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

Squires, Allison; Wang, Quan; Dahlberg, Peter; Moerner, W. E.

doi:10.1063/5.0079042

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

Journal Article · 15 February 2022 · Journal of Chemical Physics

DOI: https://doi.org/10.1063/5.0079042 · OSTI ID:1843432

Squires, Allison ^[1]; Wang, Quan ^[2]; Dahlberg, Peter ^[3];

^[3]

Univ. of Chicago, IL (United States); Stanford University
Princeton Univ., NJ (United States)
Stanford Univ., CA (United States)

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.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Stanford Univ., CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC02-76SF00515; FG02-07ER15892

OSTI ID:: 1843432

Journal Information:: Journal of Chemical Physics, Journal Name: Journal of Chemical Physics Journal Issue: 7 Vol. 156; ISSN 0021-9606

Publisher:: American Institute of Physics (AIP)Copyright Statement

Country of Publication:: United States

Language:: English

References (68)

Revealing Conformational Variants of Solution-Phase Intrinsically Disordered Tau Protein at the Single-Molecule Level Manger, Lydia H.; Foote, Alexander K.; Wood, Sharla L. Angewandte Chemie International Edition, Vol. 56, Issue 49 https://doi.org/10.1002/anie.201708242	journal	November 2017
Fluorescence correlation spectroscopy. I. Conceptual basis and theory Elson, Elliot L.; Magde, Douglas Biopolymers, Vol. 13, Issue 1 https://doi.org/10.1002/bip.1974.360130102	journal	January 1974
Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at 2.3 Å resolution Brejc, Katjuša; Ficner, Ralf; Huber, Robert Journal of Molecular Biology, Vol. 249, Issue 2 https://doi.org/10.1006/jmbi.1995.0307	journal	January 1995
Cyanobacterial Phycobilisomes MacColl, Robert Journal of Structural Biology, Vol. 124, Issue 2-3 https://doi.org/10.1006/jsbi.1998.4062	journal	December 1998
Allophycocyanin B (?max 671, 618 nm): A new cyanobacterial phycobiliprotein Glazer, A. N.; Bryant, D. A. Archives of Microbiology, Vol. 104, Issue 1 https://doi.org/10.1007/BF00447294	journal	January 1975
Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant Adir, Noam Photosynthesis Research, Vol. 85, Issue 1 https://doi.org/10.1007/s11120-004-2143-y	journal	July 2005
Revisiting the optical properties of the FMO protein Milder, Maaike T. W.; Brüggemann, Ben; van Grondelle, Rienk Photosynthesis Research, Vol. 104, Issue 2-3 https://doi.org/10.1007/s11120-010-9540-1	journal	March 2010
Resolving the contribution of the uncoupled phycobilisomes to cyanobacterial pulse-amplitude modulated (PAM) fluorometry signals Acuña, Alonso M.; Snellenburg, Joris J.; Gwizdala, Michal Photosynthesis Research, Vol. 127, Issue 1 https://doi.org/10.1007/s11120-015-0141-x	journal	April 2015
A functional compartmental model of the Synechocystis PCC 6803 phycobilisome van Stokkum, Ivo H. M.; Gwizdala, Michal; Tian, Lijin Photosynthesis Research, Vol. 135, Issue 1-3 https://doi.org/10.1007/s11120-017-0424-5	journal	July 2017
A carotenoid-protein from cyanobacteria Kay Holt, Thomas; Krogmann, David W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 637, Issue 3 https://doi.org/10.1016/0005-2728(81)90045-1	journal	October 1981
Spectroscopic studies of phycobilisome subcore preparations lacking key core chromophores: Assignment of excited state energies to the Lcm, β18 and αAP-B chromophores Gindt, Yvonne M.; Zhou, Jianhui; Bryant, Donald A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1186, Issue 3 https://doi.org/10.1016/0005-2728(94)90174-0	journal	July 1994
The orange carotenoid protein of Synechocystis PCC 68031Publication No. 15377.1 Wu, Yi Pyng; Krogmann, David W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1322, Issue 1 https://doi.org/10.1016/S0005-2728(97)00067-4	journal	November 1997
The structure and function of the LH2 (B800–850) complex from the purple photosynthetic bacterium Rhodopseudomonas acidophila strain 10050 Cogdell, Richard J.; Isaacs, Neil W.; Freer, Andy A. Progress in Biophysics and Molecular Biology, Vol. 68, Issue 1 https://doi.org/10.1016/S0079-6107(97)00010-2	journal	January 1997
