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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 » of other natural and artificial light-harvesting systems.« less

Authors:
 [1];  [1]
  1. Stanford Univ., CA (United States). Dept. of Chemistry
Publication Date:
Research Org.:
Stanford Univ., CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
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 Volume: 112; Journal Issue: 45; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
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.
Wang, Quan, & Moerner, W. E. Dissecting pigment architecture of individual photosynthetic antenna complexes in solution. United States. doi:10.1073/pnas.1514027112.
Wang, Quan, and Moerner, W. E. Mon . "Dissecting pigment architecture of individual photosynthetic antenna complexes in solution". United States. doi:10.1073/pnas.1514027112.
@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 = {2015},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1514027112

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Cited by: 13 works
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Works referenced in this record:

Natural strategies for photosynthetic light harvesting
journal, June 2014

  • Croce, Roberta; van Amerongen, Herbert
  • Nature Chemical Biology, Vol. 10, Issue 7
  • DOI: 10.1038/nchembio.1555

Energy transfer and trapping in photosynthesis
journal, August 1994

  • van Grondelle, Rienk; Dekker, Jan P.; Gillbro, Tomas
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1187, Issue 1
  • DOI: 10.1016/0005-2728(94)90166-X

A Little Coherence in Photosynthetic Light Harvesting
journal, November 2013

  • Anna, Jessica M.; Scholes, Gregory D.; van Grondelle, Rienk
  • BioScience, Vol. 64, Issue 1
  • DOI: 10.1093/biosci/bit002

Biliproteins
journal, March 1981

  • Scheer, Hugo
  • Angewandte Chemie International Edition in English, Vol. 20, Issue 3
  • DOI: 10.1002/anie.198102411

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

  • Miller, Rebekah A.; Presley, Andrew D.; Francis, Matthew B.
  • Journal of the American Chemical Society, Vol. 129, Issue 11
  • DOI: 10.1021/ja063887t

Effect of salts on C-phycocyanin
journal, October 1971

  • MacColl, Robert; Berns, Donald S.; Koven, Norman L.
  • Archives of Biochemistry and Biophysics, Vol. 146, Issue 2
  • DOI: 10.1016/0003-9861(71)90151-2

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

  • Debreczeny, Martin P.; Sauer, Kenneth; Zhou, Jianhui
  • The Journal of Physical Chemistry, Vol. 97, Issue 38
  • DOI: 10.1021/j100140a050

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

  • Bopp, M. A.; Jia, Y.; Li, L.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 20
  • DOI: 10.1073/pnas.94.20.10630

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

  • Ying, Liming; Xie, X. Sunney
  • The Journal of Physical Chemistry B, Vol. 102, Issue 50
  • DOI: 10.1021/jp983227d

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


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

  • Rutkauskas, Danielis; Novoderezkhin, Vladimir; Cogdell, Richard J.
  • Biochemistry, Vol. 43, Issue 15
  • DOI: 10.1021/bi0497648

Fluorescence Spectral Dynamics of Single LHCII Trimers
journal, June 2010

  • Krüger, Tjaart P. J.; Novoderezhkin, Vladimir I.; Ilioaia, Cristian
  • Biophysical Journal, Vol. 98, Issue 12
  • DOI: 10.1016/j.bpj.2010.03.028

Allophycocyanin and energy transfer
journal, July 2004


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

  • Tian, Lijin; van Stokkum, Ivo H. M.; Koehorst, Rob B. M.
  • Journal of the American Chemical Society, Vol. 133, Issue 45
  • DOI: 10.1021/ja206414m

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

  • Cohen, A. E.; Moerner, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 12
  • DOI: 10.1073/pnas.0509976103

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

  • Wang, Quan; Goldsmith, Randall H.; Jiang, Yan
  • Accounts of Chemical Research, Vol. 45, Issue 11
  • DOI: 10.1021/ar200304t

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


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

  • Goldsmith, Randall H.; Moerner, W. E.
  • Nature Chemistry, Vol. 2, Issue 3
  • DOI: 10.1038/nchem.545

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

  • Wang, Quan; Moerner, W. E.
  • The Journal of Physical Chemistry B, Vol. 117, Issue 16
  • DOI: 10.1021/jp308949d

