Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II

Zhang, Miao; Bommer, Martin; Chatterjee, Ruchira; Hussein, Rana; Yano, Junko; Dau, Holger; Kern, Jan; Dobbek, Holger; Zouni, Athina

doi:10.7554/eLife.26933

Title: Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn₄CaO₅-cluster in photosystem II

Abstract

In plants, algae and cyanobacteria, Photosystem II (PSII) catalyzes the light-driven splitting of water at a protein-bound Mn₄CaO₅-cluster, the water-oxidizing complex (WOC). In the photosynthetic organisms, the light-driven formation of the WOC from dissolved metal ions is a key process because it is essential in both initial activation and continuous repair of PSII. Structural information is required for understanding of this chaperone-free metal-cluster assembly. For the first time, we obtained a structure of PSII from Thermosynechococcus elongatus without the Mn₄CaO₅-cluster. Surprisingly, cluster-removal leaves the positions of all coordinating amino acid residues and most nearby water molecules largely unaffected, resulting in a pre-organized ligand shell for kinetically competent and error-free photo-assembly of the Mn₄CaO₅-cluster. First experiments initiating (i) partial disassembly and (ii) partial re-assembly after complete depletion of the Mn4CaO5-cluster agree with a specific bi-manganese cluster, likely a di-µ-oxo bridged pair of Mn(III) ions, as an assembly intermediate.

Authors:

^[1]; Bommer, Martin ^[1]; Chatterjee, Ruchira ^[2]; Hussein, Rana ^[1]; Yano, Junko ^[2]; Dau, Holger ^[3]; Kern, Jan ^[2];

^[1];

^[1]

Humboldt Univ. of Berlin (Germany). Inst. of Biology
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Freie Univ., Berlin (Germany)

Publication Date:: Tue Jul 18 00:00:00 EDT 2017

Research Org.:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1408448

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Accepted Manuscript

Journal Name:: eLife

Additional Journal Information:: Journal Volume: 6; Journal ID: ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.

Country of Publication:: United States

Language:: English

Subject:: 60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Zhang, Miao, Bommer, Martin, Chatterjee, Ruchira, Hussein, Rana, Yano, Junko, Dau, Holger, Kern, Jan, Dobbek, Holger, and Zouni, Athina. Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II.  United States: N. p., 2017. 
Web.  doi:10.7554/eLife.26933.

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                    Zhang, Miao, Bommer, Martin, Chatterjee, Ruchira, Hussein, Rana, Yano, Junko, Dau, Holger, Kern, Jan, Dobbek, Holger, & Zouni, Athina. Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II.  United States.  https://doi.org/10.7554/eLife.26933

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                    Zhang, Miao, Bommer, Martin, Chatterjee, Ruchira, Hussein, Rana, Yano, Junko, Dau, Holger, Kern, Jan, Dobbek, Holger, and Zouni, Athina. Tue .  
"Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II".  United States.  https://doi.org/10.7554/eLife.26933.  https://www.osti.gov/servlets/purl/1408448.

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@article{osti_1408448,

  title        = {Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II},

  author       = {Zhang, Miao and Bommer, Martin and Chatterjee, Ruchira and Hussein, Rana and Yano, Junko and Dau, Holger and Kern, Jan and Dobbek, Holger and Zouni, Athina},

  abstractNote = {In plants, algae and cyanobacteria, Photosystem II (PSII) catalyzes the light-driven splitting of water at a protein-bound Mn4CaO5-cluster, the water-oxidizing complex (WOC). In the photosynthetic organisms, the light-driven formation of the WOC from dissolved metal ions is a key process because it is essential in both initial activation and continuous repair of PSII. Structural information is required for understanding of this chaperone-free metal-cluster assembly. For the first time, we obtained a structure of PSII from Thermosynechococcus elongatus without the Mn4CaO5-cluster. Surprisingly, cluster-removal leaves the positions of all coordinating amino acid residues and most nearby water molecules largely unaffected, resulting in a pre-organized ligand shell for kinetically competent and error-free photo-assembly of the Mn4CaO5-cluster. First experiments initiating (i) partial disassembly and (ii) partial re-assembly after complete depletion of the Mn4CaO5-cluster agree with a specific bi-manganese cluster, likely a di-µ-oxo bridged pair of Mn(III) ions, as an assembly intermediate.},

  doi          = {10.7554/eLife.26933},

  journal      = {eLife},

  number       = ,

  volume       = 6,

  place        = {United States},

  year         = {Tue Jul 18 00:00:00 EDT 2017},

  month        = {Tue Jul 18 00:00:00 EDT 2017}

}

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One of the Substrate Waters for O₂ Formation in Photosystem II Is Provided by the Water-Splitting Mn₄CaO₅ Cluster’s Ca²⁺ Ion