Spectroscopy of individual LH2 complexes of Rhodopseudomonas acidophila: localized excitations in the B800 band van Oijen, A. M.; Ketelaars, M.; Köhler, J. Chemical Physics, Vol. 247, Issue 1 https://doi.org/10.1016/S0301-0104(99)00105-6	journal	August 1999
The Crystal Structure of a Cyanobacterial Water-Soluble Carotenoid Binding Protein Kerfeld, Cheryl A.; Sawaya, Michael R.; Brahmandam, Vishnu Structure, Vol. 11, Issue 1 https://doi.org/10.1016/S0969-2126(02)00936-X	journal	January 2003
Allophycocyanin and energy transfer MacColl, Robert Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1657, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.04.005	journal	July 2004
The amazing phycobilisome Adir, Noam; Bar-Zvi, Shira; Harris, Dvir Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 4 https://doi.org/10.1016/j.bbabio.2019.07.002	journal	April 2020
Picosecond Kinetics of Light Harvesting and Photoprotective Quenching in Wild-Type and Mutant Phycobilisomes Isolated from the Cyanobacterium Synechocystis PCC 6803 Tian, Lijin; Gwizdala, Michal; van Stokkum, Ivo H. M. Biophysical Journal, Vol. 102, Issue 7 https://doi.org/10.1016/j.bpj.2012.03.008	journal	April 2012
Vibronic Enhancement of Algae Light Harvesting Dean, Jacob C.; Mirkovic, Tihana; Toa, Zi S. D. Chem, Vol. 1, Issue 6 https://doi.org/10.1016/j.chempr.2016.11.002	journal	December 2016
Light guides Glazer, A. N. Journal of Biological Chemistry, Vol. 264, Issue 1 https://doi.org/10.1016/s0021-9258(17)31212-7	journal	January 1989
Single-Molecule Fluorescence Spectroscopy of Photosynthetic Systems Kondo, Toru; Chen, Wei Jia; Schlau-Cohen, Gabriela S. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00195	journal	March 2016
Joint Detection of Change Points in Multichannel Single-Molecule Measurements Wilson, Hugh; Wang, Quan The Journal of Physical Chemistry B, Vol. 125, Issue 49 https://doi.org/10.1021/acs.jpcb.1c08869	journal	December 2021
Single-Molecule Identification of Quenched and Unquenched States of LHCII Schlau-Cohen, Gabriela S.; Yang, Hsiang-Yu; Krüger, Tjaart P. J. The Journal of Physical Chemistry Letters, Vol. 6, Issue 5 https://doi.org/10.1021/acs.jpclett.5b00034	journal	February 2015
Resolving Mixtures in Solution by Single-Molecule Rotational Diffusivity Yang, Hsiang-Yu; Moerner, W. E. Nano Letters, Vol. 18, Issue 8 https://doi.org/10.1021/acs.nanolett.8b02280	journal	July 2018
Interferometric Scattering Enables Fluorescence-Free Electrokinetic Trapping of Single Nanoparticles in Free Solution Squires, Allison H.; Lavania, Abhijit A.; Dahlberg, Peter D. Nano Letters, Vol. 19, Issue 6 https://doi.org/10.1021/acs.nanolett.9b01514	journal	May 2019
Probing Single Biomolecules in Solution Using the Anti-Brownian Electrokinetic (ABEL) Trap Wang, Quan; Goldsmith, Randall H.; Jiang, Yan Accounts of Chemical Research, Vol. 45, Issue 11 https://doi.org/10.1021/ar200304t	journal	March 2012
Electronic Absorption Spectra from MM and ab Initio QM/MM Molecular Dynamics: Environmental Effects on the Absorption Spectrum of Photoactive Yellow Protein Isborn, Christine M.; Götz, Andreas W.; Clark, Matthew A. Journal of Chemical Theory and Computation, Vol. 8, Issue 12 https://doi.org/10.1021/ct3006826	journal	September 2012
Controlling Light Harvesting with Light Gwizdala, Michal; Berera, Rudi; Kirilovsky, Diana Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b04811	journal	September 2016
Lifetime and Spectrally Resolved Characterization of the Photodynamics of Single Fluorophores in Solution Using the Anti-Brownian Electrokinetic Trap Wang, Quan; Moerner, W. E. The Journal of Physical Chemistry B, Vol. 117, Issue 16 https://doi.org/10.1021/jp308949d	journal	November 2012
Fluorescence Spectroscopy, Exciton Dynamics, and Photochemistry of Single Allophycocyanin Trimers Ying, Liming; Xie, X. Sunney The Journal of Physical Chemistry B, Vol. 102, Issue 50 https://doi.org/10.1021/jp983227d	journal	December 1998
An Adaptive Anti-Brownian Electrokinetic Trap with Real-Time Information on Single-Molecule Diffusivity and Mobility Wang, Quan; Moerner, W. E. ACS Nano, Vol. 5, Issue 7 https://doi.org/10.1021/nn2014968	journal	June 2011
Photosynthesis of picoplankton in the oligotrophic ocean Platt, Trevor; Rao, D. V. Subba; Irwin, Brian Nature, Vol. 301, Issue 5902 https://doi.org/10.1038/301702a0	journal	February 1983
