Discovery of Multiple Light-Harvesting States of the Photosynthetic Protein PE545

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

doi:10.1021/jacs.4c06307

Title: Discovery of Multiple Light-Harvesting States of the Photosynthetic Protein PE545

Journal Article · 25 September 2024 · Journal of the American Chemical Society

DOI: https://doi.org/10.1021/jacs.4c06307 · OSTI ID:2448543

Norris, Audrey C. ^[1];

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Massachusetts Institute of Technology (MIT), Cambridge, MA (United States); Massachusetts Institute of Technology
Princeton University, NJ (United States)
Virginia Commonwealth University, Richmond, VA (United States)
Massachusetts Institute of Technology (MIT), Cambridge, MA (United States)

Cryptophytes are photosynthetic microalga that flourish in a remarkable diversity of natural environments by using pigment-containing proteins with absorption maxima tuned to each ecological niche. While this diversity in the absorption has been well established, the subsequent photophysics is highly sensitive to the local protein environment and so may exhibit similar variation. Thermal fluctuations of the protein conformation are expected to introduce photophysical heterogeneity of the pigments that may have evolved important functional properties in a manner similar to that of the absorption. However, such heterogeneity is averaged out in ensemble measurements and, therefore, has not yet been probed. Here, we report single-molecule measurements of phycoerythrin 545 (PE545), the prototypical cryptophyte antenna protein, in its native dimeric form. A conformational ensemble was resolved consisting of distinct photophysical states with different light-harvesting properties. Proteins that did not quench, partially quenched, or fully quenched absorbed light were observed. Light intensity increased the quenched-state population of the dimer, potentially as a mechanism to deal with the extreme light intensities found in aqueous environments. Cross-linking, which mimics local interactions, introduces this light-dependent functionality while also suppressing other conformational dynamics. The cellular organization can, therefore, actively modulate the protein conformation and dynamics, selecting for distinct levels of light harvesting. Furthermore, the complex conformational equilibrium provides an additional mechanism for cryptophytes and likely other photosynthetic organisms to optimize solar energy capture and conversion.

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Research Organization:: BioLEC EFRC, Princeton, NJ (United States)

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

Grant/Contract Number:: SC0019370

OSTI ID:: 2448543

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 40 Vol. 146; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (49)

