The use of advanced mass spectrometry to dissect the life-cycle of photosystem II

Weisz, Daniel A.; Gross, Michael L.; Pakrasi, Himadri B.

doi:10.3389/fpls.2016.00617

Title: The use of advanced mass spectrometry to dissect the life-cycle of photosystem II

Abstract

Photosystem II (PSII) is a photosynthetic membrane-protein complex that undergoes an intricate, tightly regulated cycle of assembly, damage, and repair. The available crystal structures of cyanobacterial PSII are an essential foundation for understanding PSII function, but nonetheless provide a snapshot only of the active complex. To study aspects of the entire PSII life-cycle, mass spectrometry (MS) has emerged as a powerful tool that can be used in conjunction with biochemical techniques. In this article, we present the MS-based approaches that are used to study PSII composition, dynamics, and structure, and review the information about the PSII life-cycle that has been gained by these methods. This information includes the composition of PSII subcomplexes, discovery of accessory PSII proteins, identification of post-translational modifications and quantification of their changes under various conditions, determination of the binding site of proteins not observed in PSII crystal structures, conformational changes that underlie PSII functions, and identification of water and oxygen channels within PSII. Lastly, we conclude with an outlook for the opportunity of future MS contributions to PSII research.

Authors:

Weisz, Daniel A. ^[1]; Gross, Michael L. ^[2]; Pakrasi, Himadri B. ^[3]

Washington Univ., St. Louis, St. Louis, MO (United States). Dept. of Biology; Dept. of Chemistry
Washington Univ., St. Louis, St. Louis, MO (United States). Dept. of Chemistry
Washington Univ., St. Louis, St. Louis, MO (United States). Dept. of Biology

Publication Date:: Tue May 10 00:00:00 EDT 2016

Research Org.:: Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)

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

OSTI Identifier:: 1282178

Grant/Contract Number:: SC0001035; FG02-99ER20350

Resource Type:: Accepted Manuscript

Journal Name:: Frontiers in Plant Science

Additional Journal Information:: Journal Volume: 7; Journal ID: ISSN 1664-462X

Publisher:: Frontiers Research Foundation

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Photosystem II; Photosystem II life-cycle; mass spectrometry; post-translational modification; chemical cross-linking; protein footprinting; sp pcc 6803; synechocystis sp pcc-6803; cyanobacterium thermosynechococcus-elongatus; manganese-stabilizing protein; integral membrane-proteins; orange carotenoid protein; reaction-center complex; alga chlamydomonas-reinhardtii; excitation-energy distribution

Citation Formats


                    Weisz, Daniel A., Gross, Michael L., and Pakrasi, Himadri B. The use of advanced mass spectrometry to dissect the life-cycle of photosystem II.  United States: N. p., 2016. 
Web.  doi:10.3389/fpls.2016.00617.

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                    Weisz, Daniel A., Gross, Michael L., & Pakrasi, Himadri B. The use of advanced mass spectrometry to dissect the life-cycle of photosystem II.  United States.  https://doi.org/10.3389/fpls.2016.00617

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                    Weisz, Daniel A., Gross, Michael L., and Pakrasi, Himadri B. Tue .  
"The use of advanced mass spectrometry to dissect the life-cycle of photosystem II".  United States.  https://doi.org/10.3389/fpls.2016.00617.  https://www.osti.gov/servlets/purl/1282178.

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@article{osti_1282178,

  title        = {The use of advanced mass spectrometry to dissect the life-cycle of photosystem II},

