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Excited-State Properties of Canthaxanthin in Cyanobacterial Carotenoid-Binding Proteins HCP2 and HCP3

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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Phys. Chem. B 2020, 124, 24, 4896-4905
    B: Biophysics; Physical Chemistry of Biological Systems and Biomolecules

    Excited-State Properties of Canthaxanthin in Cyanobacterial Carotenoid-Binding Proteins HCP2 and HCP3
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    • Tuhin Khan
      Tuhin Khan
      Institute of Physics, Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic
      More by Tuhin Khan
      Orcidhttp://orcid.org/0000-0002-2790-3002
    • Maria Agustina Dominguez-Martin
      Maria Agustina Dominguez-Martin
      Environmental Genomics and Systems Biology and Molecular Biophysics and Integrated Bioimaging Divisions, Lawrence Berkeley National Laboratory, Berkeley, California 94720, United States
      MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, Michigan 48824, United States
      More by Maria Agustina Dominguez-Martin
    • Ivana Šímová
      Ivana Šímová
      Institute of Physics, Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic
      More by Ivana Šímová
    • Marcel Fuciman
      Marcel Fuciman
      Institute of Physics, Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic
      More by Marcel Fuciman
      Orcidhttp://orcid.org/0000-0002-0004-528X
    • Cheryl A. Kerfeld
      Cheryl A. Kerfeld
      Environmental Genomics and Systems Biology and Molecular Biophysics and Integrated Bioimaging Divisions, Lawrence Berkeley National Laboratory, Berkeley, California 94720, United States
      MSU-DOE Plant Research Laboratory  and  Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824, United States
      More by Cheryl A. Kerfeld
      Orcidhttp://orcid.org/0000-0002-9977-8482
    • Tomáš Polívka*
      Tomáš Polívka
      Institute of Physics, Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic
      *Email: [email protected]
      More by Tomáš Polívka
      Orcidhttp://orcid.org/0000-0002-6176-0420
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    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2020, 124, 24, 4896–4905
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.0c03137
    Published May 21, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Recently a new family of carotenoproteins, homologues of the N-terminal domain of the orange carotenoid protein (NTD-OCP), have been identified in cyanobacteria. These homologues are called helical carotenoid proteins (HCPs) as they are all predicted to maintain the all-helical structure of the NTD-OCP and to bind carotenoids. Here, HCP2 and HCP3 isolated from the cyanobacterium Tolypothrix PCC 7601 were studied by ultrafast transient absorption spectroscopy to explore the excited-state dynamics of the bound carotenoid, canthaxanthin. The lowest excited state, S1, of canthaxanthin in both HCPs yields a lifetime of 3.5 ps; it is thus shorter than for canthaxanthin in solution (4.5 ps). This is because of the longer effective conjugation of canthaxanthin in HCPs, as one of the terminal rings is in an s-trans configuration. Use of two different excitation wavelengths, 470 and 570 nm, revealed excitation wavelength dependent spectroscopic response. Additional excited-state absorption bands are observed after excitation at 470 nm for both HCPs, proving the presence of more than one ground state conformer.

    Copyright © 2020 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.jpcb.0c03137.

    • Canthaxanthin decay in methanol and effect of chloroform (Figure S1); SDS-PAGE of HCPs (Figure S2); white light continuum and its S/N ratio (Figure S3); comparison of HCP2 and canthaxanthin fwhm (Figure S4); canthaxanthin in methanol global analysis (Figure S5); near-IR decay of HCPs (Figure S6); 470 nm pumped S1 decay of HCPs (Figure S7); comparison of S1 and S* decay (Figure S8); carotenoid binding pockets of HCPs (Figure S9); 570 nm pumped TA spectra of HCPs (Figure S10); LED irradiated absorption spectra of HCP3 (Figure S11); electrostatic potential of HCPs/RCP (Figure S12); electrostatic potential of carotenoid binding pockets (Figure S13); carotenoid analysis of HCP3 (Table S1) (PDF)

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    Cited By

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    This article is cited by 15 publications.