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
Spectral Variability in Phycocyanin Cryptophyte Antenna Complexes is Controlled by Changes in the α‐Polypeptide Chains Corbella, Marina; Cupellini, Lorenzo; Lipparini, Filippo ChemPhotoChem, Vol. 3, Issue 9 https://doi.org/10.1002/cptc.201900045	journal	May 2019
Light-Harvesting Systems in Chlorophyll c-Containing Algae Macpherson, Alisdair N.; Hiller, Roger G. Light-Harvesting Antennas in Photosynthesis https://doi.org/10.1007/978-94-017-2087-8_11	book	January 2003
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
Phycobiliprotein diffusion in chloroplasts of cryptophyte Rhodomonas CS24 Mirkovic, Tihana; Wilk, Krystyna E.; Curmi, Paul M. G. Photosynthesis Research, Vol. 100, Issue 1 https://doi.org/10.1007/s11120-009-9412-8	journal	February 2009
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
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
The organisation of photosynthetic pigments in a cryptophyte alga: A linear dichroism study Hiller, Roger G.; Scaramuzzi, Carol D.; Breton, Jacques Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1102, Issue 3 https://doi.org/10.1016/0005-2728(92)90135-O	journal	October 1992
Spectroscopy of Individual Light-Harvesting 2 Complexes of Rhodopseudomonas acidophila: Diagonal Disorder, Intercomplex Heterogeneity, Spectral Diffusion, and Energy Transfer in the B800 Band van Oijen, A. M.; Ketelaars, M.; Köhler, J. Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76709-9	journal	March 2000
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
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
Membrane-dependent heterogeneity of LHCII characterized using single-molecule spectroscopy Manna, Premashis; Davies, Thomas; Hoffmann, Madeline Biophysical Journal, Vol. 120, Issue 15 https://doi.org/10.1016/j.bpj.2021.06.010	journal	August 2021
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
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
The photophysics of cryptophyte light-harvesting Doust, Alexander B.; Wilk, Krystyna E.; Curmi, Paul M. G. Journal of Photochemistry and Photobiology A: Chemistry, Vol. 184, Issue 1-2 https://doi.org/10.1016/j.jphotochem.2006.06.006	journal	November 2006
Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms Mirkovic, Tihana; Ostroumov, Evgeny E.; Anna, Jessica M. Chemical Reviews, Vol. 117, Issue 2 https://doi.org/10.1021/acs.chemrev.6b00002	journal	March 2016
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
Vibronic Wavepackets and Energy Transfer in Cryptophyte Light-Harvesting Complexes Jumper, Chanelle C.; van Stokkum, Ivo H. M.; Mirkovic, Tihana The Journal of Physical Chemistry B, Vol. 122, Issue 24 https://doi.org/10.1021/acs.jpcb.8b02629	journal	May 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
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
Controllable Phycobilin Modification: An Alternative Photoacclimation Response in Cryptophyte Algae Spangler, Leah C.; Yu, Mina; Jeffrey, Philip D. ACS Central Science, Vol. 8, Issue 3 https://doi.org/10.1021/acscentsci.1c01209	journal	February 2022
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
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
Bilin Organization in Cryptomonad Biliproteins MacColl, Robert; Eisele, Leslie E.; Dhar, Manika Biochemistry, Vol. 38, Issue 13 https://doi.org/10.1021/bi982059c	journal	March 1999
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
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
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
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
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
Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature Collini, Elisabetta; Wong, Cathy Y.; Wilk, Krystyna E. Nature, Vol. 463, Issue 7281 https://doi.org/10.1038/nature08811	journal	February 2010
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
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
Solar light harvesting by energy transfer: from ecology to coherence Scholes, Gregory D.; Mirkovic, Tihana; Turner, Daniel B. Energy & Environmental Science, Vol. 5, Issue 11 https://doi.org/10.1039/c2ee23013e	journal	January 2012
Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins Harrop, Stephen J.; Wilk, Krystyna E.; Dinshaw, Rayomond Proceedings of the National Academy of Sciences, Vol. 111, Issue 26 https://doi.org/10.1073/pnas.1402538111	journal	June 2014
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
Orange carotenoid protein burrows into the phycobilisome to provide photoprotection Harris, Dvir; Tal, Ofir; Jallet, Denis Proceedings of the National Academy of Sciences, Vol. 113, Issue 12 https://doi.org/10.1073/pnas.1523680113	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
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
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
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
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
EFFECT OF LIGHT INTENSITY AND GLYCEROL ON THE GROWTH, PIGMENT COMPOSITION, AND ULTRASTRUCTURE OF CHROOMONAS SP.^1,^2,³ Faust, Maria A.; Gantt, Elisabeth Journal of Phycology, Vol. 9, Issue 4 https://doi.org/10.1111/j.1529-8817.1973.tb04125.x	journal	December 1973
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
Excitation Energy Transfer in the Cryptophytes. Fluorescence Excitation Spectra and Picosecond Time‐Resolved Emission Spectra of Intact Algae at 77 k Bruce, Doug; Biggins, John; Steiner, Tom Photochemistry and Photobiology, Vol. 44, Issue 4 https://doi.org/10.1111/j.1751-1097.1986.tb04702.x	journal	October 1986
Factors Controlling the Mobility of Photosynthetic Proteins ^† Mullineaux, Conrad W. Photochemistry and Photobiology, Vol. 84, Issue 6 https://doi.org/10.1111/j.1751-1097.2008.00420.x	journal	November 2008
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
Phycocyanin Sensitizes both Photosystem I and Photosystem II in Cryptophyte Chroomonas CCMP270 Cells van der Weij-De Wit, Chantal D.; Doust, Alexander B.; van Stokkum, Ivo H. M. Biophysical Journal, Vol. 94, Issue 6 https://doi.org/10.1529/biophysj.107.113993	journal	March 2008
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

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Cryptophytes
Dyes and pigments
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Monomers
Oligomers
Photosynthetic protein

Title: Discovery of Multiple Light-Harvesting States of the Photosynthetic Protein PE545

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References (49)

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