  author       = {Weisz, Daniel A. and Gross, Michael L. and Pakrasi, Himadri B.},

  abstractNote = {Photosystem II (PSII) is a photosynthetic membrane-protein complex that undergoes an intricate, tightly regulated cycle of assembly, damage, and repair. The available crystal structures of cyanobacterial PSII are an essential foundation for understanding PSII function, but nonetheless provide a snapshot only of the active complex. To study aspects of the entire PSII life-cycle, mass spectrometry (MS) has emerged as a powerful tool that can be used in conjunction with biochemical techniques. In this article, we present the MS-based approaches that are used to study PSII composition, dynamics, and structure, and review the information about the PSII life-cycle that has been gained by these methods. This information includes the composition of PSII subcomplexes, discovery of accessory PSII proteins, identification of post-translational modifications and quantification of their changes under various conditions, determination of the binding site of proteins not observed in PSII crystal structures, conformational changes that underlie PSII functions, and identification of water and oxygen channels within PSII. Lastly, we conclude with an outlook for the opportunity of future MS contributions to PSII research.},

  doi          = {10.3389/fpls.2016.00617},

  journal      = {Frontiers in Plant Science},

  number       = ,

  volume       = 7,

  place        = {United States},

  year         = {Tue May 10 00:00:00 EDT 2016},

  month        = {Tue May 10 00:00:00 EDT 2016}

}

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Works referencing / citing this record:

Mass spectrometry-based cross-linking study shows that the Psb28 protein binds to cytochrome b ₅₅₉ in Photosystem II
journal, February 2017

Weisz, Daniel A.; Liu, Haijun; Zhang, Hao
Proceedings of the National Academy of Sciences, Vol. 114, Issue 9
DOI: 10.1073/pnas.1620360114

Reactive oxygen species leave a damage trail that reveals water channels in Photosystem II
journal, November 2017

Weisz, Daniel A.; Gross, Michael L.; Pakrasi, Himadri B.
Science Advances, Vol. 3, Issue 11
DOI: 10.1126/sciadv.aao3013

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

Weisz, Daniel A.; Johnson, Virginia M.; Niedzwiedzki, Dariusz M.
Proceedings of the National Academy of Sciences, Vol. 116, Issue 43
DOI: 10.1073/pnas.1909644116

Similar Records in DOE PAGES and OSTI.GOV collections:

A novel chlorophyll protein complex in the repair cycle of photosystem II

Journal Article Weisz, Daniel A. ; Johnson, Virginia M. ; Niedzwiedzki, Dariusz M. ; ... - Proceedings of the National Academy of Sciences of the United States of America

In oxygenic photosynthetic organisms, photosystem II (PSII) is a unique membrane protein complex that catalyzes light-driven oxidation of water. PSII undergoes frequent damage due to its demanding photochemistry. It must undergo a repair and reassembly process following photodamage, many facets of which remain unknown. We have discovered a PSII subcomplex that lacks 5 key PSII core reaction center polypeptides: D1, D2, PsbE, PsbF, and PsbI. This pigment–protein complex does contain the PSII core antenna proteins CP47 and CP43, as well as most of their associated low molecular mass subunits, and the assembly factor Psb27. Immunoblotting, mass spectrometry, and ultrafast spectroscopicmore »« less
Cited by 25
https://doi.org/10.1073/pnas.1909644116
Advances in the Understanding of the Lifecycle of Photosystem II

Journal Article Johnson, Virginia M. ; Pakrasi, Himadri B. - Microorganisms

Photosystem II is a light-driven water-plastoquinone oxidoreductase present in cyanobacteria, algae and plants. It produces molecular oxygen and protons to drive ATP synthesis, fueling life on Earth. As a multi-subunit membrane-protein-pigment complex, Photosystem II undergoes a dynamic cycle of synthesis, damage, and repair known as the Photosystem II lifecycle, to maintain a high level of photosynthetic activity at the cellular level. Cyanobacteria, oxygenic photosynthetic bacteria, are frequently used as model organisms to study oxygenic photosynthetic processes due to their ease of growth and genetic manipulation. The cyanobacterial PSII structure and function have been well-characterized, but its lifecycle is under activemore »« less
https://doi.org/10.3390/microorganisms10050836
Advances in the Understanding of the Lifecycle of Photosystem II

