Excitonic Energy Transfer in Red Algal Photosystem I Reveals an Evolutionary Bridge between Cyanobacteria and Plants

Abstract

Photosystem I converts light into chemical energy with near-unity quantum efficiency,yet its energy-transfer and charge-separation mechanisms remain debated. Evolution has diversified PSI architectures. The unicellular red algae Cyanidioschyzon merolae represents a key evolutionary intermediate,featuring a cyanobacterial-like monomeric core surrounded by three to five LHCR subunits. This hybrid organization provides a unique system to bridge mechanistic models across lineages. We applied two-dimensional electronic spectroscopy at ultralow temperatures to disentangle overlapping excitation pathways in C. merolae PSI. Cryogenic measurements suppressed thermal broadening, resolving five dynamical components: sub-picosecond equilibration acrossthe core-LHCR interface, subsequent population transfer into progressively lowerenergy manifolds, and slower feeding into red pools distributed across both core and antenna. On the longest timescales, a persistent ground-state bleach signifies excitons stabilised in terminal sinks. Notably, comparison of 8 K and 80 K spectra reveals that excitations are heterogeneously partitioned among multiple sinks at low disorder, whereas modest thermal activation promotes selective convergence into core-associated red chlorophylls. To interpret these dynamics, we employed atomistic excitonic Hamiltonians with time-nonlocal master equations, providing a quantitative framework for exciton migration and thermal redistribution. Together, these results demonstrate that C. merolae PSI broadens the kinetic funnel by distributing sinks across core and antenna, an evolutionary adaptation that extends spectral coverage whilst ensuring efficient trapping. These insights reconcile cyanobacterial and plant paradigms and illuminate how antenna expansion reshaped PSI function during the course of photosynthetic evolution.