DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca²⁺ or Ca²⁺ substituted by Sr²⁺

Abstract

The oxygen-evolving complex of photosystem II can function with either Ca²⁺ or Sr²⁺ as the heterocation, but the reason for differing turnover rates remains unresolved despite reported X-ray crystal structures for both forms. Using quantum mechanics/molecular mechanics (QM/MM) calculations, we optimize structures with each cation in both the resting state (S₁) and in a series of reduced states (S₀, S₋₁, and S-₂). Through comparison with experimental data, we determine that X-ray crystal structures with either Ca²⁺ or Sr²⁺ are most consistent with the S-₂ state, Mn₄[III,III,III,II] with O4 and O5 protonated. As expected, the QM/MM models show that Ca²⁺/Sr²⁺ substitution results in elongation of the heterocation bonds and displaces terminal waters W3 and W4. The optimized structures also show that hydrogen-bonded W5 is displaced in all S states with Sr²⁺ as the heterocation, suggesting that this water may play a critical role during water oxidation.

Authors:
 [1];  [2];  [1];  [1];  [1]
  1. Yale Univ., New Haven, CT (United States)
  2. Yale Univ., New Haven, CT (United States); Brookhaven National Lab. (BNL), Upton, NY (United States)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1183828
Report Number(s):
BNL-107849-2015-JA
Journal ID: ISSN 0006-2960; R&D Project: CO045; KC0301020
Grant/Contract Number:  
SC00112704
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 54; Journal Issue: 3; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Vogt, Leslie, Ertem, Mehmed Z., Pal, Rhitankar, Brudvig, Gary W., and Batista, Victor S. Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca²⁺ or Ca²⁺ substituted by Sr²⁺. United States: N. p., 2015. Web. doi:10.1021/bi5011706.
Vogt, Leslie, Ertem, Mehmed Z., Pal, Rhitankar, Brudvig, Gary W., & Batista, Victor S. Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca²⁺ or Ca²⁺ substituted by Sr²⁺. United States. https://doi.org/10.1021/bi5011706
Vogt, Leslie, Ertem, Mehmed Z., Pal, Rhitankar, Brudvig, Gary W., and Batista, Victor S. Thu . "Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca²⁺ or Ca²⁺ substituted by Sr²⁺". United States. https://doi.org/10.1021/bi5011706. https://www.osti.gov/servlets/purl/1183828.
@article{osti_1183828,
title = {Computational insights on crystal structures of the oxygen-evolving complex of photosystem II with either Ca²⁺ or Ca²⁺ substituted by Sr²⁺},
author = {Vogt, Leslie and Ertem, Mehmed Z. and Pal, Rhitankar and Brudvig, Gary W. and Batista, Victor S.},
abstractNote = {The oxygen-evolving complex of photosystem II can function with either Ca²⁺ or Sr²⁺ as the heterocation, but the reason for differing turnover rates remains unresolved despite reported X-ray crystal structures for both forms. Using quantum mechanics/molecular mechanics (QM/MM) calculations, we optimize structures with each cation in both the resting state (S₁) and in a series of reduced states (S₀, S₋₁, and S-₂). Through comparison with experimental data, we determine that X-ray crystal structures with either Ca²⁺ or Sr²⁺ are most consistent with the S-₂ state, Mn₄[III,III,III,II] with O4 and O5 protonated. As expected, the QM/MM models show that Ca²⁺/Sr²⁺ substitution results in elongation of the heterocation bonds and displaces terminal waters W3 and W4. The optimized structures also show that hydrogen-bonded W5 is displaced in all S states with Sr²⁺ as the heterocation, suggesting that this water may play a critical role during water oxidation.},
doi = {10.1021/bi5011706},
journal = {Biochemistry},
number = 3,
volume = 54,
place = {United States},
year = {Thu Jan 15 00:00:00 EST 2015},
month = {Thu Jan 15 00:00:00 EST 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 29 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Photosystem II: The machinery of photosynthetic water splitting
journal, October 2008


Recent developments in research on water oxidation by photosystem II
journal, April 2012

  • Dau, Holger; Zaharieva, Ivelina; Haumann, Michael
  • Current Opinion in Chemical Biology, Vol. 16, Issue 1-2
  • DOI: 10.1016/j.cbpa.2012.02.011

Photosystem II: The Reaction Center of Oxygenic Photosynthesis
journal, June 2013


Water-Splitting Chemistry of Photosystem II
journal, November 2006

  • McEvoy, James P.; Brudvig, Gary W.
  • Chemical Reviews, Vol. 106, Issue 11
  • DOI: 10.1021/cr0204294

COOPERATION OF CHARGES IN PHOTOSYNTHETIC O 2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM
journal, June 1970


Alternating electron and proton transfer steps in photosynthetic water oxidation
journal, September 2012

  • Klauss, A.; Haumann, M.; Dau, H.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
  • DOI: 10.1073/pnas.1206266109

