Multi-Scale Simulations of Excited-State Energy Transfer Pathways in the C2S2-Type PSII-LHCII Supercomplex of Spinach

Abstract

Photosystem II-light-harvesting complex II (PSII-LHCII) supercomplex achieves efficient excitation energy transfer (EET), yet how directional transfer emerges from its nearly flat energy landscape has remained unclear. Here, we investigate the C2S2-type spinach PSII-LHCII supercomplex containing 206 pigments by integrating microsecond-scale molecular dynamics, QM/MM site energy calculations, and generalized Forster theory. The computed site energy landscape shows overall downhill gradients from peripheral antennas to the reaction center (RC), with small variations fully explained by dynamic structural fluctuations. Pairwise transfer rates reveal a dense multi-timescale EET network, where fast intra-subunit and interface couplings provide robust channels and slower links maintain global connectivity. Key interface pigments act as energy-funneling hotspots that converge excitations toward the RC. Within the PSII core, both the D1 and D2 branches ultimately transfer energy downhill to ChlD1 and ChlD2, respectively, ensuring thermodynamic feasibility of delivery. Three major transfer pathways were identified, all falling within functional timescales (< 250 ps). Bidirectional dynamics were also observed, with rapid reverse transfers enabling excess excitation to be safely dissipated through peripheral antennas. Together, these results demonstrate that PSII maintains fully downhill energy transfer through the combined effects of structural constraints and dynamic regulation, thereby achieving both efficient energy delivery and photoprotection.