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Title: Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation

Abstract

Photosynthetic cyanobacteria are an important contributor to global carbon and nitrogen budgets. A protein, known as the Orange Carotenoid Protein (OCP) protects the photosynthetic apparatus from damage by dissipating excess energy absorbed by the phycobilisome, the major lightharvesting complex in many cyanobacteria. OCP binds one carotenoid pigment, but the color of this pigment depends on conditions. It is orange in the dark and red when exposed to light. We modified the orange and red forms of OCP by using isotopically coded cross-linking agents and then analyzed the structural features by using LC-MS/MS. Unequivocal cross-linking pairs uniquely detected in red OCP indicate that, upon photoactivation, the OCP N-terminal domain (NTD) and C-terminal domain (CTD) reorient relative to each other. Our data also indicate that the intrinsically unstructured loop connecting NTD and CTD is not only involved in the interaction between the two domains in orange OCP but also, together with the N-terminal extension, provides a structural buffer system facilitating an intramolecular breathing motion of the OCP, thus helping conversion back and forth from orange to red form during the OCP photocycle. These results have important implications for understanding the molecular mechanism of action of cyanobacterial photoprotection.

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1387527
Alternate Identifier(s):
OSTI ID: 1371153
Grant/Contract Number:  
SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 55; Journal Issue: 7; Related Information: PARC partners with Washington University in St. Louis (lead); University of California, Riverside; University of Glasgow, UK; Los Alamos National Laboratory; University of New Mexico; New Mexico Corsortium; North Carolina State University; Northwestern University; Oak Ridge National Laboratory; University of Pennsylvania; Sandia National Laboratories; University of Sheffield, UK; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Photosynthesis; solar (fuels), photosynthesis (natural and artificial), biofuels (including algae and biomass), bio-inspired, charge transport, membrane, synthesis (novel materials), synthesis (self-assembly)

Citation Formats

Liu, Haijun, Zhang, Hao, Orf, Gregory S., Lu, Yue, Jiang, Jing, King, Jeremy D., Wolf, Nathan R., Gross, Michael L., and Blankenship, Robert E. Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation. United States: N. p., 2016. Web. doi:10.1021/acs.biochem.6b00013.
Liu, Haijun, Zhang, Hao, Orf, Gregory S., Lu, Yue, Jiang, Jing, King, Jeremy D., Wolf, Nathan R., Gross, Michael L., & Blankenship, Robert E. Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation. United States. doi:10.1021/acs.biochem.6b00013.
Liu, Haijun, Zhang, Hao, Orf, Gregory S., Lu, Yue, Jiang, Jing, King, Jeremy D., Wolf, Nathan R., Gross, Michael L., and Blankenship, Robert E. Tue . "Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation". United States. doi:10.1021/acs.biochem.6b00013. https://www.osti.gov/servlets/purl/1387527.
@article{osti_1387527,
title = {Dramatic Domain Rearrangements of the Cyanobacterial Orange Carotenoid Protein upon Photoactivation},
author = {Liu, Haijun and Zhang, Hao and Orf, Gregory S. and Lu, Yue and Jiang, Jing and King, Jeremy D. and Wolf, Nathan R. and Gross, Michael L. and Blankenship, Robert E.},
abstractNote = {Photosynthetic cyanobacteria are an important contributor to global carbon and nitrogen budgets. A protein, known as the Orange Carotenoid Protein (OCP) protects the photosynthetic apparatus from damage by dissipating excess energy absorbed by the phycobilisome, the major lightharvesting complex in many cyanobacteria. OCP binds one carotenoid pigment, but the color of this pigment depends on conditions. It is orange in the dark and red when exposed to light. We modified the orange and red forms of OCP by using isotopically coded cross-linking agents and then analyzed the structural features by using LC-MS/MS. Unequivocal cross-linking pairs uniquely detected in red OCP indicate that, upon photoactivation, the OCP N-terminal domain (NTD) and C-terminal domain (CTD) reorient relative to each other. Our data also indicate that the intrinsically unstructured loop connecting NTD and CTD is not only involved in the interaction between the two domains in orange OCP but also, together with the N-terminal extension, provides a structural buffer system facilitating an intramolecular breathing motion of the OCP, thus helping conversion back and forth from orange to red form during the OCP photocycle. These results have important implications for understanding the molecular mechanism of action of cyanobacterial photoprotection.},
doi = {10.1021/acs.biochem.6b00013},
journal = {Biochemistry},
number = 7,
volume = 55,
place = {United States},
year = {2016},
month = {2}
}

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Works referencing / citing this record:

Cyanobacterial photoprotection by the orange carotenoid protein
journal, December 2016


Single-molecule trapping and spectroscopy reveals photophysical heterogeneity of phycobilisomes quenched by Orange Carotenoid Protein
journal, March 2019


Interdomain interactions reveal the molecular evolution of the orange carotenoid protein
journal, September 2019


Photoprotective, excited-state quenching mechanisms in diverse photosynthetic organisms
journal, January 2018

  • Magdaong, Nikki Cecil M.; Blankenship, Robert E.
  • Journal of Biological Chemistry, Vol. 293, Issue 14
  • DOI: 10.1074/jbc.tm117.000233

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
  • DOI: 10.1111/nph.14670

Phycobilisomes Harbor FNR L in Cyanobacteria
journal, April 2019