Journal Article Johnson, Virginia M. ; Pakrasi, Himadri B. - Microorganisms

Photosystem II is a light-driven water-plastoquinone oxidoreductase present in cyanobacteria, algae and plants. It produces molecular oxygen and protons to drive ATP synthesis, fueling life on Earth. As a multi-subunit membrane-protein-pigment complex, Photosystem II undergoes a dynamic cycle of synthesis, damage, and repair known as the Photosystem II lifecycle, to maintain a high level of photosynthetic activity at the cellular level. Cyanobacteria, oxygenic photosynthetic bacteria, are frequently used as model organisms to study oxygenic photosynthetic processes due to their ease of growth and genetic manipulation. The cyanobacterial PSII structure and function have been well-characterized, but its lifecycle is under activemore »« less
https://doi.org/10.3390/microorganisms10050836

Full Text Available
Mass spectrometry-based cross-linking study shows that the Psb28 protein binds to cytochrome b ₅₅₉ in Photosystem II

Journal Article Weisz, Daniel A. ; Liu, Haijun ; Zhang, Hao ; ... - Proceedings of the National Academy of Sciences of the United States of America

Photosystem II (PSII), a large pigment protein complex, undergoes rapid turnover under natural conditions. During assembly of PSII, oxidative damage to vulnerable assembly intermediate complexes must be prevented. Psb28, the only cytoplasmic extrinsic protein in PSII, protects the RC47 assembly intermediate of PSII and assists its efficient conversion into functional PSII. Its role is particularly important under stress conditions when PSII damage occurs frequently. Psb28 is not found, however, in any PSII crystal structure, and its structural location has remained unknown. Here in this study, we used chemical cross-linking combined with mass spectrometry to capture the transient interaction of Psb28more »« less
Cited by 31
https://doi.org/10.1073/pnas.1620360114
AlphaFold and Structural Mass Spectrometry Enable Interrogations on the Intrinsically Disordered Regions in Cyanobacterial Light-harvesting Complex Phycobilisome

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Intrinsically disordered proteins/regions (IDPRs) are a very large and functionally important class of proteins that participate in weak multivalent interactions in protein complexes. They are recalcitrant for interrogations using X-ray crystallography and cryo-EM. The IDPRs observed at the interface of the photosynthetic pigment protein complexes (PPCs) remain much less clear, e.g., the major cyanobacterial light-harvesting complex (PBS) contains an unstructured PB-loop insertion in the phycocyanobilin domain (PB domain) of ApcE (the largest polypeptide in PBS). Here, a joint platform is built to probe such structural domains. This platform is characterized by two-round progressive justifications of in silico models by usingmore »« less
https://doi.org/10.1016/j.jmb.2022.167831

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Title: The use of advanced mass spectrometry to dissect the life-cycle of photosystem II

Abstract

Citation Formats

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journal, September 2006

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journal, October 2012

Role of the carboxy-terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803:assembly requires a free carboxyl group at C-terminal position 344
journal, November 1992

Production of reactive oxygen species by photosystem II
journal, October 2009

A phosphorylation map of the photosystem II supercomplex C2S2M2
journal, January 2013

Large‐scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis
journal, January 2008

Data-directed top-down Fourier-transform mass spectrometry of a large integral membrane protein complex: Photosystem II from Galdieria sulphuraria
journal, September 2010

Multiplexed Protein Quantitation in Saccharomyces cerevisiae Using Amine-reactive Isobaric Tagging Reagents
journal, September 2004

Architectural switch in plant photosynthetic membranes induced by light stress
journal, November 2012

Quantitative Proteomics in Plants: Choices in Abundance
journal, November 2007

Biogenesis of the cyanobacterial thylakoid membrane system - an update: Cyanobacterial thylakoid membrane biogenesis
journal, September 2010

Association of chlorophyll a/c2 complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24
journal, September 2008

Proteomic characterization and three-dimensional electron microscopy study of PSII–LHCII supercomplexes from higher plants
journal, September 2014

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

Analysis of photosystem II biogenesis in cyanobacteria
journal, March 2016

Photoinhibition and D1 Protein Degradation in Peas Acclimated to Different Growth Irradiances
journal, November 1993

Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present
journal, July 2012

The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes
journal, October 2001

Chemical Cross-linking and Mass Spectrometry for Protein Structural Modeling
journal, August 2003

The lipoproteins of cyanobacterial photosystem II
journal, July 2011

Role of Novel Dimeric Photosystem II (PSII)-Psb27 Protein Complex in PSII Repair
journal, July 2011

Isolation and Characterization of a Novel Xanthophyll-rich Pigmentprotein complex from Spinach
book, January 1998

Proteomic Analysis of a Highly Active Photosystem II Preparation from the Cyanobacterium Synechocystis sp. PCC 6803 Reveals the Presence of Novel Polypeptides
journal, May 2002

Differences in the Interactions between the Subunits of Photosystem II Dependent on D1 Protein Variants in the Thermophilic Cyanobacterium Thermosynechococcus elongatus
journal, July 2010

Novel Protein Phosphorylation Site Identification in Spinach Stroma Membranes by Titanium Dioxide Microcolumns and Tandem Mass Spectrometry
journal, April 2006

Recent advances in the use of mass spectrometry to examine structure/function relationships in photosystem II
journal, November 2015

N-terminal sequence analysis of the 8 kDa protein in Chlamydomonas reinhardii Localization of the phosphothreonine
journal, August 1988

Mass Spectrometric Resolution of Reversible Protein Phosphorylation in Photosynthetic Membranes of Arabidopsis thaliana
journal, December 2000

A Designed Inhibitor of a CLC Antiporter Blocks Function through a Unique Binding Mode
journal, November 2012

Phosphorylation of Light-harvesting Complex II and Photosystem II Core Proteins Shows Different Irradiance-dependent Regulation in Vivo : APPLICATION OF PHOSPHOTHREONINE ANTIBODIES TO ANALYSIS OF THYLAKOID PHOSPHOPROTEINS
journal, November 1997

Complete Protein Characterization Using Top-Down Mass Spectrometry and Ultraviolet Photodissociation
journal, June 2013

Benchmarking Multiple Fragmentation Methods on an Orbitrap Fusion for Top-down Phospho-Proteoform Characterization
journal, April 2015

Lifetimes of photosystem I and II proteins in the cyanobacterium Synechocystis sp. PCC 6803
journal, December 2011

Phosphorylation of the light-harvesting chlorophyll-protein regulates excitation energy distribution between Photosystem II and Photosystem I
journal, June 1982

Tubular Crystals of a Photosystem II Core Complex
journal, June 1996

Mass spectrometric characterization of membrane integral low molecular weight proteins from photosystem II in barley etioplasts
journal, February 2009

Biogenesis, assembly and turnover of photosystem II units
journal, October 2002

Chemical cross-linkers for protein structure studies by mass spectrometry
journal, January 2013

Evidence That the PsbK Polypeptide Is Associated with the Photosystem II Core Antenna Complex CP43
journal, August 2003

Close association of the 33 kDa extrinsic protein with the apoprotein of CPa1 in photosystem II
journal, April 1988

Kojak: Efficient Analysis of Chemically Cross-Linked Protein Complexes
journal, April 2015

Cyanobacterial Small Chlorophyll-binding Protein ScpD (HliB) Is Located on the Periphery of Photosystem II in the Vicinity of PsbH and CP47 Subunits
journal, August 2006

Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency inChlamydomonas reinhardtii
journal, November 2007

The Chloroplast Grana Proteome Defined by Intact Mass Measurements from Liquid Chromatography Mass Spectrometry
journal, October 2001

PHOTOSYSTEM II PROTEIN33, a Protein Conserved in the Plastid Lineage, Is Associated with the Chloroplast Thylakoid Membrane and Provides Stability to Photosystem II Supercomplexes in Arabidopsis
journal, December 2014

