Abstract
Cyanobacteria have produced Earth’s oxygen for 2.4 billion years by adapting to fluctuating irradiance. This adaptation relies on orange carotenoid protein (OCP), which mediates light-intensity– dependent photoprotective energy dissipation using a unique two-photon absorption mechanism. Photon absorption by ground-state OCP (OCP O ) generates a metastable intermediate (OCP 1hν ) that either relaxes thermally or, upon absorption of a second photon within ∼1 s, converts to the active photoprotective state (OCP R ). By integrating static and time-resolved crystallography, cryo-EM, computation, spectroscopy and biochemistry, we assign the structure of OCP 1hν , establish its functional relevance and capture structural snapshots along the OCP O →OCP 1hν and OCP 1hν →OCP R photochemical pathways. We elucidate the molecular mechanism of OCP, which serves as a unique biological circuit breaker protecting the photosynthetic machinery from high light flux.
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Structural basis of the two-photon photoactivation mechanism of orange carotenoid protein
Abstract
Cyanobacteria have produced Earth’s oxygen for 2.4 billion years by adapting to fluctuating irradiance. This adaptation relies on orange carotenoid protein (OCP), which mediates light-intensity– dependent photoprotective energy dissipation using a unique two-photon absorption mechanism. Photon absorption by ground-state OCP (OCPO) generates a metastable intermediate (OCP1hν) that either relaxes thermally or, upon absorption of a second photon within ∼1 s, converts to the active photoprotective state (OCPR). By integrating static and time-resolved crystallography, cryo-EM, computation, spectroscopy and biochemistry, we assign the structure of OCP1hν, establish its functional relevance and capture structural snapshots along the OCPO→OCP1hν and OCP1hν→OCPR photochemical pathways. We elucidate the molecular mechanism of OCP, which serves as a unique biological circuit breaker protecting the photosynthetic machinery from high light flux.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
One Sentence Summary: Snapshots of a biological light intensity sensor reveal intermediates in consecutive two photon driven reactions.
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