Glycerol binding at the narrow channel of photosystem II stabilizes the low-spin S.sub.2 state of the oxygen-evolving complex

• Published in: Photosynthesis research 2022-05, Vol.152 (2), p.167
• Main Authors: Flesher, David A, Liu, Jinchan, Wiwczar, Jessica M, Reiss, Krystle, Yang, Ke R, Wang, Jimin, Askerka, Mikhail
• Format: Article
• Language: English
• Subjects: Analysis; Crystals; Glycerin; Glycerol; Hydrogen; Structure
• ISSN: 0166-8595
• DOI: 10.1007/s11120-022-00911-0

The oxygen-evolving complex (OEC) of photosystem II (PSII) cycles through redox intermediate states S.sub.i (i = 0-4) during the photochemical oxidation of water. The S.sub.2 state involves an equilibrium of two isomers including the low-spin S.sub.2 (LS-S.sub.2) state with its characteristic electron paramagnetic resonance (EPR) multiline signal centered at g = 2.0, and a high-spin S.sub.2 (HS-S.sub.2) state with its g = 4.1 EPR signal. The relative intensities of the two EPR signals change under experimental conditions that shift the HS-S.sub.2/LS-S.sub.2 state equilibrium. Here, we analyze the effect of glycerol on the relative stability of the LS-S.sub.2 and HS-S.sub.2 states when bound at the narrow channel of PSII, as reported in an X-ray crystal structure of cyanobacterial PSII. Our quantum mechanics/molecular mechanics (QM/MM) hybrid models of cyanobacterial PSII show that the glycerol molecule perturbs the hydrogen-bond network in the narrow channel, increasing the pK.sub.a of D1-Asp61 and stabilizing the LS-S.sub.2 state relative to the HS-S.sub.2 state. The reported results are consistent with the absence of the HS-S.sub.2 state EPR signal in native cyanobacterial PSII EPR spectra and suggest that the narrow water channel hydrogen-bond network regulates the relative stability of OEC catalytic intermediates during water oxidation.