Role of the PsbI Protein in Photosystem II Assembly and Repair in the Cyanobacterium Synechocystis sp. PCC 6803
journal, October 2007

Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer
journal, January 2002

Identification of cross-linked peptides from complex samples
journal, July 2012

Automated Assignment of MS/MS Cleavable Cross-Links in Protein 3D-Structure Analysis
journal, September 2014

A Protein Phosphorylation Threshold for Functional Stacking of Plant Photosynthetic Membranes
journal, June 2010

Chemical cross-linking with NHS esters: a systematic study on amino acid reactivities
journal, May 2009

STN8 Protein Kinase in Arabidopsis thaliana Is Specific in Phosphorylation of Photosystem II Core Proteins
journal, July 2005

Rapid interchange between two distinct forms of cyanobacterial photosystem II reaction-center protein D1 in response to photoinhibition.
journal, November 1993

Photosystem II Component Lifetimes in the Cyanobacterium Synechocystis sp. Strain PCC 6803 : SMALL Cab-LIKE PROTEINS STABILIZE BIOSYNTHESIS INTERMEDIATES AND AFFECT EARLY STEPS IN CHLOROPHYLL SYNTHESIS
journal, November 2011

Structural Mass Spectrometry of Proteins Using Hydroxyl Radical Based Protein Footprinting
journal, October 2011

Isotope-Coded and Affinity-Tagged Cross-Linking (ICATXL): An Efficient Strategy to Probe Protein Interaction Surfaces
journal, August 2006

Chemical crosslinking studies of extrinsic proteins in cyanobacterial photosystem II
journal, November 1994

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

Mass spectrometry footprinting reveals the structural rearrangements of cyanobacterial orange carotenoid protein upon light activation
journal, December 2014

Identification of Oxidized Amino Acid Residues in the Vicinity of the Mn ₄ CaO ₅ Cluster of Photosystem II: Implications for the Identification of Oxygen Channels within the Photosystem
journal, July 2012

Too much of a good thing: light can be bad for photosynthesis
journal, February 1992

Intermolecular and Intramolecular Interactions of the 33-kDa Protein in Photosystem II
journal, December 1996

An Activated Glutamate Residue Identified in Photosystem II at the Interface between the Manganese-stabilizing Subunit and the D2 Polypeptide
journal, July 2007

Compositional and topological studies of the PsbW protein in spinach thylakoid membrane
journal, January 1997

Association of chlorophyll a/c2 complexes to photosystem I and photosystem II in the cryptophyte Rhodomonas CS24
journal, September 2008

Proteomic approach to characterize the supramolecular organization of photosystems in higher plants
journal, June 2004

Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559
journal, January 1987

Desiccation enhances phosphorylation of PSII and affects the distribution of protein complexes in the thylakoid membrane
journal, September 2014

Functional Characterization and Quantification of the Alternative PsbA Copies in Thermosynechococcus elongatus and Their Role in Photoprotection
journal, July 2010

Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases
journal, October 2005

Comparative cross-linking study on the 50S ribosomal subunit from Escherichia coli
journal, May 1989

Toward Full Peptide Sequence Coverage by Dual Fragmentation Combining Electron-Transfer and Higher-Energy Collision Dissociation Tandem Mass Spectrometry
journal, October 2012

Changes in thylakoid polypeptide phosphorylation during membrane biogenesis in Chlamydomonas reinhardii y-1
journal, January 1983

Lifetimes of photosystem I and II proteins in the cyanobacterium Synechocystis sp. PCC 6803
journal, December 2011

Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes
journal, November 2004

Mass Spectrometry-Based Protein Footprinting Characterizes the Structures of Oligomeric Apolipoprotein E2, E3, and E4
journal, September 2011

Identification of the phosphorylation site of an 8.3 kDa protein from photosystem II of spinach
journal, February 1987

Role of the carboxy-terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803:assembly requires a free carboxyl group at C-terminal position 344
journal, November 1992

Proteogenomic analysis and global discovery of posttranslational modifications in prokaryotes
journal, December 2014