Entropy is an important design principle in the photosystem II supercomplex

Abstract

Photosystem II (PSII) can achieve near-unity quantum efficiency of light harvesting in ideal conditions and can dissipate excess light energy as heat to prevent the formation of reactive oxygen species (ROS) under light stress. Understanding how this pigment-protein complex accomplishes these opposing goals is a topic of great interest that has so far been explored primarily through the lens of the system energetics. Despite PSII's known flat energy landscape, a thorough consideration of the entropic effects on energy transfer in PSII is lacking. In this work, we aim to discern the free energetic design principles underlying the PSII energy transfer network. To accomplish this goal, we employ a structure-based rate matrix and compute the free energy terms in time following a specific initial excitation to discern how entropy and enthalpy drive ensemble system dynamics. We find that the interplay between the entropy and enthalpy components differ among each protein subunit, which allows each subunit to fulfill a unique role in the energy transfer network. This individuality ensures that PSII can accomplish efficient energy trapping in the reaction center (RC), effective nonphotochemical quenching (NPQ) in the periphery, and robust energy trapping in the other-monomer RC if the same-monomer RC is closed. We also show that entropy, in particular, is a dynamically tunable feature of the PSII free energy landscape accomplished through regulation of LHCII binding. These findings help rationalize natural photosynthesis and provide design principles for more efficient solar energy harvesting technologies.

Keywords: energy landscape; ensemble dynamics; entropy; excitation energy transfer; free energy.

Fig. 1.

The pigment arrangement of the C₂S₂M₂-type PSII supercomplex with protein subunits labeled (PDB: 5XNL) (20). The solid line marks the separation of the two monomers.

Fig. 2.

Entropy (solid line) and enthalpy (dashed line) components of the free energy change in time for initial excitations at selected states in the core antenna (A and B), minor antenna (C and D), and peripheral antenna (E–H) complexes. In order of A–E, excitations are localized in Chl a 509 in CP43, Chl a 610 in CP47, Chl a 604 in CP26, Chl a 604 in CP29, Chl a 610 in S-LHCII (B), Chl a 610 in M-LHCII (B), Chl b 609 in S-LHCII (B), and Chl b 609 in M-LHCII (B).

Fig. 3.

Population contraction times for each initial excitation in the C₂S₂M₂-type PSII supercomplex when (A) both RCs are open and (B) the monomer 2 (Bottom) RC is closed, projected onto the site basis. The charge transfer state is located between Chl_D1 and Pheo_D1 in the RC.

Fig. 4.

The probability for each initial excitation to be trapped in the monomer 1 RC (Top), assuming all population ends up in the traps, projected onto the site basis.

Fig. 5.

Population contraction times for each initial excitation in the C₂S₂-type PSII supercomplex when (A) both RCs are open and (B) the monomer 2 (Bottom) RC is closed, projected onto the site basis. The charge transfer state is located between Chl_D1 and Pheo_D1 in the RC.