Journal Article Kim, Christopher J. ; Debus, Richard J. - Biochemistry

During the catalytic step immediately prior to O–O bond formation in Photosystem II, a water molecule deprotonates and moves next to the water-splitting Mn₄CaO₅ cluster’s O5 oxo bridge. Considerable evidence identifies O5 as one of the two substrate waters that ultimately form O₂. The relocated oxygen, known as O6 or Ox, may be the second. It is currently debated whether O6 or Ox originates as the Mn-bound water denoted W2 or as the Ca²⁺-bound water denoted W3. To distinguish between these two possibilities, we analyzed the D–O–D bending mode of the water molecule that deprotonates/relocates to become O6/Ox. Here, wemore »« less
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https://doi.org/10.1021/acs.biochem.9b00418

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Title: Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn4CaO5-cluster in photosystem II

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Photosystem II repair in plant chloroplasts — Regulation, assisting proteins and shared components with photosystem II biogenesis journal, September 2015

Linking Crystallographic Model and Data Quality journal, May 2012

Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal journal, November 2014

Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution journal, May 2016

Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 journal, August 1970

Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster journal, May 2010

Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride journal, February 2009

Water-Splitting Chemistry of Photosystem II journal, November 2006

Photoactivation: The Light-Driven Assembly of the Water Oxidation Complex of Photosystem II journal, May 2016

Analysis of photosystem II biogenesis in cyanobacteria journal, March 2016

Location of the High-Affinity Mn 2+ Site in Photosystem II Detected by PELDOR journal, July 2015

Towards automated crystallographic structure refinement with phenix.refine journal, March 2012

Reflections on substrate water and dioxygen formation journal, August 2013

Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II journal, December 2005

Photosystem II Assembly: From Cyanobacteria to Plants journal, April 2013

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

Calcium Induces Binding and Formation of a Spin-Coupled Dimanganese(II,II) Center in the Apo-Water Oxidation Complex of Photosystem II as Precursor to the Functional Tetra-Mn/Ca Cluster † journal, September 1997

XDSAPP : a graphical user interface for the convenient processing of diffraction data using XDS journal, April 2012

Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin journal, March 2012

Highly Purified Thermo-Stable Oxygen-Evolving Photosystem II Core Complex from the Thermophilic Cyanobacterium Synechococcus elongatus Having His-Tagged CP43 journal, January 1999

XDS journal, January 2010

Recent advances in understanding the assembly and repair of photosystem II journal, March 2010

Light-induced quinone reduction in photosystem II journal, January 2012

Stepwise Transition of the Tetra-Manganese Complex of Photosystem II to a Binuclear Mn2(μ-O)2 Complex in Response to a Temperature Jump: A Time-Resolved Structural Investigation Employing X-Ray Absorption Spectroscopy journal, February 2003

Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG journal, April 2010

The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis journal, April 2015

Architecture of the Photosynthetic Oxygen-Evolving Center journal, March 2004

Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor journal, January 2005

Structure of photosystem II and substrate binding at room temperature journal, November 2016

Calcium Modulates the Photo-assembly of Photosystem II (Mn)4-Clusters by Preventing Ligation of Nonfunctional High-Valency States of Manganese journal, October 1995

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

X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution journal, December 1998

Improved R-factors for diffraction data analysis in macromolecular crystallography journal, April 1997

MolProbity : all-atom structure validation for macromolecular crystallography journal, December 2009

Mn 4 Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen journal, March 2014

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

Features and development of Coot journal, March 2010

Intermediates in Assembly by Photoactivation after Thermally Accelerated Disassembly of the Manganese Complex of Photosynthetic Water Oxidation † journal, December 2006

Photoactivation of the manganese catalyst of O2 evolution. I. Biochemical and kinetic aspects journal, November 1971

Spare quinones in the QB cavity of crystallized photosystem II from Thermosynechococcus elongatus journal, June 2007

