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 , 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.

The molecular mechanisms of light adaption in light-harvesting complexes of purple bacteria revealed by a multiscale modeling

“…The obtained results, reported in Table S5 of the ESI, † clearly show that, if we use the crystal structures without any relaxation, a very large (and unphysical) blue-shi of ca. 2000 cm À1 is found for both a and bBChls when moving from LHL to LL, exactly as found by De Vico et al 20 However, as soon as we relax the bond lengths (and bond angles), still keeping the dihedral angles frozen (and hence the macrocycle curvature), these differences almost disappear: they reduce to 40 cm À1 and 60 cm À1 when calculated for the isolated a and bBChls, respectively, and to 65 and 186 cm À1 when the effect of the MMPol environment is included. If we further relax all the internal degrees of freedom together with the close by residues, we do not see any further signicant change, showing that the bond lengths play a major role in determining the excitation energy.…”

“…3, but now the simulated spectra of LL-LH2 and HM-PucD have been obtained by correcting the site energies by the additional blue-shi induced by the different out-of-plane distorsion of aBChl and bBChl as predicted by crystal data (for HM-PucD we have assumed the same distorsion as LL-LH2). This conclusion in some way goes against what reported in recent computational studies by De Vico and coworkers, 20,58 who used a multistate multiconguration restricted active space with second-order perturbation theory correction (MS-RASPT2) to calculate the excitation energies of the BChl at their crystal structure. In the same study, instead, a different source of the blue shi was suggested, that is, the change in the BChl macrocycle ring curvature.…”

“…In particular, the huge differences found in the literature for the Q y excitations of HL and LL-LH2 (ref. 20,58) can be accurately explained by the fact that the crystal (1NKZ) structure of HL-LH2 displays an unphysical conjugation pattern of the macrocycle ring due to inaccurate bond lengths. Instead, the BChls from the crystal structure of LH3 (1IJD) present a more regular pattern of bond lengths within the macrocycle ring and, as a result, a huge blue-shi is obtained when compared to the HL-LH2.…”

“…Deformation of the macrocycle ring has been suggested to give large shis of the Q y absorption band. 20 Electrostatic and polarization effects: the residues around the BChls can produce large shis in absorption, with the magnitude and direction of the shi depending upon the electric elds and the polarization effects due to their specic nature and the disposition in the different complexes. 21,22 Charge transfer (CT) effects: the coupling between higher energy CT states between BChls in the 18-meric ring and the locally excited Q y states inuences the exciton structure of the complex, 23,24 lowering the energy of the rst bright exciton state, which gives rise to the longest wavelength band in the absorption spectrum.…”

Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation

“…As a matter of fact, more accurate QM methods have been also used for LH complexes, mostly as benchmarks for less expensive methods [41,42], even though some direct applications have also been presented. In particular, we quote here the complete active space methods in combination with perturbation theory (CAS-PT2) used for bacteriochlorophylls and carotenoids of LH2 [43,44], the approximate second-order coupled cluster (CC2) and the algebraic diagrammatic construction through second-order (ADC(2)) methods used for dimers and larger clusters of (bacterio)chlorophylls [45,46], and the Bethe-Salpeter equation and the GW approximation (BSE/GW) used for phycoerythrobilins of PE545 [47].…”