Structural and spectroscopic characterization of HCP2
Abstract
The Helical Carotenoid Proteins (HCPs) are a large group of newly identified carotenoid-binding proteins found in ecophysiologically diverse cyanobacteria. They likely evolved before becoming the effector (quenching) domain of the modular Orange Carotenoid Protein (OCP). The number of discrete HCP families—at least nine—suggests they are involved in multiple distinct functions. Here we report the 1.7 Å crystal structure of HCP2, one of the most widespread HCPs found in nature, from the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601. By purifying HCP2 from the native source we are able to identify its natively-bound carotenoid, which is exclusively canthaxanthin. In solution, HCP2 is a monomer with an absorbance maximum of 530 nm. However, the HCP2 crystals have a maximum absorbance at 548 nm, which is accounted by the stacking of the β1 rings of the carotenoid in the two molecules in the asymmetric unit. Our results demonstrate how HCPs provide a valuable system to study carotenoid-protein interactions and their spectroscopic implications, and contribute to efforts to understand the functional roles of this large, newly discovered family of pigment proteins, which to-date remain enigmatic.
- Authors:
- Publication Date:
- Research Org.:
- Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); Czech Science Foundation; Marie Curie Fellowship
- OSTI Identifier:
- 1547628
- Alternate Identifier(s):
- OSTI ID: 1607873
- Grant/Contract Number:
- FG02-91ER20021; AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Biochimica et Biophysica Acta - Bioenergetics
- Additional Journal Information:
- Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1860 Journal Issue: 5; Journal ID: ISSN 0005-2728
- Publisher:
- Elsevier
- Country of Publication:
- Netherlands
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; helical carotenoid protein; photoprotection; cyanobacteria; spectroscopic; crystal structure; carotenoid aggregates
Citation Formats
Dominguez-Martin, Maria Agustina, Polívka, Tomáš, Sutter, Markus, Ferlez, Bryan, Lechno-Yossef, Sigal, Montgomery, Beronda L., and Kerfeld, Cheryl A. Structural and spectroscopic characterization of HCP2. Netherlands: N. p., 2019.
Web. doi:10.1016/j.bbabio.2019.03.004.
Dominguez-Martin, Maria Agustina, Polívka, Tomáš, Sutter, Markus, Ferlez, Bryan, Lechno-Yossef, Sigal, Montgomery, Beronda L., & Kerfeld, Cheryl A. Structural and spectroscopic characterization of HCP2. Netherlands. https://doi.org/10.1016/j.bbabio.2019.03.004
Dominguez-Martin, Maria Agustina, Polívka, Tomáš, Sutter, Markus, Ferlez, Bryan, Lechno-Yossef, Sigal, Montgomery, Beronda L., and Kerfeld, Cheryl A. Wed .
"Structural and spectroscopic characterization of HCP2". Netherlands. https://doi.org/10.1016/j.bbabio.2019.03.004.
@article{osti_1547628,
title = {Structural and spectroscopic characterization of HCP2},
author = {Dominguez-Martin, Maria Agustina and Polívka, Tomáš and Sutter, Markus and Ferlez, Bryan and Lechno-Yossef, Sigal and Montgomery, Beronda L. and Kerfeld, Cheryl A.},
abstractNote = {The Helical Carotenoid Proteins (HCPs) are a large group of newly identified carotenoid-binding proteins found in ecophysiologically diverse cyanobacteria. They likely evolved before becoming the effector (quenching) domain of the modular Orange Carotenoid Protein (OCP). The number of discrete HCP families—at least nine—suggests they are involved in multiple distinct functions. Here we report the 1.7 Å crystal structure of HCP2, one of the most widespread HCPs found in nature, from the chromatically acclimating cyanobacterium Tolypothrix sp. PCC 7601. By purifying HCP2 from the native source we are able to identify its natively-bound carotenoid, which is exclusively canthaxanthin. In solution, HCP2 is a monomer with an absorbance maximum of 530 nm. However, the HCP2 crystals have a maximum absorbance at 548 nm, which is accounted by the stacking of the β1 rings of the carotenoid in the two molecules in the asymmetric unit. Our results demonstrate how HCPs provide a valuable system to study carotenoid-protein interactions and their spectroscopic implications, and contribute to efforts to understand the functional roles of this large, newly discovered family of pigment proteins, which to-date remain enigmatic.},
doi = {10.1016/j.bbabio.2019.03.004},
journal = {Biochimica et Biophysica Acta - Bioenergetics},
number = 5,
volume = 1860,
place = {Netherlands},
year = {Wed May 01 00:00:00 EDT 2019},
month = {Wed May 01 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1016/j.bbabio.2019.03.004
https://doi.org/10.1016/j.bbabio.2019.03.004
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 15 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Additional families of orange carotenoid proteins in the photoprotective system of cyanobacteria
journal, July 2017
- Bao, Han; Melnicki, Matthew R.; Pawlowski, Emily G.
