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Title: Roles of D1-Glu189 and D1-Glu329 in O2 Formation by the Water-Splitting Mn4Ca Cluster in Photosystem II

Abstract

During the catalytic step that precedes O–O bond formation in Photosystem II, a water molecule deprotonates and moves next to the water-splitting Mn4Ca cluster’s O5 oxo bridge. The relocated oxygen, known as O6 or Ox, may serve as a substrate, combining with O5 to form O2 during the final step in the catalytic cycle, or may be positioned to become a substrate during the next catalytic cycle. Recent serial femtosecond X-ray crystallographic studies show that the flexibility of D1-E189 plays a critical role in facilitating the relocation of O6/Ox. In this study, the D1-E189G and D1-E189S mutations were characterized with FTIR difference spectroscopy. The data show that both mutations support Mn4Ca cluster assembly, substantially inhibit advancement beyond the S2 state, and alter the network of H bonds that surrounds the Mn4Ca cluster. Previously, the D1-E189Q, D1-E189K, and D1-E189R mutations were shown to have little impact on the activity, electron transfer rates, or spectral properties of Photosystem II. A rationale for this behavior is presented. The residue D1-E329 interacts with water molecules in the O1 water network that has been suggested recently to supply substrate during the catalytic cycle. Characterization of the D1-E329A mutant with FTIR difference spectroscopy shows that thismore » mutation does not substantially perturb the structure of PSII or the water molecules whose O–H stretching modes change during the catalytic cycle. Furthermore, this result provides additional evidence that the water molecules whose vibrational properties change during the S1 to S2 transition are confined approximately to the region bounded by D1-N87, D1-N298, and D2-K317.« less

Authors:
 [1]; ORCiD logo [1]
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  1. Univ. of California, Riverside, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Riverside, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1785436
Grant/Contract Number:  
SC0005291
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 59; Journal Issue: 40; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Genetics; Fourier transform infrared spectroscopy; Molecules; Transition metals; Cluster chemistry

Citation Formats

Kim, Christopher J., and Debus, Richard J. Roles of D1-Glu189 and D1-Glu329 in O2 Formation by the Water-Splitting Mn4Ca Cluster in Photosystem II. United States: N. p., 2020. Web. doi:10.1021/acs.biochem.0c00541.
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Kim, Christopher J., & Debus, Richard J. Roles of D1-Glu189 and D1-Glu329 in O2 Formation by the Water-Splitting Mn4Ca Cluster in Photosystem II. United States. https://doi.org/10.1021/acs.biochem.0c00541
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Kim, Christopher J., and Debus, Richard J. Tue . "Roles of D1-Glu189 and D1-Glu329 in O2 Formation by the Water-Splitting Mn4Ca Cluster in Photosystem II". United States. https://doi.org/10.1021/acs.biochem.0c00541. https://www.osti.gov/servlets/purl/1785436.
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@article{osti_1785436,
title = {Roles of D1-Glu189 and D1-Glu329 in O2 Formation by the Water-Splitting Mn4Ca Cluster in Photosystem II},
author = {Kim, Christopher J. and Debus, Richard J.},
abstractNote = {During the catalytic step that precedes O–O bond formation in Photosystem II, a water molecule deprotonates and moves next to the water-splitting Mn4Ca cluster’s O5 oxo bridge. The relocated oxygen, known as O6 or Ox, may serve as a substrate, combining with O5 to form O2 during the final step in the catalytic cycle, or may be positioned to become a substrate during the next catalytic cycle. Recent serial femtosecond X-ray crystallographic studies show that the flexibility of D1-E189 plays a critical role in facilitating the relocation of O6/Ox. In this study, the D1-E189G and D1-E189S mutations were characterized with FTIR difference spectroscopy. The data show that both mutations support Mn4Ca cluster assembly, substantially inhibit advancement beyond the S2 state, and alter the network of H bonds that surrounds the Mn4Ca cluster. Previously, the D1-E189Q, D1-E189K, and D1-E189R mutations were shown to have little impact on the activity, electron transfer rates, or spectral properties of Photosystem II. A rationale for this behavior is presented. The residue D1-E329 interacts with water molecules in the O1 water network that has been suggested recently to supply substrate during the catalytic cycle. Characterization of the D1-E329A mutant with FTIR difference spectroscopy shows that this mutation does not substantially perturb the structure of PSII or the water molecules whose O–H stretching modes change during the catalytic cycle. Furthermore, this result provides additional evidence that the water molecules whose vibrational properties change during the S1 to S2 transition are confined approximately to the region bounded by D1-N87, D1-N298, and D2-K317.},
doi = {10.1021/acs.biochem.0c00541},
journal = {Biochemistry},
number = 40,
volume = 59,
place = {United States},
year = {Tue Sep 15 00:00:00 EDT 2020},
month = {Tue Sep 15 00:00:00 EDT 2020}
}
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Structural Effects of Ammonia Binding to the Mn 4 CaO 5 Cluster of Photosystem II
journal, January 2018