Calcium reconstitutes high rates of oxygen evolution in polypeptide depleted Photosystem II preparations
journal, February 1984


Quantifying the Ion Selectivity of the Ca 2+ Site in Photosystem II:  Evidence for Direct Involvement of Ca 2+ in O 2 Formation
journal, July 2001

  • Vrettos, John S.; Stone, Daniel A.; Brudvig, Gary W.
  • Biochemistry, Vol. 40, Issue 26
  • DOI: 10.1021/bi010679z

Biosynthetic Ca2+/Sr2+ Exchange in the Photosystem II Oxygen-evolving Enzyme of Thermosynechococcus elongatus
journal, May 2004

  • Boussac, Alain; Rappaport, Fabrice; Carrier, Patrick
  • Journal of Biological Chemistry, Vol. 279, Issue 22
  • DOI: 10.1074/jbc.M401677200

Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011

  • Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09913

Structure of Sr-substituted photosystem II at 2.1 A resolution and its implications in the mechanism of water oxidation
journal, February 2013

  • Koua, F. H. M.; Umena, Y.; Kawakami, K.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 10
  • DOI: 10.1073/pnas.1219922110

Electronic Structure of the Mn 4 O x Ca Cluster in the S 0 and S 2 States of the Oxygen-Evolving Complex of Photosystem II Based on Pulse 55 Mn-ENDOR and EPR Spectroscopy
journal, November 2007

  • Kulik, Leonid V.; Epel, Boris; Lubitz, Wolfgang
  • Journal of the American Chemical Society, Vol. 129, Issue 44
  • DOI: 10.1021/ja071487f

S 1 -State Model of the O 2 -Evolving Complex of Photosystem II
journal, July 2011

  • Luber, Sandra; Rivalta, Ivan; Umena, Yasufumi
  • Biochemistry, Vol. 50, Issue 29
  • DOI: 10.1021/bi200681q

X-ray damage to the Mn4Ca complex in single crystals of photosystem II: A case study for metalloprotein crystallography
journal, August 2005

  • Yano, J.; Kern, J.; Irrgang, K. -D.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue 34
  • DOI: 10.1073/pnas.0505207102

Entangled quantum electronic wavefunctions of the Mn4CaO5 cluster in photosystem II
journal, June 2013

  • Kurashige, Yuki; Chan, Garnet Kin-Lic; Yanai, Takeshi
  • Nature Chemistry, Vol. 5, Issue 8
  • DOI: 10.1038/nchem.1677

Oxygen-Evolving Mn Cluster in Photosystem II: The Protonation Pattern and Oxidation State in the High-Resolution Crystal Structure
journal, April 2012

  • Galstyan, Artur; Robertazzi, Arturo; Knapp, Ernst Walter
  • Journal of the American Chemical Society, Vol. 134, Issue 17
  • DOI: 10.1021/ja300254n

Structural models of the manganese complex of photosystem II and mechanistic implications
journal, January 2012

  • Grundmeier, Alexander; Dau, Holger
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.07.004

S 0 -State Model of the Oxygen-Evolving Complex of Photosystem II
journal, October 2013

  • Pal, Rhitankar; Negre, Christian F. A.; Vogt, Leslie
  • Biochemistry, Vol. 52, Issue 44
  • DOI: 10.1021/bi401214v

PSII manganese cluster: Protonation of W2, O5, O4 and His337 in the S1 state explored by combined quantum chemical and electrostatic energy computations
journal, August 2014

  • Robertazzi, Arturo; Galstyan, Artur; Knapp, Ernst Walter
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 8
  • DOI: 10.1016/j.bbabio.2014.03.018

Two Interconvertible Structures that Explain the Spectroscopic Properties of the Oxygen-Evolving Complex of Photosystem II in the S 2 State
journal, August 2012

  • Pantazis, Dimitrios A.; Ames, William; Cox, Nicholas
  • Angewandte Chemie International Edition, Vol. 51, Issue 39
  • DOI: 10.1002/anie.201204705

Electronic structure of the oxygen-evolving complex in photosystem II prior to O-O bond formation
journal, August 2014


Geometry optimization with QM/MM, ONIOM, and other combined methods. I. Microiterations and constraints
journal, April 2003

  • Vreven, Thom; Morokuma, Keiji; Farkas, Ödön
  • Journal of Computational Chemistry, Vol. 24, Issue 6
  • DOI: 10.1002/jcc.10156

Density‐functional thermochemistry. III. The role of exact exchange
journal, April 1993

  • Becke, Axel D.
  • The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652
  • DOI: 10.1063/1.464913

Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms Sc to Hg
journal, January 1985

  • Hay, P. Jeffrey; Wadt, Willard R.
  • The Journal of Chemical Physics, Vol. 82, Issue 1
  • DOI: 10.1063/1.448799

Ab initio effective core potentials for molecular calculations. Potentials for main group elements Na to Bi
journal, January 1985

