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Title: Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs

Abstract

Contents Summary 937 I. Introduction 937 II. The structure of the OCP 938 III. OCP function 939 IV. Distribution of OCPs, FRP and domains in cyanobacteria 943 V. Carotenoid–protein interactions in the OCP and the HCPs 947 VI. Conclusions and prospects 948 Acknowledgements 948 References 949 Summary The orange carotenoid protein ( OCP ) is a water‐soluble, photoactive protein involved in thermal dissipation of excess energy absorbed by the light‐harvesting phycobilisomes ( PBS ) in cyanobacteria. The OCP is structurally and functionally modular, consisting of a sensor domain, an effector domain and a keto‐carotenoid. On photoactivation, the OCP converts from a stable orange form, OCP O , to a red form, OCP R . Activation is accompanied by a translocation of the carotenoid deeper into the effector domain. The increasing availability of cyanobacterial genomes has enabled the identification of new OCP families ( OCP 1, OCP 2, OCPX ). The fluorescence recovery protein ( FRP ) detaches OCP 1 from the PBS core, accelerating its back‐conversion to OCP O ; by contrast, other OCP families are not regulated by FRP . N‐terminal domain homologs, the helical carotenoid proteins ( HCP s), have been found among diverse cyanobacteria, occurring as multiplemore » paralogous groups, with two representatives exhibiting strong singlet oxygen ( 1 O 2 ) quenching ( HCP 2, HCP 3) and another capable of dissipating PBS excitation ( HCP 4). Crystal structures are presently available for OCP 1 and HCP 1, and models of other HCP subtypes can be readily produced as a result of strong sequence conservation, providing new insights into the determinants of carotenoid binding and 1 O 2 quenching.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3]
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  1. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing MI 48824 USA; Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley CA 94720 USA; Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing MI 48824 USA
  2. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing MI 48824 USA; Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley CA 94720 USA
  3. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing MI 48824 USA
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)
OSTI Identifier:
1596267
Alternate Identifier(s):
OSTI ID: 1401906
Grant/Contract Number:  
FG02-91ER20021; DE‐FG02‐91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 215; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kerfeld, Cheryl A., Melnicki, Matthew R., Sutter, Markus, and Dominguez-Martin, Maria Agustina. Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. United States: N. p., 2017. Web. doi:10.1111/nph.14670.
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Kerfeld, Cheryl A., Melnicki, Matthew R., Sutter, Markus, & Dominguez-Martin, Maria Agustina. Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. United States. https://doi.org/10.1111/nph.14670
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Kerfeld, Cheryl A., Melnicki, Matthew R., Sutter, Markus, and Dominguez-Martin, Maria Agustina. Tue . "Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs". United States. https://doi.org/10.1111/nph.14670. https://www.osti.gov/servlets/purl/1596267.
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@article{osti_1596267,
title = {Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs},
author = {Kerfeld, Cheryl A. and Melnicki, Matthew R. and Sutter, Markus and Dominguez-Martin, Maria Agustina},
abstractNote = {Contents Summary 937 I. Introduction 937 II. The structure of the OCP 938 III. OCP function 939 IV. Distribution of OCPs, FRP and domains in cyanobacteria 943 V. Carotenoid–protein interactions in the OCP and the HCPs 947 VI. Conclusions and prospects 948 Acknowledgements 948 References 949 Summary The orange carotenoid protein ( OCP ) is a water‐soluble, photoactive protein involved in thermal dissipation of excess energy absorbed by the light‐harvesting phycobilisomes ( PBS ) in cyanobacteria. The OCP is structurally and functionally modular, consisting of a sensor domain, an effector domain and a keto‐carotenoid. On photoactivation, the OCP converts from a stable orange form, OCP O , to a red form, OCP R . Activation is accompanied by a translocation of the carotenoid deeper into the effector domain. The increasing availability of cyanobacterial genomes has enabled the identification of new OCP families ( OCP 1, OCP 2, OCPX ). The fluorescence recovery protein ( FRP ) detaches OCP 1 from the PBS core, accelerating its back‐conversion to OCP O ; by contrast, other OCP families are not regulated by FRP . N‐terminal domain homologs, the helical carotenoid proteins ( HCP s), have been found among diverse cyanobacteria, occurring as multiple paralogous groups, with two representatives exhibiting strong singlet oxygen ( 1 O 2 ) quenching ( HCP 2, HCP 3) and another capable of dissipating PBS excitation ( HCP 4). Crystal structures are presently available for OCP 1 and HCP 1, and models of other HCP subtypes can be readily produced as a result of strong sequence conservation, providing new insights into the determinants of carotenoid binding and 1 O 2 quenching.},
doi = {10.1111/nph.14670},
journal = {New Phytologist},
number = 3,
volume = 215,
place = {United States},
year = {Tue Jul 04 00:00:00 EDT 2017},
month = {Tue Jul 04 00:00:00 EDT 2017}
}
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Figures / Tables:

