DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A bottom-up perspective on photodynamics and photoprotection in light-harvesting complexes using anti-Brownian trapping

Abstract

Single-molecule fluorescence spectroscopy allows direct, real-time observation of dynamic photophysical changes in light harvesting complexes. The Anti-Brownian ELectrokinetic (ABEL) trap is one such single-molecule method with useful advantages. This approach is particularly well-suited to make detailed spectroscopic measurements of pigment-protein complexes in solution phase because it enables extended-duration single-molecule observation by counteracting Brownian motion. This Perspective summarizes recent contributions by the authors and others that have utilized the unique capabilities of the ABEL trap to advance our understanding of phycobiliproteins and the phycobilisome complex, the primary light-harvesting apparatus of cyanobacteria. Monitoring the rich spectroscopic data from these measurements, which include brightness, fluorescence lifetime, polarization, and emission spectra, among other measurable parameters, has provided direct characterization of pigments and energy transfer pathways in the phycobilisome, spanning scales from single pigments and monomeric phycobiliproteins to higher order oligomers and protein-protein interactions of the phycobilisome complex. Importantly, new photophysical states and photodynamics were observed to modulate the flow of energy through the phycobilisome and suggest a previously unknown complexity in phycobilisome light harvesting and energy transport with a possible link to photoadaptive or photoprotective functions in cyanobacteria. Here, beyond deepening our collective understanding of natural light-harvesting systems, these and future discoveries may servemore » as inspiration for engineering improved artificial light-harvesting technologies.« less

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Stanford University, CA (United States)
  2. Stanford University, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Publication Date:
Research Org.:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Stanford Univ., CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; USDOE
OSTI Identifier:
1882690
Alternate Identifier(s):
OSTI ID: 1843432; OSTI ID: 1845343
Grant/Contract Number:  
AC02-76SF00515; FG02-07ER15892
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Chemical Physics
Additional Journal Information:
Journal Volume: 156; Journal Issue: 7; Journal ID: ISSN 0021-9606
Publisher:
American Institute of Physics (AIP)
Country of Publication:
United States
Language:
English
Subject:
14 SOLAR ENERGY; 77 NANOSCIENCE AND NANOTECHNOLOGY

Citation Formats

Squires, Allison H., Wang, Quan, Dahlberg, Peter D., and Moerner, W. E. A bottom-up perspective on photodynamics and photoprotection in light-harvesting complexes using anti-Brownian trapping. United States: N. p., 2022. Web. doi:10.1063/5.0079042.
Squires, Allison H., Wang, Quan, Dahlberg, Peter D., & Moerner, W. E. A bottom-up perspective on photodynamics and photoprotection in light-harvesting complexes using anti-Brownian trapping. United States. https://doi.org/10.1063/5.0079042
Squires, Allison H., Wang, Quan, Dahlberg, Peter D., and Moerner, W. E. Wed . "A bottom-up perspective on photodynamics and photoprotection in light-harvesting complexes using anti-Brownian trapping". United States. https://doi.org/10.1063/5.0079042. https://www.osti.gov/servlets/purl/1882690.
@article{osti_1882690,
title = {A bottom-up perspective on photodynamics and photoprotection in light-harvesting complexes using anti-Brownian trapping},
author = {Squires, Allison H. and Wang, Quan and Dahlberg, Peter D. and Moerner, W. E.},
abstractNote = {Single-molecule fluorescence spectroscopy allows direct, real-time observation of dynamic photophysical changes in light harvesting complexes. The Anti-Brownian ELectrokinetic (ABEL) trap is one such single-molecule method with useful advantages. This approach is particularly well-suited to make detailed spectroscopic measurements of pigment-protein complexes in solution phase because it enables extended-duration single-molecule observation by counteracting Brownian motion. This Perspective summarizes recent contributions by the authors and others that have utilized the unique capabilities of the ABEL trap to advance our understanding of phycobiliproteins and the phycobilisome complex, the primary light-harvesting apparatus of cyanobacteria. Monitoring the rich spectroscopic data from these measurements, which include brightness, fluorescence lifetime, polarization, and emission spectra, among other measurable parameters, has provided direct characterization of pigments and energy transfer pathways in the phycobilisome, spanning scales from single pigments and monomeric phycobiliproteins to higher order oligomers and protein-protein interactions of the phycobilisome complex. Importantly, new photophysical states and photodynamics were observed to modulate the flow of energy through the phycobilisome and suggest a previously unknown complexity in phycobilisome light harvesting and energy transport with a possible link to photoadaptive or photoprotective functions in cyanobacteria. Here, beyond deepening our collective understanding of natural light-harvesting systems, these and future discoveries may serve as inspiration for engineering improved artificial light-harvesting technologies.},
doi = {10.1063/5.0079042},
journal = {Journal of Chemical Physics},
number = 7,
volume = 156,
place = {United States},
year = {Wed Feb 16 00:00:00 EST 2022},
month = {Wed Feb 16 00:00:00 EST 2022}
}

Works referenced in this record:

Prokaryotes: The unseen majority
journal, June 1998

  • Whitman, W. B.; Coleman, D. C.; Wiebe, W. J.
  • Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
  • DOI: 10.1073/pnas.95.12.6578

