Design principles for energy transfer in the photosystem II supercomplex from kinetic transition networks

Abstract

Photosystem II (PSII) has the unique ability to perform water-splitting. With light-harvesting complexes, it forms the PSII supercomplex (PSII-SC) which is a functional unit that can perform efficient energy conversion, as well as photoprotection, allowing photosynthetic organisms to adapt to the naturally fluctuating sunlight intensity. Achieving these functions requires a collaborative energy transfer network between all subunits of the PSII-SC. In this work, we perform kinetic analyses and characterise the energy landscape of the PSII-SC with a structure-based energy transfer model. With first passage time analyses and kinetic Monte Carlo simulations, we are able to map out the overall energy transfer network. We also investigate how energy transfer pathways are affected when individual protein complexes are removed from the network, revealing the functional roles of the subunits of the PSII-SC. In addition, we provide a quantitative description of the flat energy landscape of the PSII-SC. We show that it is a unique landscape that produces multiple kinetically relevant pathways, corresponding to a high pathway entropy. These design principles are crucial for balancing efficient energy conversion and photoprotection.

Fig. 1. Structure of the C₂S₂M₂-type PSII-SC.

a Pigment arrangement of the C₂S₂M₂-type PSII-SC adapted from the structure reported by Su et al. (PDB: 5XNL). b Labelling of the protein subunits. The colours of the subunits match those in (a), where the D1 subunits (CP43, CP26, and S-LHCII) are shown in green, the D2 subunits (CP47, CP29, CP24, and M-LHCII) are shown in blue and purple, and the RCs are shown in red. The black dashed line indicates the separation between the two PSII monomers, with the upper and lower monomers labelled as Monomer 1 and 2, respectively. The yellow stars represent the locations of the initial excitations discussed in the main text. RC: reaction centre. S-A: S-LHCII (A). S-B: S-LHCII (B). S-C: S-LHCII (C). M-A: M-LHCII (A). M-B: M-LHCII (B). M-C: M-LHCII (C).

Fig. 2. First passage time analysis.

a Schematic representation of how the FPT distribution from S-LHCII to the RCs can be obtained from kMC trajectories. Short/medium/long trajectories, coloured in red/yellow/blue, contribute to the corresponding shaded area in the FPT distribution. b First passage time (FPT) distributions for the pathways from the initial excitation locations in Fig. 1b to the RCs in the WT PSII-SC. c FPT distributions for the WT and selected mutants of PSII-SC starting from excitation in CP43. The final state can be either RC. The FPT distributions are normalised according to the area under the curves. The shaded areas (light grey to dark grey) correspond to the FPT ranges discussed in the main text (see Dwell Time Distribution Analysis and Fig. 3). Source data files are available at 10.5281/zenodo.13346121.

Fig. 3. Dwell time distribution for CP43 initial excitation.

Dwell time distributions extracted from the trajectories of initial excitations in CP43 in the FPT range of (a–d) 13.5 to 23.5 ps (Fig. 2c, light grey), (e–h) 50 to 90 ps (Fig. 2c, grey), (i–l) 155 to 255 ps (Fig. 2c, dark grey). The distributions from top to bottom are for the WT, koCP26, koS-C, and koS-B, respectively. In each panel, categories on the left are the subunits in Monomer 1 and categories on the right are those in Monomer 2. Source data files are available at 10.5281/zenodo.13346121.

Fig. 4. Simulation of NPQ with different quenching sites.

Probability of initial excitations in each subunit being quenched when the quencher is placed in (a) CP26, (b) S-LHCII (A) (S-A), (c) S-LHCII (B) (S-B), (d) S-LHCII (C) (S-C), (e) CP24, (f) CP29, (g) M-LHCII (A) (M-A), (h) M-LHCII (B) (M-B), and (i) M-LHCII (C) (M-C). The subunit where a quencher is placed is shown in yellow. The darker green a subunit is, the more likely the initial excitations in that subunit are quenched. Only subunits on the left side of the PSII-SC are shown (see Fig. 1). Source data files are available at 10.5281/zenodo.13346121.

Fig. 5. Energy landscape of the PSII-SC.

Free energy disconnectivity graph^, for the original WT PSII-SC kinetic transition network created using the disconnectionDPS program. Each branch terminates at one of the exciton states of the PSII-SC, which is the basis for EET calculations. Free energy increases on the vertical axis. The branches that terminate at single substates are coloured according to the mean first passage time for energy transfer to either RC for that substate, as indicated in the key. The branches close to the RC are red in this colour scheme because they have the shortest MFPT values. The initial excitation locations (CP43, CP47, S-B, and M-B) and the final states (RC1 and RC2) discussed in the Results section are pointed out by the arrows and labelled accordingly. The approximate two-fold symmetry in the graph reflects the dimeric structure of the complex. Source data files are available at 10.5281/zenodo.13346121.