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Title: Local and global structural drivers for the photoactivation of the orange carotenoid protein

Abstract

Here, photoprotective mechanisms are of fundamental importance for the survival of photosynthetic organisms. In cyanobacteria, the orange carotenoid protein (OCP), when activated by intense blue light, binds to the light-harvesting antenna and triggers the dissipation of excess captured light energy. Using a combination of small angle X-ray scattering (SAXS), X-ray hydroxyl radical footprinting, circular dichroism, and H/D exchange mass spectrometry, we identified both the local and global structural changes in the OCP upon photoactivation. SAXS and H/D exchange data showed that global tertiary structural changes, including complete domain dissociation, occur upon photoactivation, but with alteration of secondary structure confined to only the N terminus of the OCP. Microsecond radiolytic labeling identified rearrangement of the H-bonding network associated with conserved residues and structural water molecules. Collectively, these data provide experimental evidence for an ensemble of local and global structural changes, upon activation of the OCP, that are essential for photoprotection.

Authors:
 [1];  [2];  [3];  [4];  [3];  [1];  [2];  [1];  [5]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of Washington, Seattle, WA (United States)
  3. Michigan State Univ., East Lansing, MI (United States)
  4. Nazarbayev Univ., Astana (Kazakhstan)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Michigan State Univ., East Lansing, MI (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE
OSTI Identifier:
1378589
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 41; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; orange carotenoid protein; photoprotection; X-ray footprinting; hydrogen deuterium exchange; SAXS

Citation Formats

Gupta, Sayan, Guttman, Miklos, Leverenz, Ryan L., Zhumadilova, Kulyash, Pawlowski, Emily G., Petzold, Christopher J., Lee, Kelly K., Ralston, Corie Y., and Kerfeld, Cheryl A. Local and global structural drivers for the photoactivation of the orange carotenoid protein. United States: N. p., 2015. Web. doi:10.1073/pnas.1512240112.
Gupta, Sayan, Guttman, Miklos, Leverenz, Ryan L., Zhumadilova, Kulyash, Pawlowski, Emily G., Petzold, Christopher J., Lee, Kelly K., Ralston, Corie Y., & Kerfeld, Cheryl A. Local and global structural drivers for the photoactivation of the orange carotenoid protein. United States. doi:10.1073/pnas.1512240112.
Gupta, Sayan, Guttman, Miklos, Leverenz, Ryan L., Zhumadilova, Kulyash, Pawlowski, Emily G., Petzold, Christopher J., Lee, Kelly K., Ralston, Corie Y., and Kerfeld, Cheryl A. Fri . "Local and global structural drivers for the photoactivation of the orange carotenoid protein". United States. doi:10.1073/pnas.1512240112. https://www.osti.gov/servlets/purl/1378589.
@article{osti_1378589,
title = {Local and global structural drivers for the photoactivation of the orange carotenoid protein},
author = {Gupta, Sayan and Guttman, Miklos and Leverenz, Ryan L. and Zhumadilova, Kulyash and Pawlowski, Emily G. and Petzold, Christopher J. and Lee, Kelly K. and Ralston, Corie Y. and Kerfeld, Cheryl A.},
abstractNote = {Here, photoprotective mechanisms are of fundamental importance for the survival of photosynthetic organisms. In cyanobacteria, the orange carotenoid protein (OCP), when activated by intense blue light, binds to the light-harvesting antenna and triggers the dissipation of excess captured light energy. Using a combination of small angle X-ray scattering (SAXS), X-ray hydroxyl radical footprinting, circular dichroism, and H/D exchange mass spectrometry, we identified both the local and global structural changes in the OCP upon photoactivation. SAXS and H/D exchange data showed that global tertiary structural changes, including complete domain dissociation, occur upon photoactivation, but with alteration of secondary structure confined to only the N terminus of the OCP. Microsecond radiolytic labeling identified rearrangement of the H-bonding network associated with conserved residues and structural water molecules. Collectively, these data provide experimental evidence for an ensemble of local and global structural changes, upon activation of the OCP, that are essential for photoprotection.},
doi = {10.1073/pnas.1512240112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 41,
volume = 112,
place = {United States},
year = {2015},
month = {9}
}

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