The extrinsic proteins of Photosystem II journal, January 2012

Structure of a Cofactor-Deficient Nitrogenase MoFe Protein journal, April 2002

Aromatic structure of Tyrosine-92 in the extrinsic PsbU protein of red algal Photosystem II is important for its functioning journal, October 2007

Comparison of chloride-depleted and calcium-depleted PSII: the midpoint potential of QA and susceptibility to photodamage journal, March 1997

Assembly of the water-oxidizing complex in photosystem II journal, July 2011

Assembly of nonheme Mn/Fe active sites in heterodinuclear metalloproteins journal, April 2014

Evidence for Interstitial Carbon in Nitrogenase FeMo Cofactor journal, November 2011

Conformational Changes in Photosystem II Supercomplexes upon Removal of Extrinsic Subunits † journal, October 2000

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection journal, October 2016

Two tyrosines that changed the world: Interfacing the oxidizing power of photochemistry to water splitting in photosystem II journal, January 2012

Redox potentials of primary electron acceptor quinone molecule (QA)- and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d journal, April 2011

Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center journal, January 1999

The solvent component of macromolecular crystals journal, April 2015

Two Different Structures of the Oxygen-Evolving Complex in the Same Polypeptide Frameworks of Photosystem II journal, January 2017

Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution journal, February 2001

Photoassembly of the water-oxidizing complex in photosystem II journal, February 2008

Investigating the Structure and Dynamics of Apo‐Photosystem II journal, June 2019

O2 evolution and recovery of the water-oxidizing enzyme journal, March 2018

Calcium, conformational selection, and redox-active tyrosine YZ in the photosynthetic oxygen-evolving cluster journal, May 2018

A novel chlorophyll protein complex in the repair cycle of photosystem II journal, October 2019

Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions journal, September 2019

Assessment of the manganese cluster’s oxidation state via photoactivation of photosystem II microcrystals journal, December 2019

Surface-grafted lanthanoid complexes of the tungstosilicate polyanion [SiW 12 O 40 ] 4− : a synthetic, structural and computational investigation journal, October 2018

Structural Changes in the Acceptor Site of Photosystem II upon Ca2+/Sr2+ Exchange in the Mn4CaO5 Cluster Site and the Possible Long-Range Interactions journal, August 2019

Investigating the Structure and Dynamics of Apo‐Photosystem II text, January 2019

Structural changes in the acceptor site of photosystem II upon Ca$^{2+}$/Sr$^{2+}$ exchange in the Mn$_4$CaO$_5$ Cluster Site and the Possible Long-Range Interactions text, January 2019

Title: Structural insights into the light-driven auto-assembly process of the water-oxidizing Mn₄CaO₅-cluster in photosystem II

Photosystem II repair in plant chloroplasts — Regulation, assisting proteins and shared components with photosystem II biogenesis
journal, September 2015

Linking Crystallographic Model and Data Quality
journal, May 2012

Native-like Photosystem II Superstructure at 2.44 Å Resolution through Detergent Extraction from the Protein Crystal
journal, November 2014

Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution
journal, May 2016

Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
journal, August 1970

Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster
journal, May 2010

Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride
journal, February 2009

Water-Splitting Chemistry of Photosystem II
journal, November 2006

Photoactivation: The Light-Driven Assembly of the Water Oxidation Complex of Photosystem II
journal, May 2016

Analysis of photosystem II biogenesis in cyanobacteria
journal, March 2016

Location of the High-Affinity Mn ²⁺ Site in Photosystem II Detected by PELDOR
journal, July 2015

Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

Reflections on substrate water and dioxygen formation
journal, August 2013

Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II
journal, December 2005

Photosystem II Assembly: From Cyanobacteria to Plants
journal, April 2013

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

Calcium Induces Binding and Formation of a Spin-Coupled Dimanganese(II,II) Center in the Apo-Water Oxidation Complex of Photosystem II as Precursor to the Functional Tetra-Mn/Ca Cluster ^†
journal, September 1997

XDSAPP : a graphical user interface for the convenient processing of diffraction data using XDS
journal, April 2012

Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin
journal, March 2012

Highly Purified Thermo-Stable Oxygen-Evolving Photosystem II Core Complex from the Thermophilic Cyanobacterium Synechococcus elongatus Having His-Tagged CP43
journal, January 1999

XDS
journal, January 2010

Recent advances in understanding the assembly and repair of photosystem II
journal, March 2010

