Structural analysis of a new carotenoid-binding protein: the C-terminal domain homolog of the OCP

Dominguez-Martin, Maria Agustina; Hammel, Michal; Gupta, Sayan; Lechno-Yossef, Sigal; Sutter, Markus; Rosenberg, Daniel J.; Chen, Yan; Petzold, Christopher J.; Ralston, Corie Y.; Polívka, Tomáš; Kerfeld, Cheryl A.

doi:10.1038/s41598-020-72383-y

Title: Structural analysis of a new carotenoid-binding protein: the C-terminal domain homolog of the OCP

Journal Article · Wed Sep 23 00:00:00 EDT 2020 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-020-72383-y· OSTI ID:1664560

Dominguez-Martin, Maria Agustina; Hammel, Michal; Gupta, Sayan; Lechno-Yossef, Sigal; Sutter, Markus; Rosenberg, Daniel J.; Chen, Yan; Petzold, Christopher J.; Ralston, Corie Y.; Polívka, Tomáš; Kerfeld, Cheryl A.

The Orange Carotenoid Protein (OCP) is a water-soluble protein that governs photoprotection in many cyanobacteria. The 35 kDa OCP is structurally and functionally modular, consisting of an N-terminal effector domain (NTD) and a C-terminal regulatory domain (CTD); a carotenoid spans the two domains. The CTD is a member of the ubiquitous Nuclear Transport Factor-2 (NTF2) superfamily (pfam02136). With the increasing availability of cyanobacterial genomes, bioinformatic analysis has revealed the existence of a new family of proteins, homologs to the CTD, the C-terminal domain-like carotenoid proteins (CCPs). Here we purify holo-CCP2 directly from cyanobacteria and establish that it natively binds canthaxanthin (CAN). We use small-angle X-ray scattering (SAXS) to characterize the structure of this carotenoprotein in two distinct oligomeric states. A single carotenoid molecule spans the two CCPs in the dimer. Our analysis with X-ray footprinting-mass spectrometry (XFMS) identifies critical residues for carotenoid binding that likely contribute to the extreme red shift (ca. 80 nm) of the absorption maximum of the carotenoid bound by the CCP2 dimer and a further 10 nm shift in the tetramer form. These data provide the first structural description of carotenoid binding by a protein consisting of only an NTF2 domain.

View Journal Article

Cite

Export

Save

Research Organization:: Michigan State Univ., East Lansing, MI (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); European Union (EU); Czech Science Foundation; National Institutes of Health (NIH)

Grant/Contract Number:: SC0020606; AC02-05CH11231; FG02-91ER20021; IOS-1557324; 795070; 18-21631S; 1R01GM126218; P30-GM124169-01

OSTI ID:: 1664560

Alternate ID(s):: OSTI ID: 1711416; OSTI ID: 1713256

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Vol. 10 Journal Issue: 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (46)

Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria Bao, Han; Melnicki, Matthew R.; Pawlowski, Emily G. Nature Plants, Vol. 3, Issue 8 https://doi.org/10.1038/nplants.2017.89	journal	July 2017
Comparative Protein Modelling by Satisfaction of Spatial Restraints Šali, Andrej; Blundell, Tom L. Journal of Molecular Biology, Vol. 234, Issue 3 https://doi.org/10.1006/jmbi.1993.1626	journal	December 1993
SASBDB, a repository for biological small-angle scattering data Valentini, Erica; Kikhney, Alexey G.; Previtali, Gianpietro Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1047	journal	October 2014
Cyanobacterial carboxysomes contain an unique rubisco‐activase‐like protein Lechno‐Yossef, Sigal; Rohnke, Brandon A.; Belza, Ana C. O. New Phytologist, Vol. 225, Issue 2 https://doi.org/10.1111/nph.16195	journal	October 2019
Different Functions of the Paralogs to the N-Terminal Domain of the Orange Carotenoid Protein in the Cyanobacterium Anabaena sp. PCC 7120 López-Igual, Rocío; Wilson, Adjélé; Leverenz, Ryan L. Plant Physiology, Vol. 171, Issue 3 https://doi.org/10.1104/pp.16.00502	journal	May 2016
Light‐controlled carotenoid transfer between water‐soluble proteins related to cyanobacterial photoprotection Slonimskiy, Yury B.; Muzzopappa, Fernando; Maksimov, Eugene G. The FEBS Journal, Vol. 286, Issue 10 https://doi.org/10.1111/febs.14803	journal	March 2019
Paired cloning vectors for complementation of mutations in the cyanobacterium Anabaena sp. strain PCC 7120 Wolk, C. Peter; Fan, Qing; Zhou, Ruanbao Archives of Microbiology, Vol. 188, Issue 6 https://doi.org/10.1007/s00203-007-0276-z	journal	July 2007
The Multiple Roles of the Protein in the Photoactivation of Orange Carotenoid Protein Bondanza, Mattia; Cupellini, Lorenzo; Lipparini, Filippo Chem, Vol. 6, Issue 1 https://doi.org/10.1016/j.chempr.2019.10.014	journal	January 2020
Assembly of photoactive orange carotenoid protein from its domains unravels a carotenoid shuttle mechanism Moldenhauer, Marcus; Sluchanko, Nikolai N.; Buhrke, David Photosynthesis Research, Vol. 133, Issue 1-3 https://doi.org/10.1007/s11120-017-0353-3	journal	February 2017
Structure, Diversity, and Evolution of a New Family of Soluble Carotenoid-Binding Proteins in Cyanobacteria Melnicki, Matthew R.; Leverenz, Ryan L.; Sutter, Markus Molecular Plant, Vol. 9, Issue 10 https://doi.org/10.1016/j.molp.2016.06.009	journal	October 2016
Structure and Function of the Water-Soluble Carotenoid-Binding Proteins of Cyanobacteria Kerfeld, Cheryl A. Photosynthesis Research, Vol. 81, Issue 3 https://doi.org/10.1023/B:PRES.0000036886.60187.c8	journal	January 2004
Carotenoids in Photosynthesis Frank, Harry A.; Cogdell, Richard J. Photochemistry and Photobiology, Vol. 63, Issue 3 https://doi.org/10.1111/j.1751-1097.1996.tb03022.x	journal	March 1996
High-Throughput SAXS for the Characterization of Biomolecules in Solution: A Practical Approach Dyer, Kevin N.; Hammel, Michal; Rambo, Robert P. Structural Genomics https://doi.org/10.1007/978-1-62703-691-7_18	book	October 2013
Structural basis for AcrVA4 inhibition of specific CRISPR-Cas12a Knott, Gavin J.; Cress, Brady F.; Liu, Jun-Jie eLife, Vol. 8 https://doi.org/10.7554/eLife.49110	journal	August 2019
A 12 A carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection Leverenz, R. L.; Sutter, M.; Wilson, A. Science, Vol. 348, Issue 6242 https://doi.org/10.1126/science.aaa7234	journal	June 2015
When There Is Too Much Light: Fig. 1. Ort, Donald R. Plant Physiology, Vol. 125, Issue 1 https://doi.org/10.1104/pp.125.1.29	journal	January 2001
Structure and functions of Orange Carotenoid Protein homologs in cyanobacteria Bao, Han; Melnicki, Matthew R.; Kerfeld, Cheryl A. Current Opinion in Plant Biology, Vol. 37 https://doi.org/10.1016/j.pbi.2017.03.010	journal	June 2017
Hydroxyl radical probe of protein surfaces using synchrotron X-ray radiolysis and mass spectrometry Kiselar, J. G.; Maleknia, S. D.; Sullivan, M. International Journal of Radiation Biology, Vol. 78, Issue 2 https://doi.org/10.1080/09553000110094805	journal	January 2002
FoXS: a web server for rapid computation and fitting of SAXS profiles Schneidman-Duhovny, D.; Hammel, M.; Sali, A. Nucleic Acids Research, Vol. 38, Issue Web Server https://doi.org/10.1093/nar/gkq461	journal	May 2010
Carotenoids of blue-green algae—11. carotenoids of chromatically-adapted cyanobacteria Fiksdahl, Anne; Foss, Per; Liaaen-Jensen, Synnøve Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 76, Issue 3 https://doi.org/10.1016/0305-0491(83)90300-0	journal	January 1983
Versatility of carotenoids: An integrated view on diversity, evolution, functional roles and environmental interactions Esteban, Raquel; Moran, Jose Fernando; Becerril, José María Environmental and Experimental Botany, Vol. 119 https://doi.org/10.1016/j.envexpbot.2015.04.009	journal	November 2015
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon Cobley, John G.; Zerweck, Edward; Reyes, Richard Plasmid, Vol. 30, Issue 2 https://doi.org/10.1006/plas.1993.1037	journal	September 1993
Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs Kerfeld, Cheryl A.; Melnicki, Matthew R.; Sutter, Markus New Phytologist, Vol. 215, Issue 3 https://doi.org/10.1111/nph.14670	journal	July 2017
Structural peculiarities of keto-carotenoids in water-soluble proteins revealed by simulation of linear absorption Pishchalnikov, Roman Y.; Yaroshevich, Igor A.; Slastnikova, Tatiana A. Physical Chemistry Chemical Physics, Vol. 21, Issue 46 https://doi.org/10.1039/c9cp04508b	journal	January 2019
Water-soluble carotenoid proteins of cyanobacteria Kerfeld, Cheryl A. Archives of Biochemistry and Biophysics, Vol. 430, Issue 1 https://doi.org/10.1016/j.abb.2004.03.018	journal	October 2004
Structural and spectroscopic characterization of HCP2 Dominguez-Martin, Maria Agustina; Polívka, Tomáš; Sutter, Markus Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1860, Issue 5 https://doi.org/10.1016/j.bbabio.2019.03.004	journal	May 2019
Structural dynamics in the C terminal domain homolog of orange carotenoid Protein reveals residues critical for carotenoid uptake Harris, Dvir; Muzzopappa, Fernando; Glaser, Fabian Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 8 https://doi.org/10.1016/j.bbabio.2020.148214	journal	August 2020
Filling out the structural map of the NTF2-like superfamily Eberhardt, Ruth Y.; Chang, Yuanyuan; Bateman, Alex BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-327	journal	November 2013
Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon Singh, Shailendra P.; Montgomery, Beronda L. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01215	journal	November 2015
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
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Comparative ultrafast spectroscopy and structural analysis of OCP1 and OCP2 from Tolypothrix Kuznetsova, Valentyna; Dominguez-Martin, Maria Agustina; Bao, Han Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 2 https://doi.org/10.1016/j.bbabio.2019.148120	journal	February 2020
Ring-to-chain conformation may be a determining factor in the ability of xanthophylls to bind to the bulk light-harvesting complex of plants Young, Andrew J.; Phillip, Denise M.; Hashimoto, Hideki Journal of Molecular Structure, Vol. 642, Issue 1-3 https://doi.org/10.1016/S0022-2860(02)00444-1	journal	December 2002
Structure and flexibility within proteins as identified through small angle X-ray scattering Pelikan, M.; Hura, G.; Hammel, M. General Physiology and Biophysics, Vol. 28, Issue 2 https://doi.org/10.4149/gpb_2009_02_174	journal	January 2009
The molecular basis of the coloration mechanism in lobster shell: -Crustacyanin at 3.2-A resolution Cianci, M.; Rizkallah, P. J.; Olczak, A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 15 https://doi.org/10.1073/pnas.152088999	journal	July 2002
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
Spectroscopic Properties of the Carotenoid 3‘-Hydroxyechinenone in the Orange Carotenoid Protein from the Cyanobacterium Arthrospira maxima ^† Polívka, Tomáš; Kerfeld, Cheryl A.; Pascher, Torbjörn Biochemistry, Vol. 44, Issue 10 https://doi.org/10.1021/bi047473t	journal	March 2005
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Synthetic OCP heterodimers are photoactive and recapitulate the fusion of two primitive carotenoproteins in the evolution of cyanobacterial photoprotection Lechno-Yossef, Sigal; Melnicki, Matthew R.; Bao, Han The Plant Journal, Vol. 91, Issue 4 https://doi.org/10.1111/tpj.13593	journal	June 2017
Accurate assessment of mass, models and resolution by small-angle scattering Rambo, Robert P.; Tainer, John A. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12070	journal	April 2013
Structural rearrangements in the C-terminal domain homolog of Orange Carotenoid Protein are crucial for carotenoid transfer Harris, Dvir; Wilson, Adjele; Muzzopappa, Fernando Communications Biology, Vol. 1, Issue 1 https://doi.org/10.1038/s42003-018-0132-5	journal	August 2018
Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS) Hura, Greg L.; Menon, Angeli L.; Hammel, Michal Nature Methods, Vol. 6, Issue 8 https://doi.org/10.1038/nmeth.1353	journal	July 2009
Characterization of Canthaxanthin Isomers Isolated from a New Soil Dietzia sp. and Their Antioxidant Activities Venugopalan, Vijayalatha Journal of Microbiology and Biotechnology, Vol. 23, Issue 2 https://doi.org/10.4014/jmb.1203.03032	journal	February 2013
A comparative study of three signaling forms of the orange carotenoid protein Maksimov, E. G.; Moldenhauer, M.; Shirshin, E. A. Photosynthesis Research, Vol. 130, Issue 1-3 https://doi.org/10.1007/s11120-016-0272-8	journal	May 2016
Effect of carotenoid structure on excited-state dynamics of carbonyl carotenoids Chábera, Pavel; Fuciman, Marcel; Hříbek, Petr Physical Chemistry Chemical Physics, Vol. 11, Issue 39 https://doi.org/10.1039/b909924g	journal	January 2009
Orange and red carotenoid proteins are involved in the adaptation of the terrestrial cyanobacterium Nostoc flagelliforme to desiccation Yang, Yi-Wen; Yin, Yan-Chao; Li, Zheng-Ke Photosynthesis Research, Vol. 140, Issue 1 https://doi.org/10.1007/s11120-019-00629-6	journal	March 2019

