Efficiency Limits of\nEnergy Conversion by Light-Driven\nRedox Chains

The\nconversion of absorbed sunlight to spatially separated electron–hole\npairs is a crucial outcome of natural photosynthesis. Many organisms\nachieve near-unit quantum yields of charge separation (one electron–hole\npair per incident photon) by dissipating as heat more than half of\nthe light energy that is deposited in the primary donor. Might alternative\nchoices have been made by Nature that would sacrifice quantum yield\nin favor of producing higher energy electron/hole pairs? Here, we\nuse a multisite electron hopping model to address the kinetic and\nthermodynamic compromises that can be made in electron transfer chains,\nwith the aim of understanding Nature’s choices and opportunities\nin bioinspired energy-converting systems. We find that if the electron-transfer\ncoordinates are even weakly coupled to a high-frequency vibrational\nmode, substantial energy dissipation is necessary to achieve the maximum\npossible energy storage in an electron-transfer chain. Since high-frequency\nvibronic coupling is common in physiological redox cofactors, we posit\nthat biological reaction centers have recruited a strategy to convert\nlight energy into redox potential with the near-optimum energy efficiency\nthat is possible in an electron-transfer chain. Our simulations also\nfind that charge separation in electron-transfer chains is subject\nto a minimum intercofactor separation distance, beneath which energy-dissipating\ncharge recombination is unavoidable. We find that high quantum yield\nand low energy dissipation can thus be realized simultaneously for\nmultistep electron transfer if recombination pathways are uncoupled\nfrom high-frequency vibrations and if the cofactors are held at small-to-intermediate\ndistances apart (ca. 3 to 8 Å edge-to-edge). Our analysis informs\nthe design of bioinspired light-harvesting structures that may exceed\n60% energy efficiency, as opposed to the ∼30% efficiency achieved\nin natural photosynthesis.