- Nature Plants, Vol. 3, Issue 8
Protection of Photosynthesis against Ultraviolet-B Radiation by Carotenoids in Transformants of the Cyanobacterium Synechococcus PCC7942
journal, June 1999
- Götz, Thomas; Windhövel, Ute; Böger, Peter
- Plant Physiology, Vol. 120, Issue 2
High-light-dependent upregulation of carotenoids and their antioxidative properties in the cyanobacterium Synechocystis PCC 6803
journal, October 1999
- Steiger, Sabine; Schäfer, Lutz; Sandmann, Gerhard
- Journal of Photochemistry and Photobiology B: Biology, Vol. 52, Issue 1-3
Carotenoid–protein interaction alters the S1 energy of hydroxyechinenone in the Orange Carotenoid Protein
journal, March 2013
- Polívka, Tomáš; Chábera, Pavel; Kerfeld, Cheryl A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 3
Different Functions of the Paralogs to the N-Terminal Domain of the Orange Carotenoid Protein in the Cyanobacterium Anabaena sp. PCC 7120
journal, May 2016
- López-Igual, Rocío; Wilson, Adjélé; Leverenz, Ryan L.
- Plant Physiology, Vol. 171, Issue 3
Overview of the CCP 4 suite and current developments
journal, March 2011
- Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Expression of a Ketolase Gene Mediates the Synthesis of Canthaxanthin in Synechococcus Leading to Tolerance Against Photoinhibition, Pigment Degradation and UV-B Sensitivity of Photosynthesis¶
journal, January 2001
- Albrecht, Manuela; Steiger, Sabine; Sandmann, Gerhard
- Photochemistry and Photobiology, Vol. 73, Issue 5
phenix.mr_rosetta: molecular replacement and model rebuilding with Phenix and Rosetta
journal, March 2012
- Terwilliger, Thomas C.; DiMaio, Frank; Read, Randy J.
- Journal of Structural and Functional Genomics, Vol. 13, Issue 2
The 2Ag− energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy
journal, May 1998
- Fujii, Ritsuko; Onaka, Kengo; Kuki, Michitaka
- Chemical Physics Letters, Vol. 288, Issue 5-6
Structure, Diversity, and Evolution of a New Family of Soluble Carotenoid-Binding Proteins in Cyanobacteria
journal, October 2016
- Melnicki, Matthew R.; Leverenz, Ryan L.; Sutter, Markus
- Molecular Plant, Vol. 9, Issue 10
Structure and Function of the Water-Soluble Carotenoid-Binding Proteins of Cyanobacteria
journal, January 2004
- Kerfeld, Cheryl A.
- Photosynthesis Research, Vol. 81, Issue 3
Direct observation of the (forbidden) S1 state in carotenoids
journal, April 1999
- Polivka, T.; Herek, J. L.; Zigmantas, D.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 9
Carotenoids of blue-green algae—11. carotenoids of chromatically-adapted cyanobacteria
journal, January 1983
- Fiksdahl, Anne; Foss, Per; Liaaen-Jensen, Synnøve
- Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, Vol. 76, Issue 3
The Cyanobacterial Photoactive Orange Carotenoid Protein Is an Excellent Singlet Oxygen Quencher
journal, April 2014
- Sedoud, Arezki; López-Igual, Rocío; ur Rehman, Ateeq
- The Plant Cell, Vol. 26, Issue 4
Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012
- Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
- Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
Water-soluble carotenoid proteins of cyanobacteria
journal, October 2004
- Kerfeld, Cheryl A.
- Archives of Biochemistry and Biophysics, Vol. 430, Issue 1
A fast and portable microspectrophotometer for protein crystallography
journal, December 1993
- Hadfield, A.; Hajdu, J.