Polarization Spectroscopy of Single Fluorescent Molecules
journal, August 1999

  • Ha, Taekjip; Laurence, Ted A.; Chemla, Daniel S.
  • The Journal of Physical Chemistry B, Vol. 103, Issue 33
  • DOI: 10.1021/jp990948j

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

  • Schaffer, J.; Volkmer, A.; Eggeling, C.
  • The Journal of Physical Chemistry A, Vol. 103, Issue 3
  • DOI: 10.1021/jp9833597

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

  • Tinnefeld, Philip; Sauer, Markus
  • Angewandte Chemie International Edition, Vol. 44, Issue 18
  • DOI: 10.1002/anie.200300647

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

  • Börner, Richard; Kowerko, Danny; Krause, Stefan
  • The Journal of Chemical Physics, Vol. 137, Issue 16
  • DOI: 10.1063/1.4759108

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

  • Cohen-Bazire, G.; B�guin, S.; Rimon, S.
  • Archives of Microbiology, Vol. 111, Issue 3
  • DOI: 10.1007/BF00549359

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


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

  • Bischoff, Mark; Hermann, Gudrun; Rentsch, Sabine
  • The Journal of Physical Chemistry B, Vol. 104, Issue 8
  • DOI: 10.1021/jp992083f

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

  • Kim, Peter W.; Rockwell, Nathan C.; Martin, Shelley S.
  • Biochemistry, Vol. 53, Issue 17
  • DOI: 10.1021/bi500108s

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

  • Riter, Ruth R.; Edington, Maurice D.; Beck, Warren F.
  • The Journal of Physical Chemistry, Vol. 100, Issue 33
  • DOI: 10.1021/jp960453j

A transient absorption study of allophycocyanin
journal, December 2002

  • Shiu, Y. J.; Zhang, J. M.; Hayashi, M.
  • Journal of Chemical Sciences, Vol. 114, Issue 6
  • DOI: 10.1007/BF02708855

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

  • Tinnefeld, Philip; Hofkens, Johan; Herten, Dirk-Peter
  • ChemPhysChem, Vol. 5, Issue 11
  • DOI: 10.1002/cphc.200400325

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

  • Brejc, Katjuša; Ficner, Ralf; Huber, Robert
  • Journal of Molecular Biology, Vol. 249, Issue 2
  • DOI: 10.1006/jmbi.1995.0307

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

  • Reuter, W.; Wiegand, G.; Huber, R.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 4
  • DOI: 10.1073/pnas.96.4.1363

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

  • Peng, Pan-Pan; Dong, Liang-Liang; Sun, Ya-Fang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 70, Issue 10
  • DOI: 10.1107/S1399004714015776

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

  • Womick, Jordan M.; Moran, Andrew M.
  • The Journal of Physical Chemistry B, Vol. 113, Issue 48
  • DOI: 10.1021/jp907644h

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

  • Womick, Jordan M.; Moran, Andrew M.
  • The Journal of Physical Chemistry B, Vol. 115, Issue 6
  • DOI: 10.1021/jp106713q

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

  • Edington, Maurice D.; Riter, Ruth E.; Beck, Warren F.
  • The Journal of Physical Chemistry, Vol. 99, Issue 43
  • DOI: 10.1021/j100043a001

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

  • McGregor, Ailie; Klartag, Merav; David, Liron
  • Journal of Molecular Biology, Vol. 384, Issue 2
  • DOI: 10.1016/j.jmb.2008.09.018

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

  • Zhao, Kai-Hong; Su, Ping; Böhm, Stephan
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.09.008

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

  • Long, Saran; Zhou, Meng; Tang, Kun
  • Physical Chemistry Chemical Physics, Vol. 17, Issue 20
  • DOI: 10.1039/C5CP01687H

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


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


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


    Works referencing / citing this record:

    Multi-dimensional super-resolution imaging enables surface hydrophobicity mapping
    journal, December 2016

    • Bongiovanni, Marie N.; Godet, Julien; Horrocks, Mathew H.
    • Nature Communications, Vol. 7, Issue 1
    • DOI: 10.1038/ncomms13544