Light Harvesting by Equally Contributing Mechanisms in a Photosynthetic Antenna Protein

Abstract

We report supramolecular quantum mechanics/molecular mechanics simulations on the peridinin-chlorophyll a protein (PCP) complex from the causative algal species of red tides. These calculations reproduce for the first time quantitatively the distinct peridinin absorptions, identify multichromophoric molecular excitations, and elucidate the mechanisms regulating the strongly allowed S (1A) → S (1B) absorptions of the bound peridinins that span a 58 nm spectral range in the region of maximal solar irradiance. We discovered that protein binding site-imposed conformations, local electrostatics, and electronic coupling contribute equally to the spectral inhomogeneity. Electronic coupling causes coherent excitations among the densely packed pigments. Complementary pairing of tuning mechanisms is the result of a competition between pigment-pigment and pigment-environment interactions. We found that the aqueous solvent works in concert with the charge distribution of PCP to produce a strong correlation between peridinin spectral bathochromism and the local dielectric environment.

Carotenoid-Chlorophyll Interactions in a Photosynthetic Antenna Protein: A Supramolecular QM/MM Approach

“…We previously found that the electrostatic environment of the aqueously solvated PCP complex significantly contributes to the Per site energy regulation [ 8 ]. By varying the energy gaps between individual Pers, and/or screening inter-chromophore interactions, the electrostatic environment could, in principle, also modulate the Per-Per and Per-Chl a interaction strengths [ 32 ].…”

“…Alternatively, the close packing of PCP cofactors could isolate the chromophores from environmental effects [ 32 ]. We demonstrated elsewhere that static charge interactions of the Pers with the PCP environment and with one another exert opposing influences on the absorption spectrum [ 8 ]. We therefore wondered if or how the environment tunes the inter-chromophore coupling strengths.…”

“…A reconstituted, recombinant PCP (RFPCP) complex ( Figure 1 c), which is a homodimer of the N -terminal domain from the wild-type protein, has been used as a model system to study both spectral tuning and excitation energy transfer [ 4 ]. The cofactor clusters in either MF- or RFPCP harvest blue-green photons with ~90% efficiency [ 4 ] by mechanisms intimately related to the structure of Per and the architecture of the solvated PCP complex [ 8 ].…”

“…By contrast, the maximal solvatochromic shift reported for the S 2 absorption maximum in a variety of homogeneous solvents is only 16–28 nm [ 6 ]. We recently reported multichromophoric quantum mechanical/molecular mechanical (QM/MM) simulations that delineated the controlling factors for wavelength regulation in PCP, and permitted the first unambiguous assignment of the distinct Per spectral signatures to specific chromophores [ 8 ]. Protein-induced conformational distortion, inter-chromophore electronic coupling, and the electrostatic environment of the complex, mediated by an aqueous dielectric, were found to make nearly equal and additive contributions to the S 0 → S 2 wavelength variation.…”

“…A step towards such understanding would at least require a full characterization of electronic coupling strengths between all chromophoric cofactors. It is only recently, with the aid of supramolecular QM/MM approaches [ 8 ], that such evaluations can be accurately obtained. Supramolecular QM/MM refers to the implementation of QM/MM methods where the quantum mechanical (QM) regions involve entire supramolecular assemblies of distinct units.…”