Thermodynamics of the S2-To-S3 state transition of the oxygen-evolving complex of photosystem II

Muhamed Amin, Divya Kaur, Ke R. Yang, Jimin Wang, Zainab Mohamed, Gary W. Brudvig, M. R. Gunner, Victor Batista

Research output: Contribution to journalArticle

Abstract

The room temperature pump-probe X-ray free electron laser (XFEL) measurements used for serial femtosecond crystallography provide remarkable information about the structures of the catalytic (S-state) intermediates of the oxygen-evolution reaction of photosystem II. However, mixed populations of these intermediates and moderate resolution limit the interpretation of the data from current experiments. The S3 XFEL structures show extra density near the OEC that may correspond to a water/hydroxide molecule. However, in the latest structure, this additional oxygen is 2.08 Å from the Oϵ2 of D1-E189, which is closer than the sum of the van der Waals radii of the two oxygens. Here, we use Boltzmann statistics and Monte Carlo sampling to provide a model for the S2-To-S3 state transition, allowing structural changes and the insertion of an additional water/hydroxide. Based on our model, water/hydroxide addition to the oxygen-evolving complex (OEC) is not thermodynamically favorable in the S2g = 2 state, but it is in the S2g = 4.1 redox isomer. Thus, formation of the S3 state starts by a transition from the S2g = 2 to the S2g = 4.1 structure. Then, electrostatic interactions support protonation of D1-H190 and deprotonation of the Ca2+-ligated water (W3) with proton loss to the lumen. The W3 hydroxide moves toward Mn4, completing the coordination shell of Mn4 and favoring its oxidation to Mn(iv) in the S3 state. In addition, binding an additional hydroxide to Mn1 leads to a conformational change of D1-E189 in the S2g = 4.1 and S3 structures. In the S3 state a fraction of D1-E189 release from Mn1 and bind a proton.

Original languageEnglish
Pages (from-to)20840-20848
Number of pages9
JournalPhysical Chemistry Chemical Physics
Volume21
Issue number37
DOIs
Publication statusPublished - Jan 1 2019

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Photosystem II Protein Complex
hydroxides
Thermodynamics
Oxygen
thermodynamics
X ray lasers
oxygen
Water
Free electron lasers
free electron lasers
water
Protons
Deprotonation
lumens
Crystallography
protons
Protonation
Coulomb interactions
Isomers
crystallography

ASJC Scopus subject areas

  • Physics and Astronomy(all)
  • Physical and Theoretical Chemistry

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Thermodynamics of the S2-To-S3 state transition of the oxygen-evolving complex of photosystem II. / Amin, Muhamed; Kaur, Divya; Yang, Ke R.; Wang, Jimin; Mohamed, Zainab; Brudvig, Gary W.; Gunner, M. R.; Batista, Victor.

In: Physical Chemistry Chemical Physics, Vol. 21, No. 37, 01.01.2019, p. 20840-20848.

Research output: Contribution to journalArticle

Amin, M, Kaur, D, Yang, KR, Wang, J, Mohamed, Z, Brudvig, GW, Gunner, MR & Batista, V 2019, 'Thermodynamics of the S2-To-S3 state transition of the oxygen-evolving complex of photosystem II', Physical Chemistry Chemical Physics, vol. 21, no. 37, pp. 20840-20848. https://doi.org/10.1039/c9cp02308a
Amin, Muhamed ; Kaur, Divya ; Yang, Ke R. ; Wang, Jimin ; Mohamed, Zainab ; Brudvig, Gary W. ; Gunner, M. R. ; Batista, Victor. / Thermodynamics of the S2-To-S3 state transition of the oxygen-evolving complex of photosystem II. In: Physical Chemistry Chemical Physics. 2019 ; Vol. 21, No. 37. pp. 20840-20848.
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