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

The
light-driven sodium-pump rhodopsin KR2 exhibits ultrafast photoisomerization
dynamics of its all-trans 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-trans to
13-cis 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.