The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection

Olsen, John D.; Martin, Elizabeth C.; Hunter, C. Neil

doi:10.1002/1873-3468.12575

Title: The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection

Abstract

Photosynthesis in some phototrophic bacteria requires the PufX component of the reaction centre–light‐harvesting 1–PufX ( RC ‐ LH 1‐PufX) complex, which creates a pore for quinone/quinol (Q/ QH ₂ ) exchange across the LH 1 barrier surrounding the RC . However, photosynthetic bacteria such as Thermochromatium (T.) tepidum do not require PufX because there are fewer carotenoid binding sites, which creates multiple pores in the LH 1 ring for Q/ QH ₂ exchange. We show that an αTrp _‐24 →Phe alteration of the Rhodobacter (Rba.) sphaeroides LH 1 antenna impairs carotenoid binding and allows photosynthetic growth in the absence of PufX. We propose that acquisition of PufX and confining Q/ QH ₂ traffic to a pore adjacent to the RC Q _B site is an evolutionary upgrade that allows increased LH 1 carotenoid content for enhanced light absorption and photoprotection.

Authors:

Olsen, John D. ^[1]; Martin, Elizabeth C. ^[1]; Hunter, C. Neil ^[1]

Department of Molecular Biology and Biotechnology University of Sheffield UK

Publication Date:: Fri Feb 10 00:00:00 EST 2017

Sponsoring Org.:: USDOE

OSTI Identifier:: 1343454

Alternate Identifier(s):: OSTI ID: 1343455

Resource Type:: Published Article

Journal Name:: FEBS Letters

Additional Journal Information:: Journal Name: FEBS Letters Journal Volume: 591 Journal Issue: 4; Journal ID: ISSN 0014-5793

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: Netherlands

Language:: English

Citation Formats


                    Olsen, John D., Martin, Elizabeth C., and Hunter, C. Neil. The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection.  Netherlands: N. p., 2017. 
Web.  doi:10.1002/1873-3468.12575.

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                    Olsen, John D., Martin, Elizabeth C., & Hunter, C. Neil. The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection.  Netherlands.  https://doi.org/10.1002/1873-3468.12575

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                    Olsen, John D., Martin, Elizabeth C., and Hunter, C. Neil. Fri .  
"The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection".  Netherlands.  https://doi.org/10.1002/1873-3468.12575.

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@article{osti_1343454,

  title        = {The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection},

  author       = {Olsen, John D. and Martin, Elizabeth C. and Hunter, C. Neil},

  abstractNote = {Photosynthesis in some phototrophic bacteria requires the PufX component of the reaction centre–light‐harvesting 1–PufX ( RC ‐ LH 1‐PufX) complex, which creates a pore for quinone/quinol (Q/ QH 2 ) exchange across the LH 1 barrier surrounding the RC . However, photosynthetic bacteria such as Thermochromatium (T.) tepidum do not require PufX because there are fewer carotenoid binding sites, which creates multiple pores in the LH 1 ring for Q/ QH 2 exchange. We show that an αTrp ‐24 →Phe alteration of the Rhodobacter (Rba.) sphaeroides LH 1 antenna impairs carotenoid binding and allows photosynthetic growth in the absence of PufX. We propose that acquisition of PufX and confining Q/ QH 2 traffic to a pore adjacent to the RC Q B site is an evolutionary upgrade that allows increased LH 1 carotenoid content for enhanced light absorption and photoprotection.},

  doi          = {10.1002/1873-3468.12575},

  journal      = {FEBS Letters},

  number       = 4,

  volume       = 591,

  place        = {Netherlands},

  year         = {Fri Feb 10 00:00:00 EST 2017},

  month        = {Fri Feb 10 00:00:00 EST 2017}

}

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Works referenced in this record:

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Title: The PufX quinone channel enables the light‐harvesting 1 antenna to bind more carotenoids for light collection and photoprotection

Abstract

Citation Formats

Carotenoid pigment conversion in rhodopseudomonas spheroides journal, August 1962

Complementation of a reaction center-deficient Rhodobacter sphaeroides pufLMX deletion strain in trans with pufBALM does not restore the photosynthesis-positive phenotype. journal, February 1990

Functional Consequences of the Organization of the Photosynthetic Apparatus in Rhodobacter sphaeroides: I. QUINONE DOMAINS AND EXCITATION TRANSFER IN CHROMATOPHORES AND REACTION CENTER{middle dot}ANTENNA COMPLEXES journal, January 2005

Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides journal, October 2014

Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides. journal, July 1994

Crystal Structure of the RC-LH1 Core Complex from Rhodopseudomonas palustris journal, December 2003

Pleiotropic effects of pufX gene deletion on the structure and function of the photosynthetic apparatus of Rhodobacter capsulatus journal, May 1992

Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides : LH2 at 6 Å, LH1 and RC-LH1 at 25 Å 1 1Edited by K. Nagai journal, October 1998

The Rhodobacter sphaeroides PufX protein is not required for photosynthetic competence in the absence of a light harvesting system journal, August 1994

Single amino acid substitutions in the B870 alpha and beta light-harvesting polypeptides of Rhodobacter capsulatus. Structural and spectral effects journal, December 1991

Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM journal, February 2003

Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties journal, May 2012

Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å journal, March 2014

Role of the PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 2. PufX is required for efficient ubiquinone/ubiquinol exchange between the reaction center QB site and the cytochrome bc1 complex. journal, November 1995

Role of PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 1. PufX is required for efficient light-driven electron transfer and photophosphorylation under anaerobic conditions. journal, November 1995

Role of the N- and C-terminal regions of the PufX protein in the structural organization of the photosynthetic core complex of Rhodobacter sphaeroides: Core complex organization in Rb. sphaeroides journal, April 2002

The structure of the photoreceptor unit of Rhodopseudomonas viridis journal, April 1984

Possible Pathway for Ubiquinone Shuttling in Rhodospirillum rubrum Revealed by Molecular Dynamics Simulation journal, January 2007

The 8.5Å Projection Structure of the Core RC–LH1–PufX Dimer of Rhodobacter sphaeroides journal, June 2005

Three-Dimensional Structure of the Rhodobacter sphaeroides RC-LH1-PufX Complex: Dimerization and Quinone Channels Promoted by PufX journal, October 2013

Three-dimensional Reconstruction of a Membrane-bending Complex journal, March 2008

PucC and LhaA direct efficient assembly of the light-harvesting complexes in Rhodobacter sphaeroides : Photosystem assembly in journal, November 2015

Isolation and characterization of the pigment-protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate/polyacrylamide gel electrophoresis. journal, January 1980

Construction and characterization of a mutant of Rhodobacter sphaeroides with the reaction center as the sole pigment-protein complex journal, May 1992

Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum journal, July 1994

Use of Engineered Unique Cysteine Residues to Facilitate Oriented Coupling of Proteins Directly to a Gold Substrate: Photochemistry and Photobiology journal, July 2011

Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution journal, August 2002

Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX journal, February 2004

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes journal, June 2005

Structural Analysis of the Reaction Center Light-harvesting Complex I Photosynthetic Core Complex of Rhodospirillum rubrum Using Atomic Force Microscopy journal, October 2003

Probing the Effect of the Binding Site on the Electrostatic Behavior of a Series of Carotenoids Reconstituted into the Light-Harvesting 1 Complex from Purple Photosynthetic Bacterium Rhodospirillum rubrum Detected by Stark Spectroscopy journal, August 2008

Aberrant Assembly Complexes of the Reaction Center Light-harvesting 1 PufX (RC-LH1-PufX) Core Complex of Rhodobacter sphaeroides Imaged by Atomic Force Microscopy journal, September 2014

Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway journal, February 2015

Consequences for the Organization of Reaction Center-Light Harvesting Antenna 1 (LH1) Core Complexes of Rhodobacter sphaeroides Arising from Deletion of Amino Acid Residues from the C Terminus of the LH1 Polypeptide journal, February 1996

Catalytic properties of the expressed acyclic carotenoid 2-ketolases from Rhodobacter capsulatus and Rubrivivax gelatinosus journal, February 2009

Carotenoid pigment conversion in rhodopseudomonas spheroides
journal, August 1962

Complementation of a reaction center-deficient Rhodobacter sphaeroides pufLMX deletion strain in trans with pufBALM does not restore the photosynthesis-positive phenotype.
journal, February 1990

Functional Consequences of the Organization of the Photosynthetic Apparatus in Rhodobacter sphaeroides: I. QUINONE DOMAINS AND EXCITATION TRANSFER IN CHROMATOPHORES AND REACTION CENTER{middle dot}ANTENNA COMPLEXES
journal, January 2005

Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides
journal, October 2014

Modification of a hydrogen bond to a bacteriochlorophyll a molecule in the light-harvesting 1 antenna of Rhodobacter sphaeroides.
journal, July 1994

