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The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways

Carotenoids are isoprenoid lipids found across the tree of life with important implications in oxidative stress adaptations, photosynthetic metabolisms, as well as in membrane dynamics. The canonical view is that C40 carotenoids are synthesized from phytoene and C30 carotenoids from diapophytoene. S...

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Autores principales: Santana-Molina, Carlos, Henriques, Valentina, Hornero-Méndez, Damaso, Devos, Damien P., Rivas-Marin, Elena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907078/
https://www.ncbi.nlm.nih.gov/pubmed/36534808
http://dx.doi.org/10.1073/pnas.2210081119
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author Santana-Molina, Carlos
Henriques, Valentina
Hornero-Méndez, Damaso
Devos, Damien P.
Rivas-Marin, Elena
author_facet Santana-Molina, Carlos
Henriques, Valentina
Hornero-Méndez, Damaso
Devos, Damien P.
Rivas-Marin, Elena
author_sort Santana-Molina, Carlos
collection PubMed
description Carotenoids are isoprenoid lipids found across the tree of life with important implications in oxidative stress adaptations, photosynthetic metabolisms, as well as in membrane dynamics. The canonical view is that C40 carotenoids are synthesized from phytoene and C30 carotenoids from diapophytoene. Squalene is mostly associated with the biosynthesis of polycyclic triterpenes, although there have been suggestions that it could also be involved in the biosynthesis of C30 carotenoids. However, demonstration of the existence of this pathway in nature is lacking. Here, we demonstrate that C30 carotenoids are synthesized from squalene in the Planctomycetes bacteria and that this squalene route to C30 carotenoids is the most widespread in prokaryotes. Using the evolutionary history of carotenoid and squalene amino oxidases, we propose an evolutionary scenario to explain the origin and diversification of the different carotenoid and squalene-related pathways. We show that carotenoid biosynthetic pathways have been constantly transferred and neofunctionalized during prokaryotic evolution. One possible origin of the squalene pathway connects it with the one of C40 carotenoid synthesis of Cyanobacteria. The widespread occurrence of the squalene route to C30 carotenoids in Bacteria increases the functional repertoire of squalene, establishing it as a general hub of carotenoids and polycyclic triterpenes synthesis.
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spelling pubmed-99070782023-02-08 The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways Santana-Molina, Carlos Henriques, Valentina Hornero-Méndez, Damaso Devos, Damien P. Rivas-Marin, Elena Proc Natl Acad Sci U S A Biological Sciences Carotenoids are isoprenoid lipids found across the tree of life with important implications in oxidative stress adaptations, photosynthetic metabolisms, as well as in membrane dynamics. The canonical view is that C40 carotenoids are synthesized from phytoene and C30 carotenoids from diapophytoene. Squalene is mostly associated with the biosynthesis of polycyclic triterpenes, although there have been suggestions that it could also be involved in the biosynthesis of C30 carotenoids. However, demonstration of the existence of this pathway in nature is lacking. Here, we demonstrate that C30 carotenoids are synthesized from squalene in the Planctomycetes bacteria and that this squalene route to C30 carotenoids is the most widespread in prokaryotes. Using the evolutionary history of carotenoid and squalene amino oxidases, we propose an evolutionary scenario to explain the origin and diversification of the different carotenoid and squalene-related pathways. We show that carotenoid biosynthetic pathways have been constantly transferred and neofunctionalized during prokaryotic evolution. One possible origin of the squalene pathway connects it with the one of C40 carotenoid synthesis of Cyanobacteria. The widespread occurrence of the squalene route to C30 carotenoids in Bacteria increases the functional repertoire of squalene, establishing it as a general hub of carotenoids and polycyclic triterpenes synthesis. National Academy of Sciences 2022-12-19 2022-12-27 /pmc/articles/PMC9907078/ /pubmed/36534808 http://dx.doi.org/10.1073/pnas.2210081119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Santana-Molina, Carlos
Henriques, Valentina
Hornero-Méndez, Damaso
Devos, Damien P.
Rivas-Marin, Elena
The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title_full The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title_fullStr The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title_full_unstemmed The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title_short The squalene route to C30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
title_sort squalene route to c30 carotenoid biosynthesis and the origins of carotenoid biosynthetic pathways
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907078/
https://www.ncbi.nlm.nih.gov/pubmed/36534808
http://dx.doi.org/10.1073/pnas.2210081119
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