Observation of conformational dynamics in single light-harvesting proteins from cryptophyte algae

Moya, Raymundo; Norris, Audrey C.; Spangler, Leah C.; Scholes, Gregory D.; Schlau-Cohen, Gabriela S.

doi:10.1063/5.0095763

Title: Observation of conformational dynamics in single light-harvesting proteins from cryptophyte algae

Journal Article · Tue Jul 19 00:00:00 EDT 2022 · Journal of Chemical Physics

DOI:https://doi.org/10.1063/5.0095763· OSTI ID:1908531

Moya, Raymundo ^[1]; Norris, Audrey C. ^[1]; Spangler, Leah C. ^[2];

^[2];

^[1]

Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Princeton Univ., NJ (United States)

Photosynthetic organisms use pigment–protein complexes to capture the sunlight that powers most life on earth. Within these complexes, the position of the embedded pigments is all optimized for light harvesting. At the same time, the protein scaffold undergoes thermal fluctuations that vary the structure, and, thus, photophysics, of the complexes. While these variations are averaged out in ensemble measurements, single-molecule spectroscopy provides the ability to probe these conformational changes. We used single-molecule fluorescence spectroscopy to identify the photophysical substates reflective of distinct conformations and the associated conformational dynamics in phycoerythrin 545 (PE545), a pigment–protein complex from cryptophyte algae. Rapid switching between photophysical states was observed, indicating that ensemble measurements average over a conformational equilibrium. A highly quenched conformation was also identified, and its population increased under high light. This discovery establishes that PE545 has the characteristics to serve as a photoprotective site. Finally, unlike homologous proteins from the evolutionarily related cyanobacteria and red algae, quenching was not observed upon photobleaching, which may allow for robust photophysics without the need for rapid repair or replacement machinery. Collectively, these observations establish the presence of a rich and robust set of conformational states of PE545. Cryptophytes exhibit particularly diverse energetics owing to the variety of microenvironments in which they survive, and the conformational states and dynamics reported here may provide photophysical flexibility that contributes to their remarkable ability to flourish under diverse conditions.

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Research Organization:: Princeton Univ., NJ (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC) Basic Energy Sciences (BES); USDOE

Grant/Contract Number:: SC0019370

OSTI ID:: 1908531

Alternate ID(s):: OSTI ID: 1876660

Journal Information:: Journal of Chemical Physics, Vol. 157, Issue 3; ISSN 0021-9606

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

Country of Publication:: United States

Language:: English

References (46)