Structure of phycobilisome from the red alga Griffithsia pacifica Zhang, Jun; Ma, Jianfei; Liu, Desheng Nature, Vol. 551, Issue 7678 https://doi.org/10.1038/nature24278	journal	October 2017
Single-molecule spectroscopy of LHCSR1 protein dynamics identifies two distinct states responsible for multi-timescale photosynthetic photoprotection Kondo, Toru; Pinnola, Alberta; Chen, Wei Jia Nature Chemistry, Vol. 9, Issue 8 https://doi.org/10.1038/nchem.2818	journal	July 2017
Watching conformational- and photodynamics of single fluorescent proteins in solution Goldsmith, Randall H.; Moerner, W. E. Nature Chemistry, Vol. 2, Issue 3 https://doi.org/10.1038/nchem.545	journal	January 2010
Single-molecule motions enable direct visualization of biomolecular interactions in solution Wang, Quan; Moerner, W. E. Nature Methods, Vol. 11, Issue 5 https://doi.org/10.1038/nmeth.2882	journal	March 2014
Single-molecule trapping and spectroscopy reveals photophysical heterogeneity of phycobilisomes quenched by Orange Carotenoid Protein Squires, Allison H.; Dahlberg, Peter D.; Liu, Haijun Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-09084-2	journal	March 2019
Structural insight into the mechanism of energy transfer in cyanobacterial phycobilisomes Zheng, Lvqin; Zheng, Zhenggao; Li, Xiying Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-25813-y	journal	September 2021
ABEL-FRET: tether-free single-molecule FRET with hydrodynamic profiling Wilson, Hugh; Wang, Quan Nature Methods, Vol. 18, Issue 7 https://doi.org/10.1038/s41592-021-01173-9	journal	June 2021
Single-molecule spectroscopy of photosynthetic proteins in solution: exploration of structure–function relationships Schlau-Cohen, Gabriela S.; Bockenhauer, Samuel; Wang, Quan Chem. Sci., Vol. 5, Issue 8 https://doi.org/10.1039/C4SC00582A	journal	January 2014
Method for trapping and manipulating nanoscale objects in solution Cohen, Adam E.; Moerner, W. E. Applied Physics Letters, Vol. 86, Issue 9 https://doi.org/10.1063/1.1872220	journal	February 2005
High resolution frequency selective photochemistry of phycobilisomes at cryogenic temperatures Köhler, W.; Friedrich, J.; Fischer, R. The Journal of Chemical Physics, Vol. 89, Issue 2 https://doi.org/10.1063/1.455209	journal	July 1988
Single-molecule diffusometry reveals the nucleotide-dependent oligomerization pathways of Nicotiana tabacum Rubisco activase Wang, Quan; Serban, Andrew J.; Wachter, Rebekka M. The Journal of Chemical Physics, Vol. 148, Issue 12 https://doi.org/10.1063/1.5005930	journal	March 2018
Suppressing Brownian motion of individual biomolecules in solution Cohen, A. E.; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 103, Issue 12 https://doi.org/10.1073/pnas.0509976103	journal	March 2006
A photoactive carotenoid protein acting as light intensity sensor Wilson, A.; Punginelli, C.; Gall, A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 33 https://doi.org/10.1073/pnas.0804636105	journal	August 2008
Electrokinetic trapping at the one nanometer limit Fields, A. P.; Cohen, A. E. Proceedings of the National Academy of Sciences, Vol. 108, Issue 22 https://doi.org/10.1073/pnas.1103554108	journal	May 2011
Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states Schlau-Cohen, G. S.; Wang, Q.; Southall, J. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1310222110	journal	June 2013
Local and global structural drivers for the photoactivation of the orange carotenoid protein Gupta, Sayan; Guttman, Miklos; Leverenz, Ryan L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 41 https://doi.org/10.1073/pnas.1512240112	journal	September 2015
Dissecting pigment architecture of individual photosynthetic antenna complexes in solution Wang, Quan; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 112, Issue 45 https://doi.org/10.1073/pnas.1514027112	journal	October 2015
Evidence for a cysteine-mediated mechanism of excitation energy regulation in a photosynthetic antenna complex Orf, Gregory S.; Saer, Rafael G.; Niedzwiedzki, Dariusz M. Proceedings of the National Academy of Sciences, Vol. 113, Issue 31 https://doi.org/10.1073/pnas.1603330113	journal	June 2016
