Efficiency Limits of Energy Conversion by Light-Driven Redox Chains.

The conversion of absorbed sunlight to spatially separated electron-hole pairs is a crucial outcome of natural photosynthesis. Many organisms achieve near-unit quantum yields of charge separation (one electron-hole pair per incident photon) by dissipating as heat more than half of the light energy that is deposited in the primary donor. Might alternative choices have been made by Nature that would sacrifice quantum yield in favor of producing higher energy electron/hole pairs? Here, we use a multisite electron hopping model to address the kinetic and thermodynamic compromises that can be made in electron transfer chains, with the aim of understanding Nature's choices and opportunities in bioinspired energy-converting systems. We find that if the electron-transfer coordinates are even weakly coupled to a high-frequency vibrational mode, substantial energy dissipation is necessary to achieve the maximum possible energy storage in an electron-transfer chain. Since high-frequency vibronic coupling is common in physiological redox cofactors, we posit that biological reaction centers have recruited a strategy to convert light energy into redox potential with the near-optimum energy efficiency that is possible in an electron-transfer chain. Our simulations also find that charge separation in electron-transfer chains is subject to a minimum intercofactor separation distance, beneath which energy-dissipating charge recombination is unavoidable. We find that high quantum yield and low energy dissipation can thus be realized simultaneously for multistep electron transfer if recombination pathways are uncoupled from high-frequency vibrations and if the cofactors are held at small-to-intermediate distances apart (ca. 3 to 8 Å edge-to-edge). Our analysis informs the design of bioinspired light-harvesting structures that may exceed 60% energy efficiency, as opposed to the ∼30% efficiency achieved in natural photosynthesis.