EXPLORING STRUCTURE-FUNCTION RELATIONSHIPS IN PHOTOSYNTHETIC LIGHT-HARVESTING ANTENNA COMPLEXES USING QUANTUM CHEMISTRY AND ULTRAFAST MULTIDIMENSIONAL ELECTRONIC SPECTROSCOPY

Abstract

Photosynthetic organisms make structurally complex light-harvesting pigment-protein complexes with high quantum efficiency. The studies presented in this dissertation explore the structure-function relationship in two complexes – peridinin chlorophyll-a protein (PCP) from dinoflagellate Amphidinium carterae and phycocyanin 645 (PC645) from cryptophyte Chroomonas mesostigmatica – using quantum chemistry and ultrafast two-dimensional electronic spectroscopy (2DES). PCP is a protein complex containing eight peridinin and two chlorophyll-a molecules, while PC645 contains eight bilins covalently bonded to a quaternary protein structure.

Focus on the functional aspect of these light-harvesting complexes is widespread in literature; their structures serve as starting geometries for chromophoric electronic excited states calculations. This dissertation starts with energy decomposition analyses of the non-covalent interactions between the chromophores and the surrounding environment using symmetry-adapted perturbation theory. Dominance of dispersion and electrostatics were identified in PCP and PC645 respectively, reflecting the different strategies in pigment-packing by the protein scaffold. Furthermore, the bilins in PC645 were shown to have pH-dependent non-covalent involvement in structural integrity.

The non-covalent interaction composition differences informed the quantum chemical electronic excited states calculations. PCP chromophores demonstrated less spectral shifts upon inclusion of the surrounding amino acids when compared to the bilins, a reflection of the weak dispersion-dominated non-covalent interactions in the former when compared to the strong electrostatics-dominance in the latter. Calculations using a quantum chemically optimized whole-PCP geometry demonstrated that the crystal structure is a poor starting geometry. In addition, double excitation character were shown to be necessary to obtain a balanced description of bilins’ excited states.

2DES was then used to propose a consistent model of the ultrafast energy transfer dynamics in PCP. 2DES is capable of relieving spectral congestion, as it extends the spectral information contained in a one-dimensional pump-probe spectrum onto an additional spectral axis. Peridinin S2 to chlorophyll-a Qx energy transfer pathway and peridinin Sx excited-state absorption was discovered.

Quantum chemistry and 2DES came together to investigate vibronic coupling in chlorophyll-a, in which the Qx state is calculated to be energetically 0.2 – 0.3 eV above the Qy state, while 2DES beat maps resolved vibrational character borrowing of the Qx state from the Qy state.