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 »
- Authors:
-
- 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.
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
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.
@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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- Chu, Hsiu-An; Nguyen, Anh P.; Debus, Richard J.
- Biochemistry, Vol. 33, Issue 20
Flash-Induced FTIR Difference Spectra of the Water Oxidizing Complex in Moderately Hydrated Photosystem II Core Films: Effect of Hydration Extent on S-State Transitions †
journal, February 2002
- Noguchi, Takumi; Sugiura, Miwa
- Biochemistry, Vol. 41, Issue 7
Impact of D1-V185 on the Water Molecules That Facilitate O 2 Formation by the Catalytic Mn 4 CaO 5 Cluster in Photosystem II
journal, June 2018
- Kim, Christopher J.; Bao, Han; Burnap, Robert L.
- Biochemistry, Vol. 57, Issue 29
Role of D1-His190 in Proton-Coupled Electron Transfer Reactions in Photosystem II: A Chemical Complementation Study †
journal, August 1998
- Hays, Anna-Maria A.; Vassiliev, Ilya R.; Golbeck, John H.
- Biochemistry, Vol. 37, Issue 32
Structural Coupling between the Oxygen-Evolving Mn Cluster and a Tyrosine Residue in Photosystem II As Revealed by Fourier Transform Infrared Spectroscopy †
journal, December 1997
- Noguchi, Takumi; Inoue, Yorinao; Tang, Xiao-Song
- Biochemistry, Vol. 36, Issue 48
Fourier Transform Infrared Difference Spectroscopy of Photosystem II Tyrosine D Using Site-Directed Mutagenesis and Specific Isotope Labeling †
journal, December 1997
- Hienerwadel, Rainer; Boussac, Alain; Breton, Jacques
- Biochemistry, Vol. 36, Issue 48
Evidence that the C-Terminus of the D1 Polypeptide of Photosystem II is Ligated to the Manganese Ion that Undergoes Oxidation During the S 1 to S 2 Transition: An Isotope-Edited FTIR Study †
journal, March 2004
- Chu, Hsiu-An; Hillier, Warwick; Debus, Richard J.
- Biochemistry, Vol. 43, Issue 11
Water Molecules Coupled to the Redox-Active Tyrosine Y D in Photosystem II as Detected by FTIR Spectroscopy
journal, November 2007
- Takahashi, Ryouta; Sugiura, Miwa; Noguchi, Takumi
- Biochemistry, Vol. 46, Issue 49
Directed alteration of the D1 polypeptide of photosystem II: evidence that tyrosine-161 is the redox component, Z, connecting the oxygen-evolving complex to the primary electron donor, P680
journal, August 1989
- Metz, James G.; Nixon, Peter J.; Rogner, Matthias
- Biochemistry, Vol. 28, Issue 17
Structure of a Histidine Ligand in the Photosynthetic Oxygen-Evolving Complex As Studied by Light-Induced Fourier Transform Infrared Difference Spectroscopy
journal, July 1999
- Noguchi, Takumi; Inoue, Yorinao; Tang, Xiao-Song
- Biochemistry, Vol. 38, Issue 31
Infrared Determination of the Protonation State of a Key Histidine Residue in the Photosynthetic Water Oxidizing Center
journal, June 2017
- Nakamura, Shin; Noguchi, Takumi
- Journal of the American Chemical Society, Vol. 139, Issue 27
Participation of Glutamate-354 of the CP43 Polypeptide in the Ligation of Manganese and the Binding of Substrate Water in Photosystem II
journal, January 2011
- Service, Rachel J.; Yano, Junko; McConnell, Iain
- Biochemistry, Vol. 50, Issue 1
Mutation of Lysine 317 in the D2 Subunit of Photosystem II Alters Chloride Binding and Proton Transport
journal, July 2013
- Pokhrel, Ravi; Service, Rachel J.; Debus, Richard J.