Similar Records

Synthetic OCP heterodimers are photoactive and recapitulate the fusion of two primitive carotenoproteins in the evolution of cyanobacterial photoprotection

Journal Article · Mon May 15 00:00:00 EDT 2017 · The Plant Journal · OSTI ID:1664560

Lechno‐Yossef, Sigal; Melnicki, Matthew R.; Bao, Han; +2 more

Binding of red form of Orange Carotenoid Protein (OCP) to phycobilisome is not sufficient for quenching

Journal Article · Sun Mar 01 00:00:00 EST 2020 · Biochimica et Biophysica Acta - Bioenergetics · OSTI ID:1664560

Lou, Wenjing; Niedzwiedzki, Dariusz M.; Jiang, Ruidong J.; +2 more

Environmental Tuning of Homologs of the Orange Carotenoid Protein-Encoding Gene in the Cyanobacterium Fremyella diplosiphon

Journal Article · Fri Dec 24 00:00:00 EST 2021 · Frontiers in Microbiology · OSTI ID:1664560

Petrescu, D. Isabel; Dilbeck, Preston L.; Montgomery, Beronda L.

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
biochemistry
biophysical chemistry
proteins
structural biology

Title: Structural analysis of a new carotenoid-binding protein: the C-terminal domain homolog of the OCP

Citation Formats

References (46)

Similar Records

Related Subjects