Understanding Ultrafast Energy Transfer across the Photosynthetic Membrane of Purple Bacteria with Near-Native Systems

Abstract

Purple bacteria are able to capture sunlight and convert it to chemical energy through charge separation with almost 100% quantum efficiency. This remarkable efficiency is due to the arrangement of their pigments into pigment-protein complexes that are further arranged into a larger antenna network within the membrane environment. Peripheral light-harvesting complex 2 (LH2) surrounds the core light-harvesting complex 1 (LH1), which in turn encircles the reaction center (RC). Energy absorbed by LH2 is transferred to LH1 and then finally the RC, where it is converted to chemical energy through charge separation. While the energy transfer dynamics of the photosynthetic light-harvesting complexes in purple bacteria have been studied for decades, two key parameters have been largely ignored: first, the ability of purple bacteria to maintain efficiency in fluctuating environmental conditions, and second, the impact of the lipid membrane environment on the energy transfer pathways. In this thesis, I explore these two parameters by investigating the energy transfer dynamics within the purple bacterial antenna network at each step. First, I study intra-complex dynamics by comparing the energy transfer rates within structural and spectral variants of LH2. Second, I investigate inter-complex energy transfer dynamics between LH2 complexes to directly resolve and understand the pair-wise energy transfer dynamics within the membrane. Finally, I investigate the influence of lipid environment on LH1 to RC energy transfer. These studies are made possible by the use of model membrane nanodiscs, through which I reconstruct the antenna network piece-by-piece to resolve key energy transfer steps in a controlled, near-native environment. Overall, the results show that the energy transfer dynamics within the purple bacterial antenna network are robust to fluctuating environmental conditions, with the membrane itself an active participant in the optimization of these energy transfer processes. Furthermore, these studies reveal the utility of nanodiscs to disentangle the many competing parameters within the membrane that influence protein behavior and energy transfer dynamics.