Consistent Model of Ultrafast Energy Transfer in Peridinin Chlorophyll- A Protein Using Two-Dimensional Electronic Spectroscopy and Förster Theory

Solar light harvesting begins with electronic energy transfer in structurally complex light-harvesting antennae such as the peridinin chlorophyll-a protein from dinoflagellate algae. Peridinin chlorophyll-a protein is composed of a unique combination of chlorophylls sensitized by carotenoids in a 4:1 ratio, and ultrafast spectroscopic methods have previously been utilized in elucidating their energy-transfer pathways and timescales. However, due to overlapping signals from various chromophores and competing pathways and timescales, a consistent model of intraprotein electronic energy transfer has been elusive. Here, we used a broad-band two-dimensional electronic spectroscopy, which alleviates the spectral congestion by dispersing excitation and detection wavelengths. Interchromophoric couplings appeared as cross peaks in two-dimensional electronic spectra, and these spectral features were observed between the peridinin S₂ states and chlorophyll-a Q_x and Q_y states. In addition, the inherently high time and frequency resolutions of two-dimensional electronic spectroscopy enabled accurate determination of the ultrafast energy-transfer dynamics. Kinetic analysis near the peridinin S₁ excited-state absorption, which forms in 24 fs after optical excitation, reveals an ultrafast energy-transfer pathway from the peridinin S₂ state to the chlorophyll-a Q_x state, a hitherto unconfirmed pathway critical for fast interchromophoric transfer. We propose a model of ultrafast peridinin chlorophyll-a protein photophysics that includes (1) a conical intersection between peridinin S₂ and S₁ states to explain both the ultrafast peridinin S₁ formation and the residual peridinin S₂ population for energy transfer to chlorophyll-a, and (2) computationally and experimentally derived peridinin S₂ site energies that support the observed ultrafast peridinin S₂ to chlorophyll-a Q_x energy transfer.