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Title: A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria

Abstract

The cyanobacterial orange carotenoid protein (OCP) protects photosynthetic cyanobacteria from photodamage by dissipating excess excitation energy collected by phycobilisomes (PBS) as heat. Dissociation of the PBS–OCP complex in vivo is facilitated by another protein known as the fluorescence recovery protein (FRP), which primarily exists as a dimeric complex. In this work, we used various mass spectrometry (MS)-based techniques to investigate the molecular mechanism of this FRP-mediated process. FRP in the dimeric state (dFRP) retains its high affinity for the C-terminal domain (CTD) of OCP in the red state (OCPr). Site-directed mutagenesis and native MS suggest the head region on FRP is a candidate to bind OCP. After attachment to the CTD, the conformational changes of dFRP allow it to bridge the two domains, facilitating the reversion of OCPr into the orange state (OCPo) accompanied by a structural rearrangement of dFRP. Interestingly, we found a mutual response between FRP and OCP; that is, FRP and OCPr destabilize each other, whereas FRP and OCPo stabilize each other. A detailed mechanism of FRP function is proposed on the basis of the experimental results.

Authors:
ORCiD logo [1];  [2];  [2];  [1];  [1];  [3];  [2]; ORCiD logo [1];  [1]
+ Show Author Affiliations
  1. Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
  2. Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC); Washington Univ., St. Louis, MO (United States)
  3. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH)
OSTI Identifier:
1534421
Grant/Contract Number:  
FG02-07ER15902; SC0001035; 2P41GM103422
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 56; Journal Issue: 22; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Biochemistry & molecular biology; Interfaces; Peptides and proteins; Monomers; Solvents; Nucleic acid structure

Citation Formats

Lu, Yue, Liu, Haijun, Saer, Rafael, Li, Veronica L., Zhang, Hao, Shi, Liuqing, Goodson, Carrie, Gross, Michael L., and Blankenship, Robert E. A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria. United States: N. p., 2017. Web. doi:10.1021/acs.biochem.7b00202.
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Lu, Yue, Liu, Haijun, Saer, Rafael, Li, Veronica L., Zhang, Hao, Shi, Liuqing, Goodson, Carrie, Gross, Michael L., & Blankenship, Robert E. A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria. United States. https://doi.org/10.1021/acs.biochem.7b00202
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Lu, Yue, Liu, Haijun, Saer, Rafael, Li, Veronica L., Zhang, Hao, Shi, Liuqing, Goodson, Carrie, Gross, Michael L., and Blankenship, Robert E. Wed . "A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria". United States. https://doi.org/10.1021/acs.biochem.7b00202. https://www.osti.gov/servlets/purl/1534421.
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@article{osti_1534421,
title = {A Molecular Mechanism for Nonphotochemical Quenching in Cyanobacteria},
author = {Lu, Yue and Liu, Haijun and Saer, Rafael and Li, Veronica L. and Zhang, Hao and Shi, Liuqing and Goodson, Carrie and Gross, Michael L. and Blankenship, Robert E.},
abstractNote = {The cyanobacterial orange carotenoid protein (OCP) protects photosynthetic cyanobacteria from photodamage by dissipating excess excitation energy collected by phycobilisomes (PBS) as heat. Dissociation of the PBS–OCP complex in vivo is facilitated by another protein known as the fluorescence recovery protein (FRP), which primarily exists as a dimeric complex. In this work, we used various mass spectrometry (MS)-based techniques to investigate the molecular mechanism of this FRP-mediated process. FRP in the dimeric state (dFRP) retains its high affinity for the C-terminal domain (CTD) of OCP in the red state (OCPr). Site-directed mutagenesis and native MS suggest the head region on FRP is a candidate to bind OCP. After attachment to the CTD, the conformational changes of dFRP allow it to bridge the two domains, facilitating the reversion of OCPr into the orange state (OCPo) accompanied by a structural rearrangement of dFRP. Interestingly, we found a mutual response between FRP and OCP; that is, FRP and OCPr destabilize each other, whereas FRP and OCPo stabilize each other. A detailed mechanism of FRP function is proposed on the basis of the experimental results.},
doi = {10.1021/acs.biochem.7b00202},
journal = {Biochemistry},
number = 22,
volume = 56,
place = {United States},
year = {Wed May 17 00:00:00 EDT 2017},
month = {Wed May 17 00:00:00 EDT 2017}
}
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Journal Article:
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Publisher's Version of Record
https://doi.org/10.1021/acs.biochem.7b00202
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Cited by: 17 works
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Figures / Tables:

Figure 1 Figure 1: Native mass spectra of FRP and the NTD/CTD mixture in a (A) 4:1 or (B) 1:4 ratio. Complexes include the dCTD-dFRP-NTD, CTD-dFRP-NTD, dCTD-dFRP and CTD-dFRP. The inset in A shows the binding of the NTD fragments to the dFRP-CTD.
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    Works referencing / citing this record:

    OCP–FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria
    journal, September 2018

    • Sluchanko, Nikolai N.; Slonimskiy, Yury B.; Shirshin, Evgeny A.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-06195-0

    Photoprotective, excited-state quenching mechanisms in diverse photosynthetic organisms
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    • Magdaong, Nikki Cecil M.; Blankenship, Robert E.
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    • DOI: 10.1074/jbc.tm117.000233

    OCP–FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria
    text, January 2018

    • Sluchanko, Nikolai N.; Slonimskiy, Yury B.; Shirshin, Evgeny A.
    • Deutsches Elektronen-Synchrotron, DESY, Hamburg
    • DOI: 10.3204/pubdb-2018-05704

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    • Slonimskiy, Yury B.; Maksimov, Eugene G.; Lukashev, Evgeny P.
    • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 5
    • DOI: 10.1016/j.bbabio.2018.03.001
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