Dissecting pigment architecture of individual photosynthetic antenna complexes in solution

Wang, Quan; Moerner, W. E.

doi:10.1073/pnas.1514027112

Title: Dissecting pigment architecture of individual photosynthetic antenna complexes in solution

Abstract

Oligomerization plays a critical role in shaping the light-harvesting properties of many photosynthetic pigment-protein complexes, but a detailed understanding of this process at the level of individual pigments is still lacking. To study the effects of oligomerization, we designed a single-molecule approach to probe the photophysical properties of individual pigment sites as a function of protein assembly state. Our method, based on the principles of anti-Brownian electrokinetic trapping of single fluorescent proteins, step-wise photobleaching, and multiparameter spectroscopy, allows pigment-specific spectroscopic information on single multipigment antennae to be recorded in a nonperturbative aqueous environment with unprecedented detail. We focus on the monomer-to-trimer transformation of allophycocyanin (APC), an important antenna protein in cyanobacteria. Here, our data reveal that the two chemically identical pigments in APC have different roles. One (α) is the functional pigment that red-shifts its spectral properties upon trimer formation, whereas the other (β) is a "protective" pigment that persistently quenches the excited state of α in the prefunctional, monomer state of the protein. These results show how subtleties in pigment organization give rise to functionally important aspects of energy transfer and photoprotection in antenna complexes. Finally, the method developed here should find immediate application in understanding the emergent propertiesmore »« less

Authors:

Wang, Quan ^[1]; Moerner, W. E. ^[1]

Department of Chemistry, Stanford University, Stanford, CA 94305

Publication Date:: Mon Oct 05 00:00:00 EDT 2015

Research Org.:: Stanford Univ., CA (United States)

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

OSTI Identifier:: 1235116

Alternate Identifier(s):: OSTI ID: 1348404

Grant/Contract Number:: FG02-07ER15892

Resource Type:: Published Article

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 45; Journal ID: ISSN 0027-8424

Publisher:: Proceedings of the National Academy of Sciences

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; ABEL trap; allophycocyanin; photosynthetic protein; single-molecule spectroscopy

Citation Formats


                    Wang, Quan, and Moerner, W. E. Dissecting pigment architecture of individual photosynthetic antenna complexes in solution.  United States: N. p., 2015. 
Web.  doi:10.1073/pnas.1514027112.

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                    Wang, Quan, & Moerner, W. E. Dissecting pigment architecture of individual photosynthetic antenna complexes in solution.  United States.  https://doi.org/10.1073/pnas.1514027112

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                    Wang, Quan, and Moerner, W. E. Mon .  
"Dissecting pigment architecture of individual photosynthetic antenna complexes in solution".  United States.  https://doi.org/10.1073/pnas.1514027112.

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@article{osti_1235116,

  title        = {Dissecting pigment architecture of individual photosynthetic antenna complexes in solution},

  author       = {Wang, Quan and Moerner, W. E.},

  abstractNote = {Oligomerization plays a critical role in shaping the light-harvesting properties of many photosynthetic pigment-protein complexes, but a detailed understanding of this process at the level of individual pigments is still lacking. To study the effects of oligomerization, we designed a single-molecule approach to probe the photophysical properties of individual pigment sites as a function of protein assembly state. Our method, based on the principles of anti-Brownian electrokinetic trapping of single fluorescent proteins, step-wise photobleaching, and multiparameter spectroscopy, allows pigment-specific spectroscopic information on single multipigment antennae to be recorded in a nonperturbative aqueous environment with unprecedented detail. We focus on the monomer-to-trimer transformation of allophycocyanin (APC), an important antenna protein in cyanobacteria. Here, our data reveal that the two chemically identical pigments in APC have different roles. One (α) is the functional pigment that red-shifts its spectral properties upon trimer formation, whereas the other (β) is a "protective" pigment that persistently quenches the excited state of α in the prefunctional, monomer state of the protein. These results show how subtleties in pigment organization give rise to functionally important aspects of energy transfer and photoprotection in antenna complexes. Finally, the method developed here should find immediate application in understanding the emergent properties of other natural and artificial light-harvesting systems.},

  doi          = {10.1073/pnas.1514027112},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 45,

  volume       = 112,

  place        = {United States},

  year         = {Mon Oct 05 00:00:00 EDT 2015},

  month        = {Mon Oct 05 00:00:00 EDT 2015}

}

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Title: Dissecting pigment architecture of individual photosynthetic antenna complexes in solution

Abstract

Citation Formats

Effect of salts on C-phycocyanin journal, October 1971

Unraveling the Electronic Structure of Individual Photosynthetic Pigment-Protein Complexes journal, July 1999

The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes journal, September 2014

A model for early events in the assembly pathway of cyanobacterial phycobilisomes journal, November 1998

Identification of Single Molecules in Aqueous Solution by Time-Resolved Fluorescence Anisotropy journal, January 1999

Higher-Excited-State Photophysical Pathways in Multichromophoric Systems Revealed by Single-Molecule Fluorescence Spectroscopy journal, November 2004