  • Wadt, Willard R.; Hay, P. Jeffrey
  • The Journal of Chemical Physics, Vol. 82, Issue 1
  • DOI: 10.1063/1.448800

The influence of polarization functions on molecular orbital hydrogenation energies
journal, January 1973

  • Hariharan, P. C.; Pople, J. A.
  • Theoretica Chimica Acta, Vol. 28, Issue 3
  • DOI: 10.1007/BF00533485

Structural–Functional Role of Chloride in Photosystem II
journal, July 2011

  • Rivalta, Ivan; Amin, Muhamed; Luber, Sandra
  • Biochemistry, Vol. 50, Issue 29
  • DOI: 10.1021/bi200685w

Strontium EXAFS Reveals the Proximity of Calcium to the Manganese Cluster of Oxygen-Evolving Photosystem II
journal, October 1998

  • Cinco, Roehl M.; Robblee, John H.; Rompel, Annette
  • The Journal of Physical Chemistry B, Vol. 102, Issue 42
  • DOI: 10.1021/jp981658q

The Basic Properties of the Electronic Structure of the Oxygen-evolving Complex of Photosystem II Are Not Perturbed by Ca 2+ Removal
journal, May 2012

  • Lohmiller, Thomas; Cox, Nicholas; Su, Ji-Hu
  • Journal of Biological Chemistry, Vol. 287, Issue 29
  • DOI: 10.1074/jbc.M112.365288

Influence of the Ca 2+ ion on the Mn 4 Ca conformation and the H-bond network arrangement in Photosystem II
journal, January 2014

  • Saito, Keisuke; Ishikita, Hiroshi
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 1
  • DOI: 10.1016/j.bbabio.2013.09.013

The structure and activation of substrate water molecules in the S2 state of photosystem II studied by hyperfine sublevel correlation spectroscopy
journal, January 2012

  • Milikisiyants, Sergey; Chatterjee, Ruchira; Coates, Christopher S.
  • Energy & Environmental Science, Vol. 5, Issue 7
  • DOI: 10.1039/c2ee21210b

The structure and activation of substrate water molecules in Sr 2+ -substituted photosystem II
journal, January 2014

  • Chatterjee, Ruchira; Milikisiyants, Sergey; Coates, Christopher S.
  • Phys. Chem. Chem. Phys., Vol. 16, Issue 38
  • DOI: 10.1039/C4CP03082F

Oxygen-evolving complex of photosystem II: correlating structure with spectroscopy
journal, January 2014

  • Pokhrel, Ravi; Brudvig, Gary W.
  • Physical Chemistry Chemical Physics, Vol. 16, Issue 24
  • DOI: 10.1039/c4cp00493k

Effects of Sr 2+ -Substitution on the Reduction Rates of Y z in PSII MembranesEvidence for Concerted Hydrogen-Atom Transfer in Oxygen Evolution
journal, December 2000

  • Westphal, Kristi L.; Lydakis-Simantiris, Nikos; Cukier, Robert I.
  • Biochemistry, Vol. 39, Issue 51
  • DOI: 10.1021/bi0018077

Ca2+ determines the entropy changes associated with the formation of transition states during water oxidation by Photosystem II
journal, January 2011

  • Rappaport, Fabrice; Ishida, Naoko; Sugiura, Miwa
  • Energy & Environmental Science, Vol. 4, Issue 7
  • DOI: 10.1039/c1ee01408k

What does the Sr-substituted 2.1 Å resolution crystal structure of photosystem II reveal about the water oxidation mechanism?
journal, January 2014

  • Terrett, Richard; Petrie, Simon; Pace, Ron J.
  • Chem. Commun., Vol. 50, Issue 24
  • DOI: 10.1039/C3CC49324E

Reduced derivatives of the manganese cluster in the photosynthetic oxygen-evolving complex
journal, December 1992

  • Riggs, Pamela J.; Yocum, Charles F.; Penner-Hahn, James E.
  • Journal of the American Chemical Society, Vol. 114, Issue 26
  • DOI: 10.1021/ja00052a079

VMD: Visual molecular dynamics
journal, February 1996


Works referencing / citing this record:

Calcium and heterometallic manganese–calcium complexes supported by tripodal pyridine-carboxylate ligands: structural, EPR and theoretical investigations
journal, January 2015

  • Gerey, Bertrand; Gennari, Marcello; Gouré, Eric
  • Dalton Transactions, Vol. 44, Issue 28
  • DOI: 10.1039/c5dt01776a

Vibrational Analysis of Water Network Around the Mn Cluster
book, January 2020

  • Nakamura, Shin
  • Molecular Mechanisms of Proton-coupled Electron Transfer and Water Oxidation in Photosystem II
  • DOI: 10.1007/978-981-15-1584-2_4

Crystallographic Data Support the Carousel Mechanism of Water Supply to the Oxygen-Evolving Complex of Photosystem II
journal, September 2017