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Triplet-driven chemical reactivity of β-carotene and its biological implications

Mateusz Zbyradowski, Mariusz Duda, Anna Wisniewska-Becker, Heriyanto, Weronika Rajwa, Joanna Fiedor, Dragan Cvetkovic, Mariusz Pilch and Leszek Fiedor ()
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Mateusz Zbyradowski: Jagiellonian University
Mariusz Duda: Jagiellonian University
Anna Wisniewska-Becker: Jagiellonian University
Heriyanto: Jagiellonian University
Weronika Rajwa: Jagiellonian University
Joanna Fiedor: AGH-University of Science and Technology
Dragan Cvetkovic: University of Niš
Mariusz Pilch: Jagiellonian University
Leszek Fiedor: Jagiellonian University

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

Abstract: Abstract The endoperoxides of β-carotene (βCar-EPOs) are regarded as main products of the chemical deactivation of 1O2 by β-carotene, one of the most important antioxidants, following a concerted singlet-singlet reaction. Here we challenge this view by showing that βCar-EPOs are formed in the absence of 1O2 in a non-concerted triplet-triplet reaction: 3O2 + 3β-carotene → βCar-EPOs, in which 3β-carotene manifests a strong biradical character. Thus, the reactivity of β-carotene towards oxygen is governed by its excited triplet state. βCar-EPOs, while being stable in the dark, are photochemically labile, and are a rare example of nonaromatic endoperoxides that release 1O2, again not in a concerted reaction. Their light-induced breakdown triggers an avalanche of free radicals, which accounts for the pro-oxidant activity of β-carotene and the puzzling swap from its anti- to pro-oxidant features. Furthermore, we show that βCar-EPOs, and carotenoids in general, weakly sensitize 1O2. These findings underlie the key role of the triplet state in determining the chemical and photophysical features of β-carotene. They shake up the prevailing models of carotenoid photophysics, the anti-oxidant functioning of β-carotene, and the role of 1O2 in chemical signaling in biological photosynthetic systems. βCar-EPOs and their degradation products are not markers of 1O2 and oxidative stress but of the overproduction of extremely hazardous chlorophyll triplets in photosystems. Hence, the chemical signaling of overexcitation of the photosynthetic apparatus is based on a 3chlorophyll-3β-carotene relay, rather than on extremely short-lived 1O2.

Date: 2022
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DOI: 10.1038/s41467-022-30095-z

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