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Title: Substitution of the D1-Asn 87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II

Abstract

Photoinduced water oxidation at the O 2-evolving complex (OEC) of photosystem II (PSII) is a complex process involving a tetramanganese-calcium cluster that is surrounded by a hydrogen-bonded network of water molecules, chloride ions, and amino acid residues. Although the structure of the OEC has remained conserved over eons of evolution, significant differences in the chloride-binding characteristics exist between cyanobacteria and higher plants. An analysis of amino acid residues in and around the OEC has identified residue 87 in the D1 subunit as the only significant difference between PSII in cyanobacteria and higher plants. We substituted the D1-Asn 87 residue in the cyanobacterium Synechocystis sp. PCC 6803 (wildtype) with alanine, present in higher plants, or with aspartic acid. We studied PSII core complexes purified from D1-N87A and D1-N87D variant strains to probe the function of the D1-Asn 87 residue in the water-oxidation mechanism. EPR spectra of the S 2 state and flash-induced FTIR spectra of both D1-N87A and D1-N87D PSII core complexes exhibited characteristics similar to those of wildtype Synechocystis PSII core complexes. However, flash-induced O 2-evolution studies revealed a decreased cycling efficiency of the D1-N87D variant, whereas the cycling efficiency of the D1-N87A PSII variant was similar to that ofmore » wildtype PSII. Steady-state O 2-evolution activity assays revealed that substitution of the D1 residue at position 87 with alanine perturbs the chloride-binding site in the proton-exit channel. Finally, these findings provide new insight into the role of the D1-Asn 87 site in the water-oxidation mechanism and explain the difference in the chloride-binding properties of cyanobacterial and higher-plant PSII.« less

Authors:
 [1];  [1];  [2]; ORCiD logo [2]; ORCiD logo [1]
  1. Yale Univ., New Haven, CT (United States). Dept. of Chemistry
  2. Univ. of California, Riverside, CA (United States). Dept. of Biochemistry
Publication Date:
Research Org.:
Yale Univ., New Haven, CT (United States); Univ. of California, Riverside, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1540308
Grant/Contract Number:  
FG02-05ER15646; SC0005291
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 293; Journal Issue: 7; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; biochemistry & molecular biology; cyanobacteria; photosynthesis; photosystem II; proton transport; water channel

Citation Formats

Banerjee, Gourab, Ghosh, Ipsita, Kim, Christopher J., Debus, Richard J., and Brudvig, Gary W. Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II. United States: N. p., 2017. Web. doi:10.1074/jbc.m117.813170.
Banerjee, Gourab, Ghosh, Ipsita, Kim, Christopher J., Debus, Richard J., & Brudvig, Gary W. Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II. United States. doi:10.1074/jbc.m117.813170.
Banerjee, Gourab, Ghosh, Ipsita, Kim, Christopher J., Debus, Richard J., and Brudvig, Gary W. Wed . "Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II". United States. doi:10.1074/jbc.m117.813170. https://www.osti.gov/servlets/purl/1540308.
@article{osti_1540308,
title = {Substitution of the D1-Asn87 site in photosystem II of cyanobacteria mimics the chloride-binding characteristics of spinach photosystem II},
author = {Banerjee, Gourab and Ghosh, Ipsita and Kim, Christopher J. and Debus, Richard J. and Brudvig, Gary W.},
abstractNote = {Photoinduced water oxidation at the O2-evolving complex (OEC) of photosystem II (PSII) is a complex process involving a tetramanganese-calcium cluster that is surrounded by a hydrogen-bonded network of water molecules, chloride ions, and amino acid residues. Although the structure of the OEC has remained conserved over eons of evolution, significant differences in the chloride-binding characteristics exist between cyanobacteria and higher plants. An analysis of amino acid residues in and around the OEC has identified residue 87 in the D1 subunit as the only significant difference between PSII in cyanobacteria and higher plants. We substituted the D1-Asn87 residue in the cyanobacterium Synechocystis sp. PCC 6803 (wildtype) with alanine, present in higher plants, or with aspartic acid. We studied PSII core complexes purified from D1-N87A and D1-N87D variant strains to probe the function of the D1-Asn87 residue in the water-oxidation mechanism. EPR spectra of the S2 state and flash-induced FTIR spectra of both D1-N87A and D1-N87D PSII core complexes exhibited characteristics similar to those of wildtype Synechocystis PSII core complexes. However, flash-induced O2-evolution studies revealed a decreased cycling efficiency of the D1-N87D variant, whereas the cycling efficiency of the D1-N87A PSII variant was similar to that of wildtype PSII. Steady-state O2-evolution activity assays revealed that substitution of the D1 residue at position 87 with alanine perturbs the chloride-binding site in the proton-exit channel. Finally, these findings provide new insight into the role of the D1-Asn87 site in the water-oxidation mechanism and explain the difference in the chloride-binding properties of cyanobacterial and higher-plant PSII.},
doi = {10.1074/jbc.m117.813170},
journal = {Journal of Biological Chemistry},
number = 7,
volume = 293,
place = {United States},
year = {2017},
month = {12}
}

