New Dimensions in Ultrafast Spectroscopy Reveal Ancient Secrets of Photosynthesis

In photosynthesis, antenna proteins harvest light and efficiently transfer the electronic excitation energy to reaction center proteins that initiate chemical transformations. The standard Forster framework for understanding electronic energy transfer is based on the adiabatic approximation of slow vibrations and fast electronic motions. Femtosecond two-dimensional spectra of many antenna proteins exhibit quantum beats with signatures indicative of nonadiabatic vibrational-electronic coupling. The longest lived beats originate from a nonadiabatic enhancement of Raman pathways for excitation of delocalized vibrations on the electronic ground state. These vibrations characterize the initial coupling between excited states and reveal nested funnels in which the adiabatic approximation fails spectacularly over entire vibrational coordinate spaces. The nonadiabatic dynamics in nested funnels is efficient at low vibrational energies and does not require the high vibrational velocities usually associated with breakdown of the adiabatic approximation. Nested funnel design principles will be discussed.