Crystal Structure of the RC-LH1 Core Complex from Rhodopseudomonas palustris
journal, December 2003

Pleiotropic effects of pufX gene deletion on the structure and function of the photosynthetic apparatus of Rhodobacter capsulatus
journal, May 1992

Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides : LH2 at 6 Å, LH1 and RC-LH1 at 25 Å 1 1Edited by K. Nagai
journal, October 1998

The Rhodobacter sphaeroides PufX protein is not required for photosynthetic competence in the absence of a light harvesting system
journal, August 1994

Single amino acid substitutions in the B870 alpha and beta light-harvesting polypeptides of Rhodobacter capsulatus. Structural and spectral effects
journal, December 1991

Nanodissection and high-resolution imaging of the Rhodopseudomonas viridis photosynthetic core complex in native membranes by AFM
journal, February 2003

Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties
journal, May 2012

Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å
journal, March 2014

Role of the PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 2. PufX is required for efficient ubiquinone/ubiquinol exchange between the reaction center QB site and the cytochrome bc1 complex.
journal, November 1995

Role of PufX protein in photosynthetic growth of Rhodobacter sphaeroides. 1. PufX is required for efficient light-driven electron transfer and photophosphorylation under anaerobic conditions.
journal, November 1995

Role of the N- and C-terminal regions of the PufX protein in the structural organization of the photosynthetic core complex of Rhodobacter sphaeroides: Core complex organization in Rb. sphaeroides
journal, April 2002

The structure of the photoreceptor unit of Rhodopseudomonas viridis
journal, April 1984

Possible Pathway for Ubiquinone Shuttling in Rhodospirillum rubrum Revealed by Molecular Dynamics Simulation
journal, January 2007

The 8.5Å Projection Structure of the Core RC–LH1–PufX Dimer of Rhodobacter sphaeroides
journal, June 2005

Three-Dimensional Structure of the Rhodobacter sphaeroides RC-LH1-PufX Complex: Dimerization and Quinone Channels Promoted by PufX
journal, October 2013

Three-dimensional Reconstruction of a Membrane-bending Complex
journal, March 2008

PucC and LhaA direct efficient assembly of the light-harvesting complexes in Rhodobacter sphaeroides : Photosystem assembly in
journal, November 2015

Isolation and characterization of the pigment-protein complexes of Rhodopseudomonas sphaeroides by lithium dodecyl sulfate/polyacrylamide gel electrophoresis.
journal, January 1980

Construction and characterization of a mutant of Rhodobacter sphaeroides with the reaction center as the sole pigment-protein complex
journal, May 1992

Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum
journal, July 1994

Use of Engineered Unique Cysteine Residues to Facilitate Oriented Coupling of Proteins Directly to a Gold Substrate: Photochemistry and Photobiology
journal, July 2011

Projection structure of the photosynthetic reaction centre-antenna complex of Rhodospirillum rubrum at 8.5 A resolution
journal, August 2002

Molecular architecture of photosynthetic membranes in Rhodobacter sphaeroides: the role of PufX
journal, February 2004

Photo-oxidative stress in Rhodobacter sphaeroides: protective role of carotenoids and expression of selected genes
journal, June 2005

Structural Analysis of the Reaction Center Light-harvesting Complex I Photosynthetic Core Complex of Rhodospirillum rubrum Using Atomic Force Microscopy
journal, October 2003

Probing the Effect of the Binding Site on the Electrostatic Behavior of a Series of Carotenoids Reconstituted into the Light-Harvesting 1 Complex from Purple Photosynthetic Bacterium Rhodospirillum rubrum Detected by Stark Spectroscopy
journal, August 2008

Aberrant Assembly Complexes of the Reaction Center Light-harvesting 1 PufX (RC-LH1-PufX) Core Complex of Rhodobacter sphaeroides Imaged by Atomic Force Microscopy
journal, September 2014

Assembly of functional photosystem complexes in Rhodobacter sphaeroides incorporating carotenoids from the spirilloxanthin pathway
journal, February 2015

Consequences for the Organization of Reaction Center-Light Harvesting Antenna 1 (LH1) Core Complexes of Rhodobacter sphaeroides Arising from Deletion of Amino Acid Residues from the C Terminus of the LH1 Polypeptide
journal, February 1996

Catalytic properties of the expressed acyclic carotenoid 2-ketolases from Rhodobacter capsulatus and Rubrivivax gelatinosus
journal, February 2009