Color tuning in short wavelength-sensitive human and mouse visual pigments: ab initio quantum mechanics/molecular mechanics studies

Abstract

We have investigated the protonation state and photoabsorption spectrum of Schiff-base (SB) nitrogen bound 11-cis-retinal in human blue and mouse UV cone visual pigments as well as in bovine rhodopsin by hybrid quantum mechanical/molecular mechanical (QM/MM) calculations. We have employed both multireference (MRCISD+Q, MR-SORCI+Q, and MR-DDCI2+Q) and single reference (TD-B3LYP and RI-CC2) QM methods. The calculated ground-state and vertical excitation energies show that UV-sensitive pigments have deprotonated SB nitrogen, while violet-sensitive pigments have protonated SB nitrogen, in agreement with some indirect experimental evidence. A significant blue shift of the absorption maxima of violet-sensitive pigments relative to rhodopsins arises from the increase in bond length alternation of the polyene chain of 11-cis-retinal induced by polarizing fields of these pigments. The main counterion is Glu113 in both violet-sensitive vertebrate pigments and bovine rhodopsin. Neither Glu113 nor the remaining pigment has a significant influence on the first excitation energy of 11-cis-retinal in the UV-sensitive pigments that have deprotonated SB nitrogen. There is no charge transfer between the SB and beta-ionone terminals of 11-cis-retinal in the ground and first excited states.

Figure 1

QM models, R1 and R2, and atom numbering of PSBR. SBR corresponds to removing the circled hydrogen (gas phase) or transferring it to Glu113 carboxylic oxygen.

Figure 2

Calculated bond length alternation along the polyene chain of the SB and PSB 11-cis-retinal chromophore for RH, HB, and MUV. Average BLA is also given.

Figure 3

HOMO and LUMO of the SB and PSB 11-cis-retinals calculated at the CASSCF level in the gas phase (labeled as QM-none) and at the CASSCF/AMBER level with RH, HB, and MUV pigment environments. Average BLA is given in parentheses.

Figure 4

B3LYP and B3LYP/MM ground-state energies (kcal/mol) of PSBR relative to SBR [QM model: (a) R2 and (b) R2 + Wat2b] in the gas phase and in RH, HB, and MUV pigment environments at the ONIOM-EE structures optimized with R1.

Figure 5

Some important amino acid sites around SB nitrogen. Coordinates taken from RH.

Figure 6

Amino acids that show strong polarization effect on the S₁ excitation energy of HB. PSBR and Lys296 bound covalently to each other are shown in green.