    1. Nicoletta Liguori, Ivo H.M. van Stokkum, Fernando Muzzopappa, John T. M. Kennis, Diana Kirilovsky, Roberta Croce. The Orange Carotenoid Protein Triggers Cyanobacterial Photoprotection by Quenching Bilins via a Structural Switch of Its Carotenoid. Journal of the American Chemical Society 2024, 146 (31) , 21913-21921. https://doi.org/10.1021/jacs.4c06695
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    3. Steve Meech. Virtual Issue on Ultrafast Spectroscopy. The Journal of Physical Chemistry B 2021, 125 (23) , 6037-6039. https://doi.org/10.1021/acs.jpcb.1c04148
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    5. Natalia B. Pigni, Kevin L. Clark, Warren F. Beck, José A. Gascón. Spectral Signatures of Canthaxanthin Translocation in the Orange Carotenoid Protein. The Journal of Physical Chemistry B 2020, 124 (50) , 11387-11395. https://doi.org/10.1021/acs.jpcb.0c08756
    6. Yadu Ram Panthi, Muhammed Arshad Thottappali, Petra Horáková, Lubomír Kubáč, Jiří Pfleger, Miroslav Menšík, Tuhin Khan. Photophysics of Benzoxazole and Dicyano Functionalised Diketopyrrolopyrrole Derivatives: Insights into Ultrafast Processes and the Triplet State. ChemPhysChem 2024, 25 (13) https://doi.org/10.1002/cphc.202300872
    7. Jenia Sklyar, Adjélé Wilson, Diana Kirilovsky, Noam Adir. Insights into energy quenching mechanisms and carotenoid uptake by orange carotenoid protein homologs: HCP4 and CTDH. International Journal of Biological Macromolecules 2024, 265 , 131028. https://doi.org/10.1016/j.ijbiomac.2024.131028
    8. Amanda Arcidiacono, Davide Accomasso, Lorenzo Cupellini, Benedetta Mennucci. How orange carotenoid protein controls the excited state dynamics of canthaxanthin. Chemical Science 2023, 14 (40) , 11158-11169. https://doi.org/10.1039/D3SC02662K
    9. Yi-Wen Yang, Ke Liu, Da Huang, Chen Yu, Si-Zhuo Chen, Min Chen, Bao-Sheng Qiu. Functional specialization of expanded orange carotenoid protein paralogs in subaerial Nostoc species. Plant Physiology 2023, 192 (4) , 2640-2655. https://doi.org/10.1093/plphys/kiad234
    10. Tuhin Khan, Valentyna Kuznetsova, Maria Agustina Dominguez‐Martin, Cheryl A. Kerfeld, Tomáš Polívka. UV Excitation of Carotenoid Binding Proteins OCP and HCP: Excited‐State Dynamics and Product Formation. ChemPhotoChem 2022, 6 (1) https://doi.org/10.1002/cptc.202100194
    11. D. Isabel Petrescu, Preston L. Dilbeck, Beronda L. Montgomery. Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon. Frontiers in Microbiology 2021, 12 https://doi.org/10.3389/fmicb.2021.819604
    12. Michal Gwizdala, Pedro H. Lebre, Gillian Maggs‐Kölling, Eugene Marais, Don A. Cowan, Tjaart P. J. Krüger. Sub‐lithic photosynthesis in hot desert habitats. Environmental Microbiology 2021, 23 (7) , 3867-3880. https://doi.org/10.1111/1462-2920.15505
    13. Kevin Clark, Natalia B. Pigni, Kithmini Wijesiri, José A. Gascón. Spectral Features of Canthaxanthin in HCP2. A QM/MM Approach. Molecules 2021, 26 (9) , 2441. https://doi.org/10.3390/molecules26092441
    14. Tuhin Khan, Radek Litvín, Václav Šebelík, Tomáš Polívka. Excited‐State Evolution of Keto‐Carotenoids after Excess Energy Excitation in the UV Region. ChemPhysChem 2021, 22 (5) , 471-480. https://doi.org/10.1002/cphc.202000982
    15. Corie Y. Ralston, Cheryl A. Kerfeld. Integrated Structural Studies for Elucidating Carotenoid-Protein Interactions. 2021, 1-10. https://doi.org/10.1007/5584_2020_615
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    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2020, 124, 24, 4896–4905
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.0c03137
    Published May 21, 2020
    Copyright © 2020 American Chemical Society
    Request reuse permissions

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