- Biochemistry, Vol. 52, Issue 28
Fourier transform infrared and mass spectrometry analyses of a site-directed mutant of D1-Asp170 as a ligand to the water-oxidizing Mn4CaO5 cluster in photosystem II
journal, January 2020
- Kitajima-Ihara, Tomomi; Suzuki, Takehiro; Nakamura, Shin
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 1
Analysis of Flash-Induced FTIR Difference Spectra of the S-State Cycle in the Photosynthetic Water-Oxidizing Complex by Uniform 15 N and 13 C Isotope Labeling †
journal, May 2003
- Noguchi, Takumi; Sugiura, Miwa
- Biochemistry, Vol. 42, Issue 20
Changes of Low-Frequency Vibrational Modes Induced by Universal 15 N- and 13 C-Isotope Labeling in S 2 /S 1 FTIR Difference Spectrum of Oxygen-Evolving Complex †
journal, November 2003
- Kimura, Yukihiro; Mizusawa, Naoki; Ishii, Asako
- Biochemistry, Vol. 42, Issue 45
Mid- to Low-Frequency Fourier Transform Infrared Spectra of S-State Cycle for Photosynthetic Water Oxidation in Synechocystis sp. PCC 6803 †
journal, June 2004
- Yamanari, Toshihiro; Kimura, Yukihiro; Mizusawa, Naoki
- Biochemistry, Vol. 43, Issue 23
Evidence from Biosynthetically Incorporated Strontium and FTIR Difference Spectroscopy that the C-Terminus of the D1 Polypeptide of Photosystem II Does Not Ligate Calcium †
journal, June 2005
- Strickler, Melodie A.; Walker, Lee M.; Hillier, Warwick
- Biochemistry, Vol. 44, Issue 24
Structural Perturbation of the Carboxylate Ligands to the Manganese Cluster upon Ca 2+ /Sr 2+ Exchange in the S-State Cycle of Photosynthetic Oxygen Evolution As Studied by Flash-Induced FTIR Difference Spectroscopy
journal, October 2006
- Suzuki, Hiroyuki; Taguchi, Yuta; Sugiura, Miwa
- Biochemistry, Vol. 45, Issue 45
Calcium Exchange and Structural Changes during the Photosynthetic Oxygen Evolving Cycle
journal, September 2006
- De Riso, Antonio; Jenson, David L.; Barry, Bridgette A.
- Biophysical Journal, Vol. 91, Issue 5
Calcium, Strontium, and Protein Dynamics during the S 2 to S 3 Transition in the Photosynthetic Oxygen-Evolving Cycle
journal, September 2013
- Polander, Brandon C.; Barry, Bridgette A.
- The Journal of Physical Chemistry Letters, Vol. 4, Issue 19
Theoretical Evaluation of Structural Models of the S 2 State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions
journal, December 2011
- Ames, William; Pantazis, Dimitrios A.; Krewald, Vera
- Journal of the American Chemical Society, Vol. 133, Issue 49
Ligation of D1-His332 and D1-Asp170 to the Manganese Cluster of Photosystem II from Synechocystis Assessed by Multifrequency Pulse EPR Spectroscopy †
journal, August 2011
- Stich, Troy A.; Yeagle, Gregory J.; Service, Rachel J.
- Biochemistry, Vol. 50, Issue 34
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
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
Aspartate 170 of the photosystem II reaction center polypeptide D1 is involved in the assembly of the oxygen-evolving manganese cluster
journal, January 1992
- Nixon, Peter J.; Diner, Bruce A.
- Biochemistry, Vol. 31, Issue 3
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
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
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
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
D1-Asp170 Is Structurally Coupled to the Oxygen Evolving Complex in Photosystem II As Revealed by Light-Induced Fourier Transform Infrared Difference Spectroscopy †
journal, February 2001
- Chu, Hsiu-An; Debus, Richard J.; Babcock, Gerald T.
- Biochemistry, Vol. 40, Issue 7
No Evidence from FTIR Difference Spectroscopy That Aspartate-170 of the D1 Polypeptide Ligates a Manganese Ion That Undergoes Oxidation during the S 0 to S 1 , S 1 to S 2 , or S 2 to S 3 Transitions in Photosystem II †
journal, February 2005
- Debus, Richard J.; Strickler, Melodie A.; Walker, Lee M.
- Biochemistry, Vol. 44, Issue 5
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
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
Amino Acid Residues That Influence the Binding of Manganese or Calcium to Photosystem II. 2. The Carboxy-Terminal Domain of the D1 Polypeptide
journal, May 1995
- Chu, Hsiu-An; Nguyen, Anh P.; Debus, Richard J.
- Biochemistry, Vol. 34, Issue 17
Proton Release Process during the S 2 -to-S 3 Transition of Photosynthetic Water Oxidation As Revealed by the pH Dependence of Kinetics Monitored by Time-Resolved Infrared Spectroscopy
journal, September 2019
- Takemoto, Hiroshi; Sugiura, Miwa; Noguchi, Takumi
- Biochemistry, Vol. 58, Issue 42
The manganese and calcium ions of photosynthetic oxygen evolution
journal, October 1992
- Debus, Richard J.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1102, Issue 3
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
The infrared absorption of amino acid side chains
journal, January 2000
- Barth, Andreas
- Progress in Biophysics and Molecular Biology, Vol. 74, Issue 3-5
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