- Journal of Applied Crystallography, Vol. 26, Issue 6
Lycopene as the most efficient biological carotenoid singlet oxygen quencher
journal, November 1989
- Di Mascio, Paolo; Kaiser, Stephan; Sies, Helmut
- Archives of Biochemistry and Biophysics, Vol. 274, Issue 2
The Phyre2 web portal for protein modeling, prediction and analysis
journal, May 2015
- Kelley, Lawrence A.; Mezulis, Stefans; Yates, Christopher M.
- Nature Protocols, Vol. 10, Issue 6
Ultraviolet radiation induces both degradation and synthesis of phycobilisomes in Nostoc sp.: a spectroscopic and biochemical approach
journal, August 1997
- Aráoz, R.
- FEMS Microbiology Ecology, Vol. 23, Issue 4
Regulation of BolA abundance mediates morphogenesis in Fremyella diplosiphon
journal, November 2015
- Singh, Shailendra P.; Montgomery, Beronda L.
- Frontiers in Microbiology, Vol. 6
Local and global structural drivers for the photoactivation of the orange carotenoid protein
journal, September 2015
- Gupta, Sayan; Guttman, Miklos; Leverenz, Ryan L.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
Lutein, Zeaxanthin, and the Macular Pigment
journal, January 2001
- Landrum, John T.; Bone, Richard A.
- Archives of Biochemistry and Biophysics, Vol. 385, Issue 1
The Nature of Singlet Exciton Fission in Carotenoid Aggregates
journal, April 2015
- Musser, Andrew J.; Maiuri, Margherita; Brida, Daniele
- Journal of the American Chemical Society, Vol. 137, Issue 15
The Dynamic Origin of Color Tuning in Proteins Revealed by a Carotenoid Pigment
journal, April 2018
- Loco, Daniele; Buda, Francesco; Lugtenburg, Johan
- The Journal of Physical Chemistry Letters, Vol. 9, Issue 9
Structural and Functional Modularity of the Orange Carotenoid Protein: Distinct Roles for the N- and C-Terminal Domains in Cyanobacterial Photoprotection
journal, January 2014
- Leverenz, Ryan L.; Jallet, Denis; Li, Ming-De
- The Plant Cell, Vol. 26, Issue 1
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems
journal, April 2004
- Polívka, Tomáš; Sundström, Villy
- Chemical Reviews, Vol. 104, Issue 4
Integration, scaling, space-group assignment and post-refinement
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144
The Crystal Structure of a Cyanobacterial Water-Soluble Carotenoid Binding Protein
journal, January 2003
- Kerfeld, Cheryl A.; Sawaya, Michael R.; Brahmandam, Vishnu
- Structure, Vol. 11, Issue 1
Oscillaxanthin and myxoxanthophyll in two cores from Lake Wabamun, Alberta, Canada
journal, January 1991
- Hickman, Michael; Schweger, CharlesE.
- Journal of Paleolimnology, Vol. 5, Issue 2
Carotenoid radical chemistry and antioxidant/pro-oxidant properties
journal, October 2004
- El-Agamey, Ali; Lowe, Gordon M.; McGarvey, David J.
- Archives of Biochemistry and Biophysics, Vol. 430, Issue 1
Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation
journal, February 2016
- Liu, Haijun; Zhang, Hao; Orf, Gregory S.
- Biochemistry, Vol. 55, Issue 7
Roles of xanthophyll carotenoids in protection against photoinhibition and oxidative stress in the cyanobacterium Synechococcus sp. strain PCC 7002
journal, December 2010
- Zhu, Yuehui; Graham, Joel E.; Ludwig, Marcus
- Archives of Biochemistry and Biophysics, Vol. 504, Issue 1
Oxidation of carotenoids by free radicals: relationship between structure and reactivity
journal, July 1997
- Woodall, Alan A.; Lee, Simon Wai-Ming; Weesie, Roland J.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1336, Issue 1
Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon
journal, May 2014
- Pattanaik, Bagmi; Busch, Andrea W. U.; Hu, Pingsha
- Microbiology, Vol. 160, Issue 5
Paired cloning vectors for complementation of mutations in the cyanobacterium Anabaena sp. strain PCC 7120
journal, July 2007
- Wolk, C. Peter; Fan, Qing; Zhou, Ruanbao
- Archives of Microbiology, Vol. 188, Issue 6
Spectroscopic Investigation of the Carotenoid Deoxyperidinin: Direct Observation of the Forbidden S 0 → S 1 Transition
journal, March 2016
- Greco, Jordan A.; LaFountain, Amy M.; Kinashi, Naoto
- The Journal of Physical Chemistry B, Vol. 120, Issue 10
Structure investigations on assembled astaxanthin molecules
journal, August 2005
- Köpsel, Christian; Möltgen, Holger; Schuch, Horst
- Journal of Molecular Structure, Vol. 750, Issue 1-3
Carotenoids in Photosynthesis
journal, March 1996
- Frank, Harry A.; Cogdell, Richard J.
