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

Abstract

The structural stabilization role of carotenoids in the formation of photosynthetic pigment-protein complexes is investigated theoretically. The pi-pi stacking and CH-pi interactions between beta-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 beta-carotenes intertwined with 90 chlorophyll molecules. The binding environments of all 22 beta-carotenes were systematically analyzed. For 21 out of the 22 cases, one or more chlorophyll molecules exist within van der Waals' contacts of the beta-carotene molecule. The calculated strengths of pi-pi stacking interactions between the conjugated core of beta-carotene and the aromatic tetrapyrrole rings of chlorophyll are substantial, ranging from -3.54 kcal/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 pi-pi stacking interaction energies on the intermolecular configurations of the two interacting pi-planes is observed. The parallel-oriented beta-carotene and chlorophyll pair is energetically much more stable than the perpendicular-positioned pair. The larger the extent of pi-pi overlapping, the stronger the interaction strength. In many cases, the beta-ring ends of beta-carotene molecules are found to interact with the tetrapyrrole rings of chlorophyll via CH-pi interactions. For the latter interactions, the calculated interaction strengths vary from -7.03 to -11.03 kcal/mol, depending on the intermolecular configuration. This work leads to the conclusion that pi-pi stacking and CH-pi interactions between beta-carotene and their surrounding chlorophylls and aromatic residues play an essential role in binding beta-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.

Structural and Functional Roles of Carotenoids in Chlorosomes

“…We may also expect that the interaction between BChl and carotenoid molecules is weaker in C. aurantiacus than in C. tepidum because the carotenoids present in C. aurantiacus (mainly ␤-carotene and ␥-carotene) do not contain end groups but ␤-rings, with two out-of-plane methyl substituents. In this case, a CH-interaction seems to be responsible for the attractive interaction between the carotenoid end ring and the conjugated system of the BChl molecule (36). CH-interaction is weaker than the -interaction, and therefore, ␤-carotene is more easily removed by hexane than chlorobactene.…”

Orbital optimization in the density matrix renormalization group, with applications to polyenes and β-carotene

“…Crystalline ␤-carotene has C i symmetry with a conjugated backbone that lies almost entirely on the xy plane except for end groups that are twisted out of plane. 93,94 ͑In the biological setting, carotenoid pigments usually adopt a twisted configuration in the conjugated backbone 95,96 ͒. There are 11 conjugated double bonds in the backbone.…”

Isolation and characterization of a PSI–LHCI super-complex and its sub-complexes from a siphonaceous marine green alga, Bryopsis Corticulans

“…These carotenes were bound at the surfaces of PsaA, PsaB, and several small subunits (Jordan et al 2001) and are suggested to play a structural role as a ''hydrophobic glue'' in stabilizing the multi-subunit PSI core complex by interactions with their surrounding chlorophylls and aromatic residues (Fromme et al 2003;Wang et al 2004). Two important implications for the replacement of b-carotene by a-carotene and e-carotene can be considered.…”