Macrocycle ring deformation as the secondary design principle for light-harvesting complexes

Abstract

Natural light-harvesting is performed by pigment-protein complexes, which collect and funnel the solar energy at the start of photosynthesis. The identity and arrangement of pigments largely define the absorption spectrum of the antenna complex, which is further regulated by a palette of structural factors. Small alterations are induced by pigment-protein interactions. In light-harvesting systems 2 and 3 from Rhodoblastus acidophilus, the pigments are arranged identically, yet the former has an absorption peak at 850 nm that is blue-shifted to 820 nm in the latter. While the shift has previously been attributed to the removal of hydrogen bonds, which brings changes in the acetyl moiety of the bacteriochlorophyll, recent work has shown that other mechanisms are also present. Using computational and modeling tools on the corresponding crystal structures, we reach a different conclusion: The most critical factor for the shift is the curvature of the macrocycle ring. The bending of the planar part of the pigment is identified as the second-most important design principle for the function of pigment-protein complexes-a finding that can inspire the design of novel artificial systems.

Keywords: LH3; MS-RASPT2; bacteriochlorophyll; chromophore mimics; macrocycle ring deformation.

Fig. 1.

Structure of LH2 and LH3. The overall structure of LH2 and LH3 (as shown in the middle) is similar: A barrel of alpha helices (green) keeps in position the various bacteriochlorophyll units, shown in blue (the B800 ring) and in red (the B850 ring). The two rings are also bridged by carotenoid molecules, which were omitted for clarity. The frame highlights BChl units 304 and 305 from B850. The differences in hydrogen bonding are shown in the two lower Insets. In LH2 (Bottom Left Inset), tyrosine 44 (Y44) and tryptophan 45 (W45) provide hydrogen bonds (dashed lines) to the acetyl moieties, while these residues are substituted by phenylalanine (F44) and leucine (L45) in LH3 (Bottom Right Inset). Possibly, in LH3, W40 and Y41 of two different chains provide hydrogen bonds to the acetyl moieties. The corresponding experimental spectra are shown above the two Insets. Reprinted from ref. . Copyright (1986), with permission from Elsevier.

Fig. 2.

Model structure of bacteriochlorophyll a. Shown is the structure of the model of bacteriochlorophyll a used in this work, with standard ring naming (A, B, C, D, E) and the investigated dihedral torsions (a, b, c, d). Numbers indicate various atoms mentioned in the text.

Fig. 3.

Computed energetics profiles of unit 304. From the top, TD-DFT (full symbols and lines) and MS-RASPT2 (open symbols and dashed lines) computed potential energy surfaces, excitation energy, oscillator strength, and TDM changes along the interpolation scan relative to unit 304, where BChl-1 and BChl-47 are the geometries obtained from LH2 and LH3 crystal structures, respectively. Relative energies were computed with respect to BChl-47. The vertical bands divide the geometries relative to torsion around dihedral angles a, b, c, and d; the adjustment of hydrogen atom position (H); and the change in the MCR curvature. A similar landscape was also found for unit 303, as reported in SI Appendix, Fig. S5. SI Appendix, Table S4 reports relative energetics along the scan for selected geometries.

Fig. 4.

Simulated spectra. (A) Simulated spectra for a hypothetical torsion from 0 to 90 degrees of the acetyl moiety. The spectra are based on TD-DFT–obtained excitation energies and TDM values, and both alpha and beta units were assigned the same excitations. (B) Changes in simulated spectra along the LH2 to LH3 scan. Underlying data are obtained from interpolated MS-RASPT2 excitation energies and TDM, for both alpha and beta units. The numbering of the spectra corresponds to the various BChl structures, as reported in the text. (C) Simulated spectrum using the excitation energies and TDM of alpha and beta units denoted 38.5 as the best approximation of the experimental spectrum of LH3. All simulated spectra are the result of considering 18 BChl units and their various couplings, as described in ref. .

Fig. 5.

Bacteriochlorophyll curvatures. Simplified models of BChl, exemplifying the differences in MCR torsion between (A) LH2 and (B) LH3. A fictitious axis is added to both structures to guide the eye. Also shown are examples of bacteriochlorophyll-inspired chromophores, in which the (${\mathrm{C}\mathrm{H}}_2$)_n bridge should induce an MCR torsion similar to that of (C) LH2 or (D) LH3, depending on the connecting atoms on the ring.