Phycobilisome's Exciton Transfer Efficiency Relies on an Energetic Funnel Driven by Chromophore-Linker Protein Interactions

The phycobilisome is the primary light-harvesting antennain cyanobacterialand red algal oxygenic photosynthesis. It maintains near-unity efficiencyof energy transfer to reaction centers despite relying on slow excitonhopping along a relatively sparse network of highly fluorescent phycobilinchromophores. How the complex maintains this high efficiency remainsunexplained. Using a two-dimensional electronic spectroscopy polarizationscheme that enhances energy transfer features, we directly watch energyflow in the phycobilisome complex of Synechocystis sp. PCC 6803 from the outer phycocyanin rods to the allophycocyanincore. The observed downhill flow of energy, previously hidden withincongested spectra, is faster than timescales predicted by Fo''rsterhopping along single rod chromophores. We attribute the fast, 8 psenergy transfer to interactions between rod-core linker proteins andterminal rod chromophores, which facilitate unidirectionally downhillenergy flow to the core. This mechanism drives the high energy transferefficiency in the phycobilisome and suggests that linker protein-chromophoreinteractions have likely evolved to shape its energetic landscape.