Insight into the Structural Role of Carotenoids in the Photosystem I: A Quantum Chemical Analysis

AbstractThe structural stabilization role of carotenoids in the formation of photosynthetic pigment-protein complexes is investigated theoretically. The π–π stacking and CH-π interactions between β-carotenes and their surrounding chlorophylls (and/or aromatic residues) in Photosystem I (PS1) from the cyanobacterium Synechococcus elongatus were studied by means of the supermolecular approach at the level of the second-order Møller-Plesset perturbation method. PS1 features a core integral antenna system consisting of 22 β-carotenes intertwined with 90 chlorophyll molecules. The binding environments of all 22 β-carotenes were systematically analyzed. For 21 out of the 22 cases, one or more chlorophyll molecules exist within van der Waals’ contacts of the β-carotene molecule. The calculated strengths of π–π stacking interactions between the conjugated core of β-carotene and the aromatic tetrapyrrole rings of chlorophyll are substantial, ranging from −3.54kcal/mol for the perpendicular-positioned BCR4004…CHL1217 pair to −16.01 kcal/mol for the parallel-oriented BCR4007…CHL1122 pair. A strong dependence of the π–π stacking interaction energies on the intermolecular configurations of the two interacting π-planes is observed. The parallel-oriented β-carotene and chlorophyll pair is energetically much more stable than the perpendicular-positioned pair. The larger the extent of π–π overlapping, the stronger the interaction strength. In many cases, the β-ring ends of β-carotene molecules are found to interact with the tetrapyrrole rings of chlorophyll via CH-π interactions. For the latter interactions, the calculated interaction strengths vary from −7.03 to −11.03kcal/mol, depending on the intermolecular configuration. This work leads to the conclusion that π–π stacking and CH-π interactions between β-carotene and their surrounding chlorophylls and aromatic residues play an essential role in binding β-carotenes in PS1 from S. elongatus. Consequently, the molecular basis of the structural stabilization function of carotenoids in formation of the photosynthetic pigment-protein complexes is established