Open AccessGlycerol binding at the narrow channel of photosystem II stabilizes the low-spin S2 state of the oxygen-evolving complex
Author(s) -
David A. Flesher,
Jinchan Liu,
Jessica Wiwczar,
Krystle Reiss,
Ke Yang,
Jimin Wang,
Mikhail Askerka,
Christopher J. Gisriel,
Víctor S. Batista,
Gary W. Brudvig
Publication year - 2022
Publication title -
photosynthesis research
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.158
H-Index - 113
eISSN - 1573-5079
pISSN - 0166-8595
DOI - 10.1007/s11120-022-00911-0
Subject(s) - electron paramagnetic resonance , photosystem ii , oxygen evolving complex , chemistry , site directed spin labeling , oxygen evolution , hydrogen bond , spin states , photochemistry , oxygen , crystallography , molecule , nuclear magnetic resonance , photosynthesis , physics , inorganic chemistry , biochemistry , organic chemistry , electrode , electrochemistry
The oxygen-evolving complex (OEC) of photosystem II (PSII) cycles through redox intermediate states S i (i = 0-4) during the photochemical oxidation of water. The S 2 state involves an equilibrium of two isomers including the low-spin S 2 (LS-S 2 ) state with its characteristic electron paramagnetic resonance (EPR) multiline signal centered at g = 2.0, and a high-spin S 2 (HS-S 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 2 /LS-S 2 state equilibrium. Here, we analyze the effect of glycerol on the relative stability of the LS-S 2 and HS-S 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 a of D1-Asp61 and stabilizing the LS-S 2 state relative to the HS-S 2 state. The reported results are consistent with the absence of the HS-S 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.