Light-induced quinone reduction in photosystem II
journal, January 2012

Stepwise Transition of the Tetra-Manganese Complex of Photosystem II to a Binuclear Mn2(μ-O)2 Complex in Response to a Temperature Jump: A Time-Resolved Structural Investigation Employing X-Ray Absorption Spectroscopy
journal, February 2003

Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG
journal, April 2010

The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis
journal, April 2015

Architecture of the Photosynthetic Oxygen-Evolving Center
journal, March 2004

Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor
journal, January 2005

Structure of photosystem II and substrate binding at room temperature
journal, November 2016

Calcium Modulates the Photo-assembly of Photosystem II (Mn)4-Clusters by Preventing Ligation of Nonfunctional High-Valency States of Manganese
journal, October 1995

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

X-ray Crystal Structure of the Fe-Only Hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom Resolution
journal, December 1998

Improved R-factors for diffraction data analysis in macromolecular crystallography
journal, April 1997

MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

Mn ₄ Ca Cluster in Photosynthesis: Where and How Water is Oxidized to Dioxygen
journal, March 2014

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

Features and development of Coot
journal, March 2010

Intermediates in Assembly by Photoactivation after Thermally Accelerated Disassembly of the Manganese Complex of Photosynthetic Water Oxidation ^†
journal, December 2006

Photoactivation of the manganese catalyst of O2 evolution. I. Biochemical and kinetic aspects
journal, November 1971

Spare quinones in the QB cavity of crystallized photosystem II from Thermosynechococcus elongatus
journal, June 2007

The extrinsic proteins of Photosystem II
journal, January 2012

Structure of a Cofactor-Deficient Nitrogenase MoFe Protein
journal, April 2002

Aromatic structure of Tyrosine-92 in the extrinsic PsbU protein of red algal Photosystem II is important for its functioning
journal, October 2007

Comparison of chloride-depleted and calcium-depleted PSII: the midpoint potential of QA and susceptibility to photodamage
journal, March 1997

Assembly of the water-oxidizing complex in photosystem II
journal, July 2011

Assembly of nonheme Mn/Fe active sites in heterodinuclear metalloproteins
journal, April 2014

Evidence for Interstitial Carbon in Nitrogenase FeMo Cofactor
journal, November 2011

Conformational Changes in Photosystem II Supercomplexes upon Removal of Extrinsic Subunits ^†
journal, October 2000

Bicarbonate-induced redox tuning in Photosystem II for regulation and protection
journal, October 2016

Two tyrosines that changed the world: Interfacing the oxidizing power of photochemistry to water splitting in photosystem II
journal, January 2012

Redox potentials of primary electron acceptor quinone molecule (QA)- and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d
journal, April 2011

Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center
journal, January 1999

The solvent component of macromolecular crystals
journal, April 2015

Two Different Structures of the Oxygen-Evolving Complex in the Same Polypeptide Frameworks of Photosystem II
journal, January 2017

Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution
journal, February 2001

Photoassembly of the water-oxidizing complex in photosystem II
journal, February 2008

Investigating the Structure and Dynamics of Apo‐Photosystem II
journal, June 2019

O2 evolution and recovery of the water-oxidizing enzyme
journal, March 2018

Calcium, conformational selection, and redox-active tyrosine YZ in the photosynthetic oxygen-evolving cluster
journal, May 2018

A novel chlorophyll protein complex in the repair cycle of photosystem II
journal, October 2019

Photosystem II oxygen-evolving complex photoassembly displays an inverse H/D solvent isotope effect under chloride-limiting conditions
journal, September 2019

Assessment of the manganese cluster’s oxidation state via photoactivation of photosystem II microcrystals
journal, December 2019

Surface-grafted lanthanoid complexes of the tungstosilicate polyanion [SiW ₁₂ O ₄₀ ] ⁴⁻ : a synthetic, structural and computational investigation
journal, October 2018

Structural Changes in the Acceptor Site of Photosystem II upon Ca2+/Sr2+ Exchange in the Mn4CaO5 Cluster Site and the Possible Long-Range Interactions
journal, August 2019

Investigating the Structure and Dynamics of Apo‐Photosystem II
text, January 2019

Structural changes in the acceptor site of photosystem II upon Ca$^{2+}$/Sr$^{2+}$ exchange in the Mn$_4$CaO$_5$ Cluster Site and the Possible Long-Range Interactions
text, January 2019