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Works referenced in this record:

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

Identification of FTIR Bands Due to Internal Water Molecules around the Quinone Binding Sites in the Reaction Center from Rhodobacter sphaeroides
journal, February 2009

  • Iwata, Tatsuya; Paddock, Mark L.; Okamura, Melvin Y.
  • Biochemistry, Vol. 48, Issue 6
  • DOI: 10.1021/bi801990s

Energetics of the S 2 State Spin Isomers of the Oxygen-Evolving Complex of Photosystem II
journal, January 2017

  • Vinyard, David J.; Khan, Sahr; Askerka, Mikhail
  • The Journal of Physical Chemistry B, Vol. 121, Issue 5
  • DOI: 10.1021/acs.jpcb.7b00110

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
  • DOI: 10.1021/bi0362323

The chloride requirement for photosynthetic oxygen evolution. Analysis of the effects of chloride and other anions on amine inhibition of the oxygen-evolving complex
journal, September 1984

  • Sandusky, Peter O.; Yocum, Charles F.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 766, Issue 3
  • DOI: 10.1016/0005-2728(84)90121-X

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

Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations
journal, September 2012

  • Vassiliev, Sergey; Zaraiskaya, Tatiana; Bruce, Doug
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 9
  • DOI: 10.1016/j.bbabio.2012.05.016

Structure of an Active Water Molecule in the Water-Oxidizing Complex of Photosystem II As Studied by FTIR Spectroscopy
journal, September 2000

  • Noguchi, Takumi; Sugiura, Miwa
  • Biochemistry, Vol. 39, Issue 36
  • DOI: 10.1021/bi001040i

Proton transfer via a transient linear water-molecule chain in a membrane protein
journal, June 2011

  • Freier, E.; Wolf, S.; Gerwert, K.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 28
  • DOI: 10.1073/pnas.1104735108

Effects of Ammonia on the Structure of the Oxygen-Evolving Complex in Photosystem II As Revealed by Light-Induced FTIR Difference Spectroscopy
journal, November 2011

  • Hou, Li-Hsiu; Wu, Chia-Ming; Huang, Hsin-Ho
  • Biochemistry, Vol. 50, Issue 43
  • DOI: 10.1021/bi200943q

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

EPR evidence for a modified S-state transition in chloride-depleted Photosystem II
journal, September 1986

  • Ono, T.; Zimmermann, J. L.; Inoue, Y.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 851, Issue 2
  • DOI: 10.1016/0005-2728(86)90125-8

Water in Photosystem II: Structural, functional and mechanistic considerations
journal, January 2014


Participation of Glutamate-333 of the D1 Polypeptide in the Ligation of the Mn 4 CaO 5 Cluster in Photosystem II
journal, November 2013

  • Service, Rachel J.; Yano, Junko; Dilbeck, Preston L.
  • Biochemistry, Vol. 52, Issue 47
  • DOI: 10.1021/bi401339f

Monitoring the reactions of photosynthetic water oxidation using infrared spectroscopy
journal, January 2013

  • Noguchi, Takumi
  • Biomedical Spectroscopy and Imaging, Vol. 2, Issue 2
  • DOI: 10.3233/BSI-130040

Direct Observation of the Bridged Water Stretching Vibrations Inside a Protein
journal, November 2000

  • Kandori, Hideki; Shichida, Yoshinori
  • Journal of the American Chemical Society, Vol. 122, Issue 47
  • DOI: 10.1021/ja0032069

FTIR detection of water reactions in the oxygen-evolving centre of photosystem II
journal, October 2007

  • Noguchi, Takumi
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1494
  • DOI: 10.1098/rstb.2007.2214

The chloride requirement for photosynthetic oxygen evolution: Factors affecting nucleophilic displacement of chloride from the oxygen-evolving complex
journal, April 1986


Insights into Substrate Binding to the Oxygen-Evolving Complex of Photosystem II from Ammonia Inhibition Studies
journal, December 2014

  • Vinyard, David J.; Brudvig, Gary W.
  • Biochemistry, Vol. 54, Issue 2
  • DOI: 10.1021/bi5014134

Properties of the Chloride-Depleted Oxygen-Evolving Complex of Photosystem II Studied by Electron Paramagnetic Resonance
journal, January 1996

  • van Vliet, Pieter; Rutherford, A. William
  • Biochemistry, Vol. 35, Issue 6
  • DOI: 10.1021/bi9514471

Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks
journal, April 2015


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
  • DOI: 10.1021/bi301700u

Water molecule reorganization in cytochrome c oxidase revealed by FTIR spectroscopy
journal, May 2011

  • Marechal, A.; Rich, P. R.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 21
  • DOI: 10.1073/pnas.1019419108

Functional waters in intraprotein proton transfer monitored by FTIR difference spectroscopy
journal, November 2005


A One-Site, Two-State Model for the Binding of Anions in Photosystem II
journal, January 1996

  • Lindberg, Katrin; Andréasson, Lars-Erik
  • Biochemistry, Vol. 35, Issue 45
  • DOI: 10.1021/bi961244s

Active and resting states of the oxygen-evolving complex of photosystem II
journal, June 1985

  • Beck, Warren F.; De Paula, Julio C.; Brudvig, Gary W.
  • Biochemistry, Vol. 24, Issue 12
  • DOI: 10.1021/bi00333a035

Competitive Binding of Acetate and Chloride in Photosystem II
journal, May 1999

  • Kühne, Henriette; Szalai, Veronika A.; Brudvig, Gary W.
  • Biochemistry, Vol. 38, Issue 20
  • DOI: 10.1021/bi990341t

Fourier transform infrared analysis of the photosynthetic oxygen-evolving center
journal, February 2008


Network of Hydrogen Bonds near the Oxygen-Evolving Mn 4 CaO 5 Cluster of Photosystem II Probed with FTIR Difference Spectroscopy
journal, February 2014

  • Service, Rachel J.; Hillier, Warwick; Debus, Richard J.
  • Biochemistry, Vol. 53, Issue 6
  • DOI: 10.1021/bi401450y

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
  • DOI: 10.1021/bi1015937

Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses
journal, November 2014

  • Suga, Michihiro; Akita, Fusamichi; Hirata, Kunio
  • Nature, Vol. 517, Issue 7532
  • DOI: 10.1038/nature13991

Probing the role of chloride in Photosystem II from Thermosynechococcus elongatus by exchanging chloride for iodide
journal, May 2012

  • Boussac, Alain; Ishida, Naoko; Sugiura, Miwa
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 5
  • DOI: 10.1016/j.bbabio.2012.02.031

Azide as a Probe of Proton Transfer Reactions in Photosynthetic Oxygen Evolution
journal, December 2008


Studies of the slowly exchanging chloride in Photosystem II of higher plants
journal, January 1993

  • Lindberg, Katrin; V�nng�rd, Tore; Andr�asson, Lars-Erik
  • Photosynthesis Research, Vol. 38, Issue 3
  • DOI: 10.1007/BF00046767

FTIR studies of metal ligands, networks of hydrogen bonds, and water molecules near the active site Mn4CaO5 cluster in Photosystem II
journal, January 2015


Probing the Effect of Mutations of Asparagine 181 in the D1 Subunit of Photosystem II
journal, February 2015

  • Pokhrel, Ravi; Debus, Richard J.; Brudvig, Gary W.
  • Biochemistry, Vol. 54, Issue 8
  • DOI: 10.1021/bi501468h

Role of internal water molecules in bacteriorhodopsin
journal, August 2000


Q-Band EPR of the S2 State of Photosystem II Confirms an S=5/2 Origin of the X-Band g=4.1 Signal
journal, October 2004


Thermodynamically accurate modeling of the catalytic cycle of photosynthetic oxygen evolution: A mathematical solution to asymmetric Markov chains
journal, July 2013

  • Vinyard, David J.; Zachary, Chase E.; Ananyev, Gennady
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 7
  • DOI: 10.1016/j.bbabio.2013.04.008

Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access
journal, February 2008

  • Ho, Felix M.; Styring, Stenbjörn
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 2
  • DOI: 10.1016/j.bbabio.2007.08.009

Does Histidine 332 of the D1 Polypeptide Ligate the Manganese Cluster in Photosystem II? An Electron Spin Echo Envelope Modulation Study
journal, March 2001

  • Debus, Richard J.; Campbell, Kristy A.; Gregor, Wolfgang
  • Biochemistry, Vol. 40, Issue 12
  • DOI: 10.1021/bi002394c

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


Time-Resolved Infrared Detection of the Proton and Protein Dynamics during Photosynthetic Oxygen Evolution
journal, April 2012

  • Noguchi, Takumi; Suzuki, Hiroyuki; Tsuno, Masaya
  • Biochemistry, Vol. 51, Issue 15
  • DOI: 10.1021/bi300294n

Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water
journal, January 1981

  • Dismukes, G. C.; Siderer, Y.
  • Proceedings of the National Academy of Sciences, Vol. 78, Issue 1
  • DOI: 10.1073/pnas.78.1.274

A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties
journal, November 1981