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A 12 Å carotenoid translocation in a photoswitch associated with cyanobacterial photoprotection

Science
26 Jun 2015
Vol 348, Issue 6242
pp. 1463-1466

Protection from too much light

Photosynthetic organisms protect themselves from too much light using pigment photoswitches that absorb excess energy. Leverenz et al. analyzed the structure of an active, energy-dissipating form of the orange carotenoid protein (OCP) from a cyanobacterium. When activated by excess light, OCP moves its hydrophobic carotenoid pigment 12 Å within the protein to accommodate nonphotochemical quenching by the broader photosynthetic antenna complex.
Science, this issue p. 1463

Abstract

Pigment-protein and pigment-pigment interactions are of fundamental importance to the light-harvesting and photoprotective functions essential to oxygenic photosynthesis. The orange carotenoid protein (OCP) functions as both a sensor of light and effector of photoprotective energy dissipation in cyanobacteria. We report the atomic-resolution structure of an active form of the OCP consisting of the N-terminal domain and a single noncovalently bound carotenoid pigment. The crystal structure, combined with additional solution-state structural data, reveals that OCP photoactivation is accompanied by a 12 angstrom translocation of the pigment within the protein and a reconfiguration of carotenoid-protein interactions. Our results identify the origin of the photochromic changes in the OCP triggered by light and reveal the structural determinants required for interaction with the light-harvesting antenna during photoprotection.

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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S9
Tables S1 to S6
References (3147)

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Information & Authors

Information

Published In

Science
Volume 348 | Issue 6242
26 June 2015

Submission history

Received: 19 January 2015
Accepted: 8 May 2015
Published in print: 26 June 2015

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Acknowledgments

Supported by the U.S. Department of Energy (DOE), Basic Energy Sciences, award DE-FG02-91ER20021. We thank the staff at the Berkeley Center for Structural Biology, which is supported in part by the National Institute of General Medical Sciences and the Howard Hughes Medical Institute. We thank R. Celestre for assistance at beamline 5.3.1. The Advanced Light Source at Lawrence Berkeley National Laboratory is supported by the Office of Science, Office of Basic Energy Sciences, of the U.S. DOE under contract no. DE-AC02-05CH11231. This research used resources of the National Energy Research Scientific Computing Center, a DOE Office of Science User Facility supported by the Office of Science of the U.S. DOE under contract no. DE-AC02-05CH11231 and of the Joint BioEnergy Institute supported by the Office of Science, Office of Biological and Environmental Research, of the U.S. DOE under contract DE-AC02-05CH11231. A.W., A.T., C.B., and D.K. are supported by a grant from the Agence Nationale de la Recherche (ANR, project CYANOPROTECT), and used resources of CNRS and the Commissariat à l’Energie Atomique (CEA). We thank S. Cot for technical assistance. Coordinates have been deposited in the RCSB Protein Data Bank under accession codes 4XB4 (RCPCAN) and 4XB5 (OCPCAN).

Authors

Affiliations

Ryan L. Leverenz*
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USA.
Markus Sutter*
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USA.
Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Adjélé Wilson
Commissariat à l’Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTec-S), 91191 Gif-sur-Yvette, France.
Centre National de la Recherche Scientifique (CNRS), I2BC, UMR 9198, 91191 Gif-sur-Yvette, France.
Sayan Gupta
Berkeley Center for Structural Biology, Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Adrien Thurotte
Commissariat à l’Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTec-S), 91191 Gif-sur-Yvette, France.
Centre National de la Recherche Scientifique (CNRS), I2BC, UMR 9198, 91191 Gif-sur-Yvette, France.
Céline Bourcier de Carbon
Commissariat à l’Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTec-S), 91191 Gif-sur-Yvette, France.
Centre National de la Recherche Scientifique (CNRS), I2BC, UMR 9198, 91191 Gif-sur-Yvette, France.
Christopher J. Petzold
Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Corie Ralston
Berkeley Center for Structural Biology, Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
François Perreau
INRA, Institut Jean-Pierre Bourgin, UMR 1318, ERL CNRS 3559, Saclay Plant Sciences, RD10, F-78026 Versailles, France.
Diana Kirilovsky
Commissariat à l’Energie Atomique (CEA), Institut de Biologie et Technologies de Saclay (iBiTec-S), 91191 Gif-sur-Yvette, France.
Centre National de la Recherche Scientifique (CNRS), I2BC, UMR 9198, 91191 Gif-sur-Yvette, France.
Cheryl A. Kerfeld [email protected]
MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI 48824, USA.
Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA.

Notes

*
These authors contributed equally to this work.
Corresponding author. E-mail: [email protected]

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