Environmental thermal energy fluctuations assist uphill excitation energy transfer from red chlorophylls to the reaction center within plant photosystem I

The PSI–LHCI chlorophyll–protein complex is a nano-machine within the photosynthetic system in which a small subset of chlorophyll molecules absorbs light at energies lower than that of the reaction center (RC). Despite this energy mismatch, the low-energy chlorophyll forms (LES) efficiently transfer excitation energy (EET) to the RC, contributing to charge separation. At room temperature, more than 80% of the thermally equilibrated excitation population resides on LES, implying that photochemical trapping frequently involves energetically uphill EET. This raises a fundamental question: how can excitation reach the RC against an energy gradient? Here, a thermodynamic framework is developed to address this question. By combining known experimental observations with a coarse-grained analysis of excitation energy transfer, it is concluded that the additional energy required to overcome the energy gap between LES and the RC comes from thermal energy fluctuations in the chlorophyll environment, including the protein scaffold and membrane, which act as an active energy source. The estimated internal energy fluctuations of the amino acid residues coordinating LES chlorophylls exceed this energy gap, thereby making fluctuation-assisted transfer physically plausible. Within this viewpoint, the excited chlorophyll–protein system operates as a stochastic rectifier, selectively capturing thermal fluctuations to drive excitation towards the RC against an energy gradient. This work proposes a shift in perspective, from viewing environmental fluctuations as a passive background to recognizing them as an active thermodynamic resource enabling uphill excitation energy transfer.