Abstract
Cryptochromes and photolyases are flavoproteins that may undergo ultrafast charge separation uponelectronic excitation of their flavin cofactors. Charge separation involves chains of three or four tryptophanresidues depending on the protein of interest. The molecular mechanisms of these processes are notcompletely clear. In the present work we investigate the relevance of quantum effects like the occurrenceof nuclear tunneling and of coherences upon charge transfer in Arabidopsis thaliana cryptochromes. Thepossible breakdown of the Condon approximation is also investigated. We have devised a simulationprotocol based on the realization of molecular dynamics simulations on diabatic potential energy surfacesdefined at the hybrid constrained density functional theory/molecular mechanics level. The outcomes ofthe simulations are analyzed through various dedicated kinetics schemes related to the Marcus theorythat account for the aforementioned quantum effects. MD simulations also provide a basic material todefine realistic model Hamiltonians for subsequent quantum dissipative dynamics. To carry out quantumsimulations, we have implemented an algorithm based on the Hierarchical Equations of Motion. Withthis new tool in hand we have been able to model the electron transfer chain considering either two- orthree-state models. Kinetic models and quantum simulations converge to the conclusion that quantumeffects have a significant impact on the rate of charge separation. Nuclear tunneling involving atoms ofthe tryptophan redox cofactors as well as of the environment (protein atoms and water molecules) issignificant. On the other hand non-Condon effects are negligible in most simulations. Taken together,the results of the present work provide new insights into the molecular mechanisms controlling chargeseparation in this family of flavoproteins.