  • Marchiori, David A.; Oyala, Paul H.; Debus, Richard J.
  • The Journal of Physical Chemistry B, Vol. 122, Issue 5
  • DOI: 10.1021/acs.jpcb.7b11101

Assembly of the Photosystem II Oxygen-evolving Complex Is Inhibited in psbA Site-directed Mutants of Chlamydomonas reinhardtii
journal, January 1995

  • Whitelegge, Julian P.; Koo, Derrick; Diner, Bruce A.
  • Journal of Biological Chemistry, Vol. 270, Issue 1
  • DOI: 10.1074/jbc.270.1.225

Dual-Mode EPR Detects the Initial Intermediate in Photoassembly of the Photosystem II Mn Cluster:  The Influence of Amino Acid Residue 170 of the D1 Polypeptide on Mn Coordination
journal, April 2000

  • Campbell, Kristy A.; Force, Dee Ann; Nixon, Peter J.
  • Journal of the American Chemical Society, Vol. 122, Issue 15
  • DOI: 10.1021/ja000142t

Photoassembly of the Manganese Cluster in Mutants Perturbed in the High Affinity Mn-Binding Site of the H 2 O-Oxidation Complex of Photosystem II
journal, November 2007

  • Hwang, Hong Jin; McLain, Aaron; Debus, Richard J.
  • Biochemistry, Vol. 46, Issue 47
  • DOI: 10.1021/bi700761v

Does Aspartate 170 of the D1 Polypeptide Ligate the Manganese Cluster in Photosystem II? An EPR and ESEEM Study †
journal, September 2003

  • Debus, Richard J.; Aznar, Constantino; Campbell, Kristy A.
  • Biochemistry, Vol. 42, Issue 36
  • DOI: 10.1021/bi034859f

Identification of a Mn−O−Mn Cluster Vibrational Mode of the Oxygen-Evolving Complex in Photosystem II by Low-Frequency FTIR Spectroscopy
journal, November 2000

  • Chu, Hsiu-An; Sackett, Heather; Babcock, Gerald T.
  • Biochemistry, Vol. 39, Issue 47
  • DOI: 10.1021/bi001751g

Water-Sensitive Low-Frequency Vibrations of Reaction Intermediates during S-State Cycling in Photosynthetic Water Oxidation †
journal, May 2005

  • Kimura, Yukihiro; Ishii, Asako; Yamanari, Toshihiro
  • Biochemistry, Vol. 44, Issue 21
  • DOI: 10.1021/bi048203d

The manganese and calcium ions of photosynthetic oxygen evolution
journal, October 1992

Pulsed and Parallel-Polarization EPR Characterization of the Photosystem II Oxygen-Evolving Complex
journal, June 2000

  • Britt, R. David; Peloquin, Jeffrey M.; Campbell, Kristy A.
  • Annual Review of Biophysics and Biomolecular Structure, Vol. 29, Issue 1
  • DOI: 10.1146/annurev.biophys.29.1.463

The infrared absorption of amino acid side chains
journal, January 2000

FTIR Detection of Water Reactions during the Flash-Induced S-State Cycle of the Photosynthetic Water-Oxidizing Complex †
journal, December 2002

  • Noguchi, Takumi; Sugiura, Miwa
  • Biochemistry, Vol. 41, Issue 52
  • DOI: 10.1021/bi020603i
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