How Energy Funnels from the Phycoerythrin Antenna Complex to Photosystem I and Photosystem II in Cryptophyte Rhodomonas CS24 Cells van der Weij-De Wit, Chantal D.; Doust, Alexander B.; van Stokkum, Ivo H. M. The Journal of Physical Chemistry B, Vol. 110, Issue 49 https://doi.org/10.1021/jp061546w	journal	November 2006
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
Structural dynamics of potassium-channel gating revealed by single-molecule FRET Wang, Shizhen; Vafabakhsh, Reza; Borschel, William F. Nature Structural & Molecular Biology, Vol. 23, Issue 1 https://doi.org/10.1038/nsmb.3138	journal	December 2015
Unique Location of the Phycobiliprotein Light-Harvesting Pigment in the Cryptophyceae Spear-bernstein, Laurel; Miller, Kenneth R. Journal of Phycology, Vol. 25, Issue 3 https://doi.org/10.1111/j.1529-8817.1989.tb00245.x	journal	September 1989
Developing a Structure–Function Model for the Cryptophyte Phycoerythrin 545 Using Ultrahigh Resolution Crystallography and Ultrafast Laser Spectroscopy Doust, Alexander B.; Marai, Christopher N. J.; Harrop, Stephen J. Journal of Molecular Biology, Vol. 344, Issue 1 https://doi.org/10.1016/j.jmb.2004.09.044	journal	November 2004
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
Excitation-energy redistribution in the cryptomonad alga Cryptomonas ovata Snyder, Ursula K.; Biggins, John Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 892, Issue 1 https://doi.org/10.1016/0005-2728(87)90246-5	journal	June 1987
Chloroplast Structure of the Cryptophyceae Gantt, E.; Edwards, M. R.; Provasoli, L. Journal of Cell Biology, Vol. 48, Issue 2 https://doi.org/10.1083/jcb.48.2.280	journal	February 1971
Application of spectrally resolved fluorescence induction to study light-induced nonphotochemical quenching in algae Kaňa, R. Photosynthetica, Vol. 56, Issue SPECIAL ISSUE https://doi.org/10.1007/s11099-018-0780-1	journal	March 2018
Toward dynamic structural biology: Two decades of single-molecule Förster resonance energy transfer Lerner, Eitan; Cordes, Thorben; Ingargiola, Antonino Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aan1133	journal	January 2018
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
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
Initial Transcription by RNA Polymerase Proceeds Through a DNA-Scrunching Mechanism Kapanidis, A. N.; Margeat, E.; Ho, S. O. Science, Vol. 314, Issue 5802 https://doi.org/10.1126/science.1131399	journal	November 2006
Generation and identification of the transient intermediates of allophycocyanin by laser photolytic and pulse radiolytic techniques Su-Ping, Zhang; Jing-Xi, Pan; Zhen-Hui, Han International Journal of Radiation Biology, Vol. 77, Issue 5 https://doi.org/10.1080/095530000110039725	journal	January 2001
Switching an Individual Phycobilisome Off and On Gwizdala, Michal; Botha, Joshua L.; Wilson, Adjélé The Journal of Physical Chemistry Letters, Vol. 9, Issue 9 https://doi.org/10.1021/acs.jpclett.8b00767	journal	April 2018
Proteomic analysis of the phycobiliprotein antenna of the cryptophyte alga Guillardia theta cultured under different light intensities Kieselbach, Thomas; Cheregi, Otilia; Green, Beverley R. Photosynthesis Research, Vol. 135, Issue 1-3 https://doi.org/10.1007/s11120-017-0400-0	journal	May 2017
Detection of Intensity Change Points in Time-Resolved Single-Molecule Measurements Watkins, Lucas P.; Yang, Haw The Journal of Physical Chemistry B, Vol. 109, Issue 1 https://doi.org/10.1021/jp0467548	journal	January 2005
Photoblinking of Rhodamine 6G in Poly(vinyl alcohol): Radical Dark State Formed through the Triplet Zondervan, Rob; Kulzer, Florian; Orlinskii, Sergei B. The Journal of Physical Chemistry A, Vol. 107, Issue 35 https://doi.org/10.1021/jp034723r	journal	August 2003
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
Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: Crystal structure of a cryptophyte phycoerythrin at 1.63-A resolution Wilk, K. E.; Harrop, S. J.; Jankova, L. Proceedings of the National Academy of Sciences, Vol. 96, Issue 16 https://doi.org/10.1073/pnas.96.16.8901	journal	August 1999
Spectral Heterogeneity in Single Light-harvesting Chlorosomes from Green Sulfur Photosynthetic Bacterium Chlorobium tepidum¶ Saga, Yoshitaka; Wazawa, Tetsuichi; Mizoguchi, Tadashi Photochemistry and Photobiology, Vol. 75, Issue 4 https://doi.org/10.1562/0031-8655(2002)0750433SHISLH2.0.CO2	journal	April 2002
The role of far-red spectral states in the energy regulation of phycobilisomes Krüger, Tjaart P. J.; van Grondelle, Rienk; Gwizdala, Michal Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 4 https://doi.org/10.1016/j.bbabio.2019.01.007	journal	April 2019
