Entropy is an important design principle in the photosystem II supercomplex

• 成果类型: Article
• 署名作者: Hall, Johanna L.; Yang, Shiun -, Jr.; Limmer, David T.; Fleming, Graham R.; Rossky, Peter J.
• 署名单位: University of California System; University of California Berkeley; United States Department of Energy (DOE); Lawrence Berkeley National Laboratory; University of California System; University of California Berkeley; United States Department of Energy (DOE); Lawrence Berkeley National Laboratory; United States Department of Energy (DOE); Lawrence Berkeley National Laboratory; Massachusetts Institute of Technology (MIT)
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-14793
• DOI: 10.1073/pnas.2426331122
• 发表日期: 2025-03-25
• 关键词: light-harvesting complexes; energy-transfer; supramolecular organization; reaction centers; optical-spectra; quantum yield; antenna; mechanism; lhcii; EVOLUTION

摘要

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.