Evidence for Coherent Energy Transfer in Allophycocyanin Trimers journal, October 1995

Branching Out of Single-Molecule Fluorescence Spectroscopy: Challenges for Chemistry and Influence on Biology journal, April 2005

A transient absorption study of allophycocyanin journal, December 2002

Lifetime and Spectrally Resolved Characterization of the Photodynamics of Single Fluorophores in Solution Using the Anti-Brownian Electrokinetic Trap journal, November 2012

Principles of Fluorescence Spectroscopy book, January 2006

Single-Molecule Spectroscopy Selectively Probes Donor and Acceptor Chromophores in the Phycobiliprotein Allophycocyanin journal, October 2004

Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions journal, August 2014

Efficient simultaneous fluorescence orientation, spectrum, and lifetime detection for single molecule dynamics journal, October 2012

RESONANCE-ENHANCED CARS SPECTROSCOPY OF BILIPROTEINS. INFLUENCE OF AGGREGATION and LINKER PROTEINS ON CHROMOPHORE STRUCTURE IN ALLOPHYCOCYANIN (Mastigocladus laminosus) journal, November 1995

Reconstitution of phycobilisome core–membrane linker, LCM, by autocatalytic chromophore binding to ApcE journal, January 2005

Excited-State Processes in Phycocyanobilin Studied by Femtosecond Spectroscopy † journal, March 2000

Suppressing Brownian motion of individual biomolecules in solution journal, March 2006

Energy transfer and trapping in photosynthesis journal, August 1994

Circular dichroism and polarized fluorescence characteristics of blue-green algal allophycocyanins journal, June 1980

Polarization Spectroscopy of Single Fluorescent Molecules journal, August 1999

Fluorescence Spectral Dynamics of Single LHCII Trimers journal, June 2010

Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant journal, July 2005

Single-molecule motions enable direct visualization of biomolecular interactions in solution journal, March 2014

Monomeric C-phycocyanin at room temperature and 77 K: resolution of the absorption and fluorescence spectra of the individual chromophores and the energy-transfer rate constants journal, September 1993

Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at 2.3 Å resolution journal, January 1995

Watching conformational- and photodynamics of single fluorescent proteins in solution journal, January 2010

Vibronic Enhancement of Exciton Sizes and Energy Transport in Photosynthetic Complexes journal, February 2011

Biliproteins journal, March 1981

Fluorescence Spectroscopy, Exciton Dynamics, and Photochemistry of Single Allophycocyanin Trimers journal, December 1998

Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria journal, November 2013

Fluorescence and photobleaching dynamics of single light-harvesting complexes journal, September 1997

Dynamic Inhomogeneity in the Photodynamics of Cyanobacterial Phytochrome Cph1 journal, April 2014

Self-Assembling Light-Harvesting Systems from Synthetically Modified Tobacco Mosaic Virus Coat Proteins journal, March 2007

Natural strategies for photosynthetic light harvesting journal, June 2014

Single-molecule spectroscopy and femtosecond transient absorption studies on the excitation energy transfer process in ApcE(1–240) dimers journal, January 2015

Fluorescence Spectral Fluctuations of Single LH2 Complexes from Rhodopseudomonas acidophila Strain 10050 † journal, April 2004

Site, Rate, and Mechanism of Photoprotective Quenching in Cyanobacteria journal, November 2011

Biliprotein maturation: the chromophore attachment: Biliprotein chromophore attachment journal, February 2008

Allophycocyanin Complexes of the Phycobilisome from Mastigocladus laminosus . Influence of the Linker Polypeptide L 8.9 C on the Spectral Properties of the Phycobiliprotein Subunits journal, January 1987

Allophycocyanin Trimer Stability and Functionality Are Primarily Due to Polar Enhanced Hydrophobicity of the Phycocyanobilin Binding Pocket journal, December 2008

Allophycocyanin and energy transfer journal, July 2004

A Little Coherence in Photosynthetic Light Harvesting journal, November 2013

Structural analysis at 2.2 A of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP*LC7.8, from phycobilisomes of Mastigocladus laminosus journal, February 1999

Physico-chemical and immunological properties of allophycocyanins journal, January 1977

Protein-Matrix Solvation Dynamics in the α Subunit of C -Phycocyanin journal, January 1996

Exciton Coherence and Energy Transport in the Light-Harvesting Dimers of Allophycocyanin journal, December 2009

Probing Single Biomolecules in Solution Using the Anti-Brownian Electrokinetic (ABEL) Trap journal, March 2012

Effect of salts on C-phycocyanin
journal, October 1971

Unraveling the Electronic Structure of Individual Photosynthetic Pigment-Protein Complexes
journal, July 1999

The structure of allophycocyanin B from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes
journal, September 2014

A model for early events in the assembly pathway of cyanobacterial phycobilisomes
journal, November 1998

Identification of Single Molecules in Aqueous Solution by Time-Resolved Fluorescence Anisotropy
journal, January 1999

