Insights into the Early-Time Excited-State Dynamics of Structurally Inhomogeneous Rhodopsin KR2

Abstract

The light-driven sodium-pump rhodopsin KR2 exhibits ultrafast photoisomerization dynamics of its all-<i>trans</i> protonated Schiff-base retinal (PSBR). However, the excited-state decay of KR2 also shows slow picosecond time constants, which are attributed to nonreactive states. The mechanism that produces long-lived states is unclear. Here, by using molecular dynamics simulations and large-scale XMCQDPT2-based QM/MM modeling, we explore the origin of reactive and nonreactive states in KR2. By calculating the S₀-S₁ vibronic band shapes, we gain insight into the early-time excited-state dynamics of PSBR and show that the protein environment can significantly alter vibrational modes that are active upon photoexcitation, thus facilitating photoisomerization from all-<i>trans</i> to 13-<i>cis</i> PSBR. Importantly, we reveal structural heterogeneity of the retinal-binding pocket of KR2, characterized by three distinct conformations, and conclude that the formation of a strong hydrogen bond between the retinal Schiff base and its counterion is essential for the ultrafast reaction dynamics.