Color Tuning in Rhodopsins: The Origin of the Spectral Shift between the Chloride-Bound and Anion-Free Forms of Halorhodopsin

Detailed knowledge of the molecular mechanisms that control
the
spectral properties in the rhodopsin protein family is important for
understanding the functions of these photoreceptors and for the rational
design of artificial photosensitive proteins. Here we used a high-level
ab initio QM/MM method to investigate the mechanism of spectral tuning
in the chloride-bound and anion-free forms of halorhodopsin from Natronobacterium pharaonis (phR) and the interprotein
spectral shift between them. We demonstrate that the chloride ion
tunes the spectral properties of phR via two distinct mechanisms:
(i) electrostatic interaction with the chromophore, which results
in a 95 nm difference between the absorption maxima of the two forms,
and (ii) induction of a structural reorganization in the protein,
which changes the positions of charged and polar residues and reduces
this difference to 29 nm. The present study expands our knowledge
concerning the role of the reorganization of the internal H-bond network
for color tuning in general and provides a detailed investigation
of the tuning mechanism in phR in particular.