Table 1 Table 1 : Summary of selected amino acids in red carotenoid protein (RCP) and HCP1, HCP2, HCP3 and HCP4 from Anabaena PCC 7120 within 4 Å distance to the carotenoid
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  • Stadnichuk, Igor N.; Yanyushin, Mikhail F.; Bernát, Gábor
  • Journal of Photochemistry and Photobiology B: Biology, Vol. 125
  • DOI: 10.1016/j.jphotobiol.2013.05.014

Light Harvesting and Blue-Green Light Induced Non-Photochemical Quenching in Two Different C-Phycocyanin Mutants of Synechocystis PCC 6803
journal, December 2012

  • Tian, Lijin; van Stokkum, Ivo H. M.; Koehorst, Rob B. M.
  • The Journal of Physical Chemistry B, Vol. 117, Issue 38
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Site of non-photochemical quenching of the phycobilisome by orange carotenoid protein in the cyanobacterium Synechocystis sp. PCC 6803
journal, August 2012

  • Stadnichuk, Igor N.; Yanyushin, Mikhail F.; Maksimov, Evgeni G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8
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Investigation of OCP-triggered dissipation of excitation energy in PSI/PSII-less Synechocystis sp. PCC 6803 mutant using non-linear laser fluorimetry
journal, July 2012

  • Kuzminov, F. I.; Karapetyan, N. V.; Rakhimberdieva, M. G.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 7
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Methionine oxidation and reduction in proteins
journal, February 2014

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  • Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1840, Issue 2
  • DOI: 10.1016/j.bbagen.2013.04.038

Study of O -Phosphorylation Sites in Proteins Involved in Photosynthesis-Related Processes in Synechocystis sp. Strain PCC 6803: Application of the SRM Approach
journal, November 2016

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
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Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically
journal, January 2013

A Soluble Carotenoid Protein Involved in Phycobilisome-Related Energy Dissipation in Cyanobacteria
journal, March 2006

  • Wilson, Adjélé; Ajlani, Ghada; Verbavatz, Jean-Marc
  • The Plant Cell, Vol. 18, Issue 4
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Methionine residues as endogenous antioxidants in proteins
journal, December 1996

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  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 26
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Structural Determinants Underlying Photoprotection in the Photoactive Orange Carotenoid Protein of Cyanobacteria
journal, April 2010

  • Wilson, Adjele; Kinney, James N.; Zwart, Petrus H.
  • Journal of Biological Chemistry, Vol. 285, Issue 24
  • DOI: 10.1074/jbc.M110.115709

The time course of non-photochemical quenching in phycobilisomes of Synechocystis sp. PCC6803 as revealed by picosecond time-resolved fluorimetry
journal, September 2014

  • Maksimov, E. G.; Schmitt, F. -J.; Shirshin, E. A.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 9
  • DOI: 10.1016/j.bbabio.2014.01.010

Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria
journal, October 2008

  • Boulay, Clémence; Abasova, Leyla; Six, Christophe
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 10
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The Late Quaternary palaeoenvironmental history of a presently deep freshwater lake in east-central Alberta, Canada and palaeoclimate implications
journal, July 1996

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Excited-state properties of the 16 kDa red carotenoid protein from Arthrospira maxima
journal, January 2011

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  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 1
  • DOI: 10.1016/j.bbabio.2010.08.013

Live Cell Chemical Profiling of Temporal Redox Dynamics in a Photoautotrophic Cyanobacterium
journal, October 2013

  • Sadler, Natalie C.; Melnicki, Matthew R.; Serres, Margrethe H.
  • ACS Chemical Biology, Vol. 9, Issue 1
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A comparative study of three signaling forms of the orange carotenoid protein
journal, May 2016

  • Maksimov, E. G.; Moldenhauer, M.; Shirshin, E. A.
  • Photosynthesis Research, Vol. 130, Issue 1-3
  • DOI: 10.1007/s11120-016-0272-8

Advancements and Application of Microsecond Synchrotron X-ray Footprinting at the Advanced Light Source
journal, January 2016

Activated OCP unlocks nonphotochemical quenching in cyanobacteria
journal, October 2015

  • Cogdell, Richard J.; Gardiner, Alastair T.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
  • DOI: 10.1073/pnas.1517477112

Singlet oxygen quenching ability of naturally occurring carotenoids
journal, February 1994

  • Hirayama, Osamu; Nakamura, Kyoko; Hamada, Syoko
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Chlorophyll Fluorescence Analysis of Cyanobacterial Photosynthesis and Acclimation
journal, September 1998

  • Campbell, Douglas; Hurry, Vaughan; Clarke, Adrian K.
  • Microbiology and Molecular Biology Reviews, Vol. 62, Issue 3
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UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune.
journal, March 1997

Carotenoid-containing outer membrane of Synechocystis sp. strain PCC6714
journal, October 1985

Assembly of photoactive orange carotenoid protein from its domains unravels a carotenoid shuttle mechanism
journal, February 2017

Isolation of the carotenoid-containing cell wall of three unicellular cyanobacteria.
journal, January 1983

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