Light Harvesting by Phycobilisomes
journal, June 1985


Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states
journal, June 2013

  • Schlau-Cohen, G. S.; Wang, Q.; Southall, J.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 27
  • DOI: 10.1073/pnas.1310222110

A carotenoid-protein from cyanobacteria
journal, October 1981

  • Kay Holt, Thomas; Krogmann, David W.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 637, Issue 3
  • DOI: 10.1016/0005-2728(81)90045-1

Resolving the contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals
journal, April 2015

  • Acuña, Alonso M.; Snellenburg, Joris J.; Gwizdala, Michal
  • Photosynthesis Research, Vol. 127, Issue 1
  • DOI: 10.1007/s11120-015-0141-x

Dissecting pigment architecture of individual photosynthetic antenna complexes in solution
journal, October 2015

  • Wang, Quan; Moerner, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 45
  • DOI: 10.1073/pnas.1514027112

Phycobilisome rod mutants in Synechocystis sp. strain PCC6803
journal, December 2004


Single-molecule diffusometry reveals the nucleotide-dependent oligomerization pathways of Nicotiana tabacum Rubisco activase
journal, March 2018

  • Wang, Quan; Serban, Andrew J.; Wachter, Rebekka M.
  • The Journal of Chemical Physics, Vol. 148, Issue 12
  • DOI: 10.1063/1.5005930

Single-Molecule Identification of Quenched and Unquenched States of LHCII
journal, February 2015

  • Schlau-Cohen, Gabriela S.; Yang, Hsiang-Yu; Krüger, Tjaart P. J.
  • The Journal of Physical Chemistry Letters, Vol. 6, Issue 5
  • DOI: 10.1021/acs.jpclett.5b00034

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

Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes
journal, September 2021


Electronic Absorption Spectra from MM and ab Initio QM/MM Molecular Dynamics: Environmental Effects on the Absorption Spectrum of Photoactive Yellow Protein
journal, September 2012

  • Isborn, Christine M.; Götz, Andreas W.; Clark, Matthew A.
  • Journal of Chemical Theory and Computation, Vol. 8, Issue 12
  • DOI: 10.1021/ct3006826

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


Revealing Conformational Variants of Solution-Phase Intrinsically Disordered Tau Protein at the Single-Molecule Level
journal, November 2017

  • Manger, Lydia H.; Foote, Alexander K.; Wood, Sharla L.
  • Angewandte Chemie International Edition, Vol. 56, Issue 49
  • DOI: 10.1002/anie.201708242

Local and global structural drivers for the photoactivation of the orange carotenoid protein
journal, September 2015

  • Gupta, Sayan; Guttman, Miklos; Leverenz, Ryan L.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
  • DOI: 10.1073/pnas.1512240112

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

Spectrally-tunable femtosecond single-molecule pump-probe spectroscopy
journal, January 2021

  • Moya, Raymundo; Kondo, Toru; Norris, Audrey C.
  • Optics Express, Vol. 29, Issue 18
  • DOI: 10.1364/OE.432995

Allophycocyanin B (?max 671, 618 nm): A new cyanobacterial phycobiliprotein
journal, January 1975

  • Glazer, A. N.; Bryant, D. A.
  • Archives of Microbiology, Vol. 104, Issue 1
  • DOI: 10.1007/BF00447294

Photosynthetic Excitons
book, January 2000

  • van Amerongen, Herbert; van Grondelle, Rienk; Valkunas, Leonas
  • World Scientific
  • DOI: 10.1142/3609

ABEL-FRET: tether-free single-molecule FRET with hydrodynamic profiling
journal, June 2021


Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex
journal, June 2016

  • Orf, Gregory S.; Saer, Rafael G.; Niedzwiedzki, Dariusz M.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 31
  • DOI: 10.1073/pnas.1603330113

In Vitro Reconstitution of the Cyanobacterial Photoprotective Mechanism Mediated by the Orange Carotenoid Protein in Synechocystis PCC 6803
journal, July 2011

  • Gwizdala, Michal; Wilson, Adjélé; Kirilovsky, Diana
  • The Plant Cell, Vol. 23, Issue 7
  • DOI: 10.1105/tpc.111.086884

The Crystal Structure of a Cyanobacterial Water-Soluble Carotenoid Binding Protein
journal, January 2003


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


Cyanobacterial Phycobilisomes
journal, December 1998


Resolving Mixtures in Solution by Single-Molecule Rotational Diffusivity
journal, July 2018


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

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

The structure and function of the LH2 (B800–850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050
journal, January 1997

  • Cogdell, Richard J.; Isaacs, Neil W.; Freer, Andy A.
  • Progress in Biophysics and Molecular Biology, Vol. 68, Issue 1
  • DOI: 10.1016/S0079-6107(97)00010-2

Structure-function relationships and energy transfer in phycobiliprotein antennae
journal, November 1991


Single-molecule trapping and spectroscopy reveals photophysical heterogeneity of phycobilisomes quenched by Orange Carotenoid Protein
journal, March 2019


