In Silico Study of a Bacteriorhodopsin/TiO2 Hybrid System at the Molecular Level

Abstract

Bacteriorhodopsin (bR) is a light-harvesting membrane protein that represents a promising sensitizer of TiO₂ for photovoltaic and photoelectrochemical devices. However, despite numerous experimental studies, the molecular-level understanding of the bR/TiO₂ hybrid system is still unsatisfactory. In this contribution, we report the construction and analysis of an atomistic model of such a system. To do so, both steered molecular dynamics-molecular dynamics and quantum mechanics/molecular mechanics computations are applied to four different bR orientations on the anatase TiO₂ surface. The resulting bR/TiO₂ models are then used to compute the light absorption maxima changes relative to those of bR. We show that all four models reproduce the experimentally observed blue-shift value induced by bR binding on TiO₂ and could be used to study the binding and binding-induced protein modifications. We conclude that the constructed models could provide a basis for future studies aiming to simulate the complex long-range electron transfer mechanism in bR/TiO₂-based solar energy conversion devices as well as in engineering bR to achieve enhanced efficiencies.

Figure 1

QM region (highlighted in the light red box) employed in the QM/MM calculations.

Figure 2

Top: tilting and rotating directions used to generate (a) bR-O1/TiO₂, (b) bR-O2/TiO₂, (c) bR-O3/TiO₂, and (d) bR-O4/TiO₂ systems. Bottom: zoom of the protein structures of bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ in the proximity of the surface. Models were created using MAESTRO 11.8 Schrödinger Release 2020–1: Maestro, Schrödinger, LLC, New York, NY, 2020). The anatase surface is shown in a ball and stick representation (gray balls represent titanium atoms, whereas red balls represent oxygen atoms). The protein is reported in its secondary structure, and residues Pro37, Arg164, and Glu234 are displayed in ball and stick representation.

Figure 3

DFT-PBE/DZVP HOMO and LUMO of the retinal in isolated bR.

Figure 4

Interacting residues within 5 Å from the surface in (a) bR-O1/TiO₂, (b) bR-O2/TiO₂, (c) bR-O3/TiO₂, and (d) bR-O4/TiO₂ systems. Atom color scheme by residue property: dark green, hydrophobic; cyan, polar uncharged; blue, positively charged; red, negatively charged. The secondary structure is shown in gray. Models were created using MAESTRO 11.8 (Schrödinger Release 2020–1: Maestro, Schrödinger, LLC, New York, NY, 2020).

Figure 5

Backbone RMSD, in Å, of the four bR/TiO₂ hybrid systems during 7.5 ns of the MD adsorption process.

Figure 6

Representation of the last interacting residues of the desorption process in (a) bR-O1/TiO₂, (b) bR-O2/TiO₂, (c) bR-O3/TiO₂, and (d) bR-O4/TiO₂ systems. Atom color scheme by residue property: dark green, hydrophobic; cyan, polar uncharged; blue, positively charged; red, negatively charged. Models were created using MAESTRO 11.8 (Schrödinger Release 2020–1: Maestro, Schrödinger, LLC, New York, NY, 2020).

Figure 7

Deviations of C−α coordinates of the optimized isolated bR and bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ systems with respect to the bR crystallographic structure.

Figure 8

Representation of the cavity environment. Only hydrogens of water molecules are reported explicitly.

Figure 9

Deviations of C−α coordinates of the amino acids present in the cavity of the optimized isolated bR and bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ systems with respect to the bR crystallographic structure.

Figure 10

Bond lengths distances (Å) along the retinal conjugated chain of bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, bR-O4/TiO₂ in comparison to those of retinal in the isolated bR model.

Figure 11

Mulliken partial charge distribution along the retinal conjugated chain (including C₅–C₁₅, N_Z and C_ε QM atoms) of bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ in comparison to that of the retinal in the isolated bR model. Hydrogen partial charges are added into the partial charge of their respective linked carbons or nitrogen atoms. The total Mulliken partial charge distribution is equal to one adding the contribution of the remaining QM atoms.

Figure 12

Dihedral angles deviation (°) along the retinal conjugated chain of bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ with respect to the isolated bR model optimized in this work.

Figure 13

CAM-B3LYP/6-31+G(d) plotted UV–Vis spectra of isolated bR, bR-O1/TiO₂, bR-O2/TiO₂, bR-O3/TiO₂, and bR-O4/TiO₂ using Molden 5.6 and a Gaussian distribution (half bandwidth set to 20 nm).