Charge transfer states in phycobilisomes Wahadoszamen, Md.; Krüger, Tjaart P. J.; Ara, Anjue Mane Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 7 https://doi.org/10.1016/j.bbabio.2020.148187	journal	July 2020
Kinetics of allophycocyanin's trimer-monomer equilibrium Huang, Cinnia; Berns, Donald S.; MacColl, Robert Biochemistry, Vol. 26, Issue 1 https://doi.org/10.1021/bi00375a033	journal	January 1987
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
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
Fluorescence and photobleaching dynamics of single light-harvesting complexes Bopp, M. A.; Jia, Y.; Li, L. Proceedings of the National Academy of Sciences, Vol. 94, Issue 20 https://doi.org/10.1073/pnas.94.20.10630	journal	September 1997
Photoprotective, excited-state quenching mechanisms in diverse photosynthetic organisms Magdaong, Nikki Cecil M.; Blankenship, Robert E. Journal of Biological Chemistry, Vol. 293, Issue 14 https://doi.org/10.1074/jbc.tm117.000233	journal	January 2018
Enzymatic Oxygen Scavenging for Photostability without pH Drop in Single-Molecule Experiments Swoboda, Marko; Henig, Jörg; Cheng, Hsin-Mei ACS Nano, Vol. 6, Issue 7 https://doi.org/10.1021/nn301895c	journal	June 2012
Phycoerythrin 545: Monomers, Energy Migration, Bilin Topography, and Monomer/Dimer Equilibrium MacColl, Robert; Malak, Henryk; Gryczynski, Ignacy Biochemistry, Vol. 37, Issue 1 https://doi.org/10.1021/bi971453s	journal	January 1998
Cooperative Subunit Refolding of a Light‐Harvesting Protein through a Self‐Chaperone Mechanism Laos, Alistair J.; Dean, Jacob C.; Toa, Zi S. D. Angewandte Chemie, Vol. 129, Issue 29 https://doi.org/10.1002/ange.201607921	journal	February 2017
Fluorescence Spectral Fluctuations of Single LH2 Complexes from Rhodopseudomonas acidophila Strain 10050 ^† Rutkauskas, Danielis; Novoderezkhin, Vladimir; Cogdell, Richard J. Biochemistry, Vol. 43, Issue 15 https://doi.org/10.1021/bi0497648	journal	April 2004
Energy Flow in the Cryptophyte PE545 Antenna Is Directed by Bilin Pigment Conformation Curutchet, Carles; Novoderezhkin, Vladimir I.; Kongsted, Jacob The Journal of Physical Chemistry B, Vol. 117, Issue 16 https://doi.org/10.1021/jp305033d	journal	October 2012
Non-Photochemical Quenching in Cryptophyte Alga Rhodomonas salina Is Located in Chlorophyll a/c Antennae Kaňa, Radek; Kotabová, Eva; Sobotka, Roman PLoS ONE, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pone.0029700	journal	January 2012
Presence of state transitions in the cryptophyte alga Guillardia theta Cheregi, Otilia; Kotabová, Eva; Prášil, Ondřej Journal of Experimental Botany, Vol. 66, Issue 20 https://doi.org/10.1093/jxb/erv362	journal	August 2015
Function, regulation and distribution of IsiA, a membrane-bound chlorophyll a-antenna protein in cyanobacteria Chen, H. -Y. S.; Bandyopadhyay, A.; Pakrasi, H. B. Photosynthetica, Vol. 56, Issue 1 https://doi.org/10.1007/s11099-018-0787-7	journal	January 2018
Immobility of phycobilins in the thylakoid lumen of a cryptophyte suggests that protein diffusion in the lumen is very restricted Kaňa, Radek; Prášil, Ondřej; Mullineaux, Conrad W. FEBS Letters, Vol. 583, Issue 4 https://doi.org/10.1016/j.febslet.2009.01.016	journal	January 2009
An Oxygen Scavenging System for Improvement of Dye Stability in Single-Molecule Fluorescence Experiments Aitken, Colin Echeverría; Marshall, R. Andrew; Puglisi, Joseph D. Biophysical Journal, Vol. 94, Issue 5 https://doi.org/10.1529/biophysj.107.117689	journal	March 2008
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
Phycocyanin: One Complex, Two States, Two Functions Gwizdala, Michal; Krüger, Tjaart P. J.; Wahadoszamen, Md. The Journal of Physical Chemistry Letters, Vol. 9, Issue 6 https://doi.org/10.1021/acs.jpclett.8b00621	journal	March 2018
High light stress and the one-helix LHC-like proteins of the cryptophyte Guillardia theta Funk, Christiane; Alami, Meriem; Tibiletti, Tania Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 7 https://doi.org/10.1016/j.bbabio.2011.03.011	journal	July 2011
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
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
Excitation Dynamics in Phycoerythrin 545: Modeling of Steady-State Spectra and Transient Absorption with Modified Redfield Theory Novoderezhkin, Vladimir I.; Doust, Alexander B.; Curutchet, Carles Biophysical Journal, Vol. 99, Issue 2 https://doi.org/10.1016/j.bpj.2010.04.039	journal	July 2010
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
Evolution of the Phycobiliproteins Apt, Kirk E.; Collier, Jackie L.; Grossman, Arthur R. Journal of Molecular Biology, Vol. 248, Issue 1 https://doi.org/10.1006/jmbi.1995.0203	journal	April 1995

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