Constrained geometric dynamics of the Fenna-Matthews-Olson complex: The role of correlated motion in reducing uncertainty in excitation energy transfer

TL;DR

This study investigates the slow protein dynamics and correlated motions in the Fenna-Matthews-Olson complex, revealing structural hierarchies and high rigidity that influence quantum coherence and energy transfer efficiency.

Contribution

It introduces constrained geometric dynamics to analyze protein flexibility and uncovers highly correlated low-frequency motions affecting excitonic interactions.

Findings

Highly correlated low-frequency motions between pigments and protein elements

The FMO complex exhibits exceptionally high rigidity

Low variance in excitonic couplings suggests inhomogeneous electronic disorder

Abstract

The Fenna Mathews Olson (FMO) complex of green sulphur bacteria is an example of a photosynthetic pigment protein complex, in which the electronic properties of the pigments are modified by the protein environment to promote efficient excitonic energy transfer from antenna complexes to the reaction centres. Many of the electronic properties of the FMO complex can be extracted from knowledge of the static crystal structure. However, the recent observation and analysis of long lasting quantum dynamics in the FMO complex point to protein dynamics as a key factor in protecting and generating quantum coherence under laboratory conditions. While fast inter and intra molecular vibrations have been investigated extensively, the slow dynamics which effectively determine the optical inhomogeneous broadening of experimental ensembles has received less attention. Our study employs constrained geometric dynamics to study the flexibility in the protein network by efficiently generating the accessible conformational states from the published crystal structure. Statistical and principle component analysis reveal highly correlated low frequency motions between functionally relevant elements, including strong correlations between pigments that are excitonically coupled. Our analysis reveals a hierarchy of structural interactions which enforce these correlated motions, from the level of monomer monomer interfaces right down to the alpha helices, beta sheets and pigments. In addition to inducing strong spatial correlations across the conformational ensemble, we find that the overall rigidity of the FMO complex is exceptionally high. We suggest that these observations support the idea of highly correlated inhomogeneous disorder of the electronic excited states, which is further supported by the remarkably low variance of the excitonic couplings of the conformational ensemble.