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:

Gupta, Sayan ^[1]; Guttman, Miklos ^[2]; Leverenz, Ryan L. ^[3]; Zhumadilova, Kulyash ^[4]; Pawlowski, Emily G. ^[3]; Petzold, Christopher J. ^[1]; Lee, Kelly K. ^[2]; Ralston, Corie Y. ^[1]; Kerfeld, Cheryl A. ^[5]

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+ Show Author Affiliations

1. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
2. Department of Medicinal Chemistry, University of Washington, Seattle, WA 98195,
3. Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,
4. School of Science and Technology, Nazarbayev University, Astana 010000, Kazakhstan,
5. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720,, Department of Energy Plant Research Laboratory, Michigan State University, East Lansing, MI 48824,, Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720,, Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824

Publication Date:

Fri Sep 18 00:00:00 EDT 2015

Research Org.:

Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE; National Institutes of Health (NIH)

OSTI Identifier:

1579281

Alternate Identifier(s):

OSTI ID: 1378589

Grant/Contract Number:  

FG02-91ER20021; AC02-05CH11231

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 112 Journal Issue: 41; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

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