The plastoquinol–plastoquinone exchange mechanism in photosystem II: insight from molecular dynamics simulations

• Published in: Photosynthesis research 2017-01, Vol.131 (1), p.15-30
• Main Authors: Zobnina, Veranika, Lambreva, Maya D., Rea, Giuseppina, Campi, Gaetano, Antonacci, Amina, Scognamiglio, Viviana, Giardi, Maria Teresa, Polticelli, Fabio
• Format: Article
• Language: English
• Subjects: Biochemistry; Biomedical and Life Sciences; Crystal structure; Electron transport; Hydrogen; Hydrogen Bonding; Hydrogen bonds; Life Sciences; Ligands; Membrane lipids; Molecular biology; Molecular dynamics; Molecular Dynamics Simulation; Original Article; Photosynthesis; Photosystem II Protein Complex - metabolism; Plant Genetics and Genomics; Plant Physiology; Plant Sciences; Plastoquinone - analogs & derivatives; Plastoquinone - metabolism
• ISSN: 0166-8595; 1573-5079
• DOI: 10.1007/s11120-016-0292-4

In the photosystem II (PSII) of oxygenic photosynthetic organisms, the reaction center (RC) core mediates the light-induced electron transfer leading to water splitting and production of reduced plastoquinone molecules. The reduction of plastoquinone to plastoquinol lowers PSII affinity for the latter and leads to its release. However, little is known about the role of protein dynamics in this process. Here, molecular dynamics simulations of the complete PSII complex embedded in a lipid bilayer have been used to investigate the plastoquinol release mechanism. A distinct dynamic behavior of PSII in the presence of plastoquinol is observed which, coupled to changes in charge distribution and electrostatic interactions, causes disruption of the interactions seen in the PSII–plastoquinone complex and leads to the “squeezing out” of plastoquinol from the binding pocket. Displacement of plastoquinol closes the second water channel, recently described in a 2.9 Å resolution PSII structure (Guskov et al. in Nat Struct Mol Biol 16:334–342, 2009 ), allowing to rule out the proposed “alternating” mechanism of plastoquinol–plastoquinone exchange, while giving support to the “single-channel” one. The performed simulations indicated a pivotal role of D 1 -Ser264 in modulating the dynamics of the plastoquinone binding pocket and plastoquinol–plastoquinone exchange via its interaction with D 1 -His252 residue. The effects of the disruption of this hydrogen bond network on the PSII redox reactions were experimentally assessed in the D 1 site-directed mutant Ser264Lys.