Higher-Excited-State Photophysical Pathways in Multichromophoric Systems Revealed by Single-Molecule Fluorescence Spectroscopy
journal, November 2004

Evidence for Coherent Energy Transfer in Allophycocyanin Trimers
journal, October 1995

Branching Out of Single-Molecule Fluorescence Spectroscopy: Challenges for Chemistry and Influence on Biology
journal, April 2005

A transient absorption study of allophycocyanin
journal, December 2002

Lifetime and Spectrally Resolved Characterization of the Photodynamics of Single Fluorophores in Solution Using the Anti-Brownian Electrokinetic Trap
journal, November 2012

Principles of Fluorescence Spectroscopy
book, January 2006

Single-Molecule Spectroscopy Selectively Probes Donor and Acceptor Chromophores in the Phycobiliprotein Allophycocyanin
journal, October 2004

Modulating energy arriving at photochemical reaction centers: orange carotenoid protein-related photoprotection and state transitions
journal, August 2014

Efficient simultaneous fluorescence orientation, spectrum, and lifetime detection for single molecule dynamics
journal, October 2012

RESONANCE-ENHANCED CARS SPECTROSCOPY OF BILIPROTEINS. INFLUENCE OF AGGREGATION and LINKER PROTEINS ON CHROMOPHORE STRUCTURE IN ALLOPHYCOCYANIN (Mastigocladus laminosus)
journal, November 1995

Reconstitution of phycobilisome core–membrane linker, LCM, by autocatalytic chromophore binding to ApcE
journal, January 2005

Excited-State Processes in Phycocyanobilin Studied by Femtosecond Spectroscopy ^†
journal, March 2000

Suppressing Brownian motion of individual biomolecules in solution
journal, March 2006

Energy transfer and trapping in photosynthesis
journal, August 1994

Circular dichroism and polarized fluorescence characteristics of blue-green algal allophycocyanins
journal, June 1980

Polarization Spectroscopy of Single Fluorescent Molecules
journal, August 1999

Fluorescence Spectral Dynamics of Single LHCII Trimers
journal, June 2010

Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant
journal, July 2005

Single-molecule motions enable direct visualization of biomolecular interactions in solution
journal, March 2014

Monomeric C-phycocyanin at room temperature and 77 K: resolution of the absorption and fluorescence spectra of the individual chromophores and the energy-transfer rate constants
journal, September 1993

Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at 2.3 Å resolution
journal, January 1995

Watching conformational- and photodynamics of single fluorescent proteins in solution
journal, January 2010

Vibronic Enhancement of Exciton Sizes and Energy Transport in Photosynthetic Complexes
journal, February 2011

Biliproteins
journal, March 1981

Fluorescence Spectroscopy, Exciton Dynamics, and Photochemistry of Single Allophycocyanin Trimers
journal, December 1998

Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria
journal, November 2013

Fluorescence and photobleaching dynamics of single light-harvesting complexes
journal, September 1997

Dynamic Inhomogeneity in the Photodynamics of Cyanobacterial Phytochrome Cph1
journal, April 2014

Self-Assembling Light-Harvesting Systems from Synthetically Modified Tobacco Mosaic Virus Coat Proteins
journal, March 2007

Natural strategies for photosynthetic light harvesting
journal, June 2014

Single-molecule spectroscopy and femtosecond transient absorption studies on the excitation energy transfer process in ApcE(1–240) dimers
journal, January 2015

Fluorescence Spectral Fluctuations of Single LH2 Complexes from Rhodopseudomonas acidophila Strain 10050 ^†
journal, April 2004

Site, Rate, and Mechanism of Photoprotective Quenching in Cyanobacteria
journal, November 2011

Biliprotein maturation: the chromophore attachment: Biliprotein chromophore attachment
journal, February 2008

Allophycocyanin Complexes of the Phycobilisome from Mastigocladus laminosus . Influence of the Linker Polypeptide L ^8.9 _C on the Spectral Properties of the Phycobiliprotein Subunits
journal, January 1987

Allophycocyanin Trimer Stability and Functionality Are Primarily Due to Polar Enhanced Hydrophobicity of the Phycocyanobilin Binding Pocket
journal, December 2008

Allophycocyanin and energy transfer
journal, July 2004

A Little Coherence in Photosynthetic Light Harvesting
journal, November 2013

Structural analysis at 2.2 A of orthorhombic crystals presents the asymmetry of the allophycocyanin-linker complex, AP*LC7.8, from phycobilisomes of Mastigocladus laminosus
journal, February 1999

Physico-chemical and immunological properties of allophycocyanins
journal, January 1977

Protein-Matrix Solvation Dynamics in the α Subunit of C -Phycocyanin
journal, January 1996

Exciton Coherence and Energy Transport in the Light-Harvesting Dimers of Allophycocyanin
journal, December 2009

Probing Single Biomolecules in Solution Using the Anti-Brownian Electrokinetic (ABEL) Trap
journal, March 2012