Optical detection and spectroscopy of single molecules in a solid
journal, May 1989


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

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


The dynamics of structural deformations of immobilized single light-harvesting complexes
journal, September 1999

  • Bopp, M. A.; Sytnik, A.; Howard, T. D.
  • Proceedings of the National Academy of Sciences, Vol. 96, Issue 20
  • DOI: 10.1073/pnas.96.20.11271

Interferometric Scattering Enables Fluorescence-Free Electrokinetic Trapping of Single Nanoparticles in Free Solution
journal, May 2019


High resolution frequency selective photochemistry of phycobilisomes at cryogenic temperatures
journal, July 1988

  • Köhler, W.; Friedrich, J.; Fischer, R.
  • The Journal of Chemical Physics, Vol. 89, Issue 2
  • DOI: 10.1063/1.455209

Joint Detection of Change Points in Multichannel Single-Molecule Measurements
journal, December 2021


Fluorescence correlation spectroscopy. I. Conceptual basis and theory
journal, January 1974


Structure of phycobilisome from the red alga Griffithsia pacifica
journal, October 2017


Fluorescence Correlation Spectroscopy: Novel Variations of an Established Technique
journal, June 2007


A photoactive carotenoid protein acting as light intensity sensor
journal, August 2008

  • Wilson, A.; Punginelli, C.; Gall, A.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
  • DOI: 10.1073/pnas.0804636105

A functional compartmental model of the Synechocystis PCC 6803 phycobilisome
journal, July 2017

  • van Stokkum, Ivo H. M.; Gwizdala, Michal; Tian, Lijin
  • Photosynthesis Research, Vol. 135, Issue 1-3
  • DOI: 10.1007/s11120-017-0424-5

A Soluble Carotenoid Protein Involved in Phycobilisome-Related Energy Dissipation in Cyanobacteria
journal, March 2006

  • Wilson, Adjélé; Ajlani, Ghada; Verbavatz, Jean-Marc
  • The Plant Cell, Vol. 18, Issue 4
  • DOI: 10.1105/tpc.105.040121

The orange carotenoid protein of Synechocystis PCC 68031Publication No. 15377.1
journal, November 1997


Electrokinetic trapping at the one nanometer limit
journal, May 2011

  • Fields, A. P.; Cohen, A. E.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 22
  • DOI: 10.1073/pnas.1103554108

Controlling Light Harvesting with Light
journal, September 2016

  • Gwizdala, Michal; Berera, Rudi; Kirilovsky, Diana
  • Journal of the American Chemical Society, Vol. 138, Issue 36
  • DOI: 10.1021/jacs.6b04811

The amazing phycobilisome
journal, April 2020

  • Adir, Noam; Bar-Zvi, Shira; Harris, Dvir
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 4
  • DOI: 10.1016/j.bbabio.2019.07.002

Allophycocyanin and energy transfer
journal, July 2004


Single-Molecule Pump-Probe Detection Resolves Ultrafast Pathways in Individual and Coupled Quantum Systems
journal, February 2005

  • van Dijk, Erik M. H. P.; Hernando, Jordi; García-López, Juan-José
  • Physical Review Letters, Vol. 94, Issue 7
  • DOI: 10.1103/PhysRevLett.94.078302

Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: Assignment of excited state energies to the Lcm, β18 and αAP-B chromophores
journal, July 1994

  • Gindt, Yvonne M.; Zhou, Jianhui; Bryant, Donald A.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1186, Issue 3
  • DOI: 10.1016/0005-2728(94)90174-0

Vibronic Enhancement of Algae Light Harvesting
journal, December 2016


Revisiting the optical properties of the FMO protein
journal, March 2010

  • Milder, Maaike T. W.; Brüggemann, Ben; van Grondelle, Rienk
  • Photosynthesis Research, Vol. 104, Issue 2-3
  • DOI: 10.1007/s11120-010-9540-1

Direct single-molecule measurements of phycocyanobilin photophysics in monomeric C-phycocyanin
journal, August 2017

  • Squires, Allison H.; Moerner, W. E.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 37
  • DOI: 10.1073/pnas.1705435114

Spectroscopy of individual LH2 complexes of Rhodopseudomonas acidophila: localized excitations in the B800 band
journal, August 1999


Single-Molecule Fluorescence Spectroscopy of Photosynthetic Systems
journal, March 2016


Structure of cyanobacterial phycobilisome core revealed by structural modeling and chemical cross-linking
journal, January 2021

  • Liu, Haijun; Zhang, Mengru M.; Weisz, Daniel A.
  • Science Advances, Vol. 7, Issue 2
  • DOI: 10.1126/sciadv.aba5743

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

Photosynthesis of picoplankton in the oligotrophic ocean
journal, February 1983

  • Platt, Trevor; Rao, D. V. Subba; Irwin, Brian
  • Nature, Vol. 301, Issue 5902
  • DOI: 10.1038/301702a0

Method for trapping and manipulating nanoscale objects in solution
journal, February 2005

  • Cohen, Adam E.; Moerner, W. E.
  • Applied Physics Letters, Vol. 86, Issue 9
  • DOI: 10.1063/1.1872220