considering also the relatively greater importance of intra-molecular nuclear motions, the protein environment around biological chromophores does not appear fine-tuned for a specific function.

Developing Consistent Molecular Dynamics Force Fields for Biological Chromophores via Force Matching

“…The observed differences in the high-frequency region of the spectral density are potentially important to correctly identify the presence (or lack of) of intramolecular vibrational modes capable of vibronic enhancement. In fact, intramolecular modes are the only one likely able to specifically couple with the electron energy transfer because recent work has shown the unspecificity of the local protein environment surrounding a pigment …”

“…B3LYP/3-21G* was used for the QM part, which was reduced through the insertion of a link atom between carbon atoms 1 and 2 of the phytyl chain. The 3-21G* basis set was used to reduce computational time as it has been found (Figure S2 in ref ) that there is good correlation between 6-31G* and 3-21G* for these systems. Four roots were computed but only the lowest was considered.…”

DFTB/MM Molecular Dynamics Simulations of the FMO Light-Harvesting Complex

“…Spectral densities represent the system–bath coupling and can be calculated from the autocorrelation function of the excitation energy fluctuations of the individual pigment molecules. To date, mainly Zerner’s intermediate neglect of differential orbital method with spectroscopic parameters together with configuration interaction using single excitations (ZINDO/S-CIS) and time-dependent density functional theory (TDDFT) calculations have been utilized in order to calculate the site energy fluctuations along classical MD-based ground-state simulations in a quantum mechanics/molecular mechanics (QM/MM) fashion. ,,,− Although the TDDFT approach is numerically less expensive than wave-function-based schemes, it is still more CPU-time-demanding than semiempirical ZINDO/S-CIS calculations . TDDFT calculations based on long-range-corrected (LC) or hybrid functionals are known to overestimate the energy gap between the ground and excited states, while the ZINDO/S-CIS scheme has been parametrized for BChl-type pigment molecules.…”

“…Structurally, BChl 3 is the terminal emitter to the reaction center, and it is believed to participate in the exciton state having the lowest site energy, ,, although this is not undisputed. ,, It is reassuring that in the QM/MM dynamics calculation with the best sampling, i.e., the 1 ns trajectory, BChl 3 actually has the lowest site energy. At the same time, we want to emphasize that the differences in the site energies of the different pigments are very small and likely within the accuracy of the employed ground- and excited-state methods.…”

Explaining the Efficiency of Photosynthesis: Quantum Uncertainty or Classical Vibrations?

“…To see this, we have reproduced the problem numerically by neglecting the analogous terms in the mapping framework. The resulting theory is formally equivalent to the so-called ground-state classical path approximation, − which has been frequently used in QM/MM simulations of FMO and other light-harvesting complexes. − Figure (d) shows the results of applying this method to describe the exciton dynamics. It can be seen that it leads to the same failure as “classical” Redfield theory, with all excitonic states becoming equally populated in the long-time limit.…”