Direct single-molecule measurements of phycocyanobilin photophysics in monomeric C-phycocyanin Squires, Allison H.; Moerner, W. E. Proceedings of the National Academy of Sciences, Vol. 114, Issue 37 https://doi.org/10.1073/pnas.1705435114	journal	August 2017
Prokaryotes: The unseen majority Whitman, W. B.; Coleman, D. C.; Wiebe, W. J. Proceedings of the National Academy of Sciences, Vol. 95, Issue 12 https://doi.org/10.1073/pnas.95.12.6578	journal	June 1998
The dynamics of structural deformations of immobilized single light-harvesting complexes Bopp, M. A.; Sytnik, A.; Howard, T. D. Proceedings of the National Academy of Sciences, Vol. 96, Issue 20 https://doi.org/10.1073/pnas.96.20.11271	journal	September 1999
Phycobilisome rod mutants in Synechocystis sp. strain PCC6803 Ughy, B. Microbiology, Vol. 150, Issue 12 https://doi.org/10.1099/mic.0.27498-0	journal	December 2004
Optical detection and spectroscopy of single molecules in a solid Moerner, W. E.; Kador, L. Physical Review Letters, Vol. 62, Issue 21 https://doi.org/10.1103/PhysRevLett.62.2535	journal	May 1989
Single-Molecule Pump-Probe Detection Resolves Ultrafast Pathways in Individual and Coupled Quantum Systems van Dijk, Erik M. H. P.; Hernando, Jordi; García-López, Juan-José Physical Review Letters, Vol. 94, Issue 7 https://doi.org/10.1103/PhysRevLett.94.078302	journal	February 2005
A Soluble Carotenoid Protein Involved in Phycobilisome-Related Energy Dissipation in Cyanobacteria Wilson, Adjélé; Ajlani, Ghada; Verbavatz, Jean-Marc The Plant Cell, Vol. 18, Issue 4 https://doi.org/10.1105/tpc.105.040121	journal	March 2006
In Vitro Reconstitution of the Cyanobacterial Photoprotective Mechanism Mediated by the Orange Carotenoid Protein in Synechocystis PCC 6803 Gwizdala, Michal; Wilson, Adjélé; Kirilovsky, Diana The Plant Cell, Vol. 23, Issue 7 https://doi.org/10.1105/tpc.111.086884	journal	July 2011
Structure of C-phycocyanin from Spirulina platensis at 2.2 Å resolution: a novel monoclinic crystal form for phycobiliproteins in phycobilisomes Wang, Xin-Quan; Li, Le-Nong; Chang, Wen-Rui Acta Crystallographica Section D Biological Crystallography, Vol. 57, Issue 6 https://doi.org/10.1107/s0907444901004528	journal	May 2001
Structure-function relationships and energy transfer in phycobiliprotein antennae Holzwarth, Alfred R. Physiologia Plantarum, Vol. 83, Issue 3 https://doi.org/10.1111/j.1399-3054.1991.tb00129.x	journal	November 1991
Structure of cyanobacterial phycobilisome core revealed by structural modeling and chemical cross-linking Liu, Haijun; Zhang, Mengru M.; Weisz, Daniel A. Science Advances, Vol. 7, Issue 2 https://doi.org/10.1126/sciadv.aba5743	journal	January 2021
Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria Liu, H.; Zhang, H.; Niedzwiedzki, D. M. Science, Vol. 342, Issue 6162 https://doi.org/10.1126/science.1242321	journal	November 2013
Photosynthetic Excitons van Amerongen, Herbert; van Grondelle, Rienk; Valkunas, Leonas World Scientific https://doi.org/10.1142/3609	book	January 2000
Light Harvesting by Phycobilisomes Glazer, A. N. Annual Review of Biophysics and Biophysical Chemistry, Vol. 14, Issue 1, p. 47-77 https://doi.org/10.1146/annurev.bb.14.060185.000403	journal	June 1985
Fluorescence Correlation Spectroscopy: Novel Variations of an Established Technique Haustein, Elke; Schwille, Petra Annual Review of Biophysics and Biomolecular Structure, Vol. 36, Issue 1 https://doi.org/10.1146/annurev.biophys.36.040306.132612	journal	June 2007
Spectrally-tunable femtosecond single-molecule pump-probe spectroscopy Moya, Raymundo; Kondo, Toru; Norris, Audrey C. Optics Express, Vol. 29, Issue 18 https://doi.org/10.1364/OE.432995	journal	January 2021
Single-Molecule Spectroscopy Selectively Probes Donor and Acceptor Chromophores in the Phycobiliprotein Allophycocyanin Loos, Davey; Cotlet, Mircea; De Schryver, Frans Biophysical Journal, Vol. 87, Issue 4 https://doi.org/10.1529/biophysj.104.046219	journal	October 2004
Microphytobenthos: The Ecological Role of the "Secret Garden" of Unvegetated, Shallow-Water Marine Habitats. I. Distribution, Abundance and Primary Production MacIntyre, Hugh L.; Geider, Richard J.; Miller, Douglas C. Estuaries, Vol. 19, Issue 2 https://doi.org/10.2307/1352224	journal	June 1996

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