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Light activation of Orange Carotenoid Protein reveals bicycle-pedal single-bond isomerization

Volha U. Chukhutsina, James M. Baxter, Alisia Fadini, Rhodri M. Morgan, Matthew A. Pope, Karim Maghlaoui, Christian M. Orr, Armin Wagner and Jasper J. Thor ()
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Volha U. Chukhutsina: Imperial College London
James M. Baxter: Imperial College London
Alisia Fadini: Imperial College London
Rhodri M. Morgan: Imperial College London
Matthew A. Pope: Imperial College London
Karim Maghlaoui: Imperial College London
Christian M. Orr: Harwell Science and Innovation Campus
Armin Wagner: Harwell Science and Innovation Campus
Jasper J. Thor: Imperial College London

Nature Communications, 2022, vol. 13, issue 1, 1-14

Abstract: Abstract Orange Carotenoid protein (OCP) is the only known photoreceptor which uses carotenoid for its activation. It is found exclusively in cyanobacteria, where it functions to control light-harvesting of the photosynthetic machinery. However, the photochemical reactions and structural dynamics of this unique photosensing process are not yet resolved. We present time-resolved crystal structures at second-to-minute delays under bright illumination, capturing the early photoproduct and structures of the subsequent reaction intermediates. The first stable photoproduct shows concerted isomerization of C9’-C8’ and C7’-C6’ single bonds in the bicycle-pedal (s-BP) manner and structural changes in the N-terminal domain with minute timescale kinetics. These are followed by a thermally-driven recovery of the s-BP isomer to the dark state carotenoid configuration. Structural changes propagate to the C-terminal domain, resulting, at later time, in the H-bond rupture of the carotenoid keto group with protein residues. Solution FTIR and UV/Vis spectroscopy support the single bond isomerization of the carotenoid in the s-BP manner and subsequent thermal structural reactions as the basis of OCP photoreception.

Date: 2022
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DOI: 10.1038/s41467-022-34137-4

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