Glycerol Binding at the Narrow Channel of Photosystem II Stabilizes the Low-Spin S2 State of the Oxygen-Evolving Complex

Flesher, David A.; Liu, Jinchan; Wiwczar, Jessica M.; Reiss, Krystle; Yang, Ke R.; Wang, Jimin; Askerka, Mikhail; Gisriel, Christopher J.; Batista, Victor S.; Brudvig, Gary W.

doi:10.1007/s11120-022-00911-0

Glycerol Binding at the Narrow Channel of Photosystem II Stabilizes the Low-Spin S₂ State of the Oxygen-Evolving Complex

Journal Article · Wed Mar 23 00:00:00 EDT 2022 · Photosynthesis Research

DOI:https://doi.org/10.1007/s11120-022-00911-0· OSTI ID:1860621

Flesher, David A. ^[1]; Liu, Jinchan ^[2]; Wiwczar, Jessica M. ^[2]; Reiss, Krystle ^[2]; Yang, Ke R. ^[2]; Wang, Jimin ^[2]; Askerka, Mikhail ^[2]; Gisriel, Christopher J. ^[2]; Batista, Victor S. ^[2]; Brudvig, Gary W. ^[2]

Yale Univ., New Haven, CT (United States); Yale University
Yale Univ., New Haven, CT (United States)

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 S₂ state involves an equilibrium of two isomers including the low-spin S₂ (LS-S₂) state with its characteristic electron paramagnetic resonance (EPR) multiline signal centered at g = 2.0, and a high-spin S₂ (HS-S₂) state with its g = 4.1 EPR signal. The relative intensities of the two EPR signals change under experimental conditions that shift the HS-S₂/LS-S₂ state equilibrium. Here, we analyze the effect of glycerol on the relative stability of the LS-S₂ and HS-S₂ 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-S₂ state relative to the HS-S₂ state. Here, the reported results are consistent with the absence of the HS-S₂ 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.

View Accepted Manuscript (DOE)

Research Organization:: Yale Univ., New Haven, CT (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-05ER15646; SC0001423

OSTI ID:: 1860621

Journal Information:: Photosynthesis Research, Journal Name: Photosynthesis Research Journal Issue: 2 Vol. 152; ISSN 0166-8595

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Electron paramagnetic resonance
Glycerol
Hydrogen-bond network
Oxygen evolution
Photosystem II
Quantum mechanics/molecular mechanics
S2 state

Glycerol Binding at the Narrow Channel of Photosystem II Stabilizes the Low-Spin S2 State of the Oxygen-Evolving Complex

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Glycerol Binding at the Narrow Channel of Photosystem II Stabilizes the Low-Spin S₂ State of the Oxygen-Evolving Complex