- Photochemistry and Photobiology, Vol. 63, Issue 3
A 12 A carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection
journal, June 2015
- Leverenz, R. L.; Sutter, M.; Wilson, A.
- Science, Vol. 348, Issue 6242
Structure and functions of Orange Carotenoid Protein homologs in cyanobacteria
journal, June 2017
- Bao, Han; Melnicki, Matthew R.; Kerfeld, Cheryl A.
- Current Opinion in Plant Biology, Vol. 37
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
Phycobilisomes from Blue-Green and Red Algae: Isolation Criteria and Dissociation Characteristics
journal, April 1979
- Gantt, Elisabeth; Lipschultz, Claudia A.; Grabowski, Joseph
- Plant Physiology, Vol. 63, Issue 4
Influence of zeaxanthin and echinenone binding on the activity of the Orange Carotenoid Protein
journal, April 2009
- Punginelli, Claire; Wilson, Adjélé; Routaboul, Jean-Marc
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 4
Construction of Shuttle Plasmids Which Can Be Efficiently Mobilized from Escherichia coli into the Chromatically Adapting Cyanobacterium, Fremyella diplosiphon
journal, September 1993
- Cobley, John G.; Zerweck, Edward; Reyes, Richard
- Plasmid, Vol. 30, Issue 2
Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs
journal, July 2017
- Kerfeld, Cheryl A.; Melnicki, Matthew R.; Sutter, Markus
- New Phytologist, Vol. 215, Issue 3
A photoactive carotenoid protein acting as light intensity sensor
journal, August 2008
- Wilson, A.; Punginelli, C.; Gall, A.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
Photoactivation mechanism of a carotenoid-based photoreceptor
journal, May 2017
- Bandara, Sepalika; Ren, Zhong; Lu, Lu
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
Crystals of the Carotenoid Protein from Arthrospira maxima Containing Uniformly Oriented Pigment Molecules
journal, November 1997
- Kerfeld, C. A.; Wu, Y. P.; Chan, C.
- Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 6
Role of carotenoids in lake sediments for reconstructing trophic history during the late Quaternary
journal, January 1989
- Z�llig, Hans
- Journal of Paleolimnology, Vol. 2, Issue 1
Ring-to-chain conformation may be a determining factor in the ability of xanthophylls to bind to the bulk light-harvesting complex of plants
journal, December 2002
- Young, Andrew J.; Phillip, Denise M.; Hashimoto, Hideki
- Journal of Molecular Structure, Vol. 642, Issue 1-3
The molecular basis of the coloration mechanism in lobster shell: -Crustacyanin at 3.2-A resolution
journal, July 2002
- Cianci, M.; Rizkallah, P. J.; Olczak, A.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 15
The Late Quaternary palaeoenvironmental history of a presently deep freshwater lake in east-central Alberta, Canada and palaeoclimate implications
journal, July 1996
- Hickman, Michael; Schweger, Charles E.
- Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 123, Issue 1-4
Supramolecular exciton chirality of carotenoid aggregates: Supramolecular Excition Chirality
journal, January 2003
- Simonyi, Miklós; Bikádi, Zsolt; Zsila, Ferenc
- Chirality, Vol. 15, Issue 8
Carotenoid composition of terrestrial cyanobacteria: response to natural light conditions in open rock habitats in Venezuela
journal, November 2001
- Lakatos, Michael; Bilger, Wolfgang; Büdel, Burkhard
- European Journal of Phycology, Vol. 36, Issue 4