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A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence

Bioluminescence relies on the oxidation of a luciferin substrate catalysed by a luciferase enzyme. Luciferins and luciferases are generic terms used to describe a large variety of substrates and enzymes. Whereas luciferins can be shared by phylogenetically distant organisms which feed on organisms p...

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Autores principales: Delroisse, Jérôme, Ullrich-Lüter, Esther, Blaue, Stefanie, Ortega-Martinez, Olga, Eeckhaut, Igor, Flammang, Patrick, Mallefet, Jérôme
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413902/
https://www.ncbi.nlm.nih.gov/pubmed/28381628
http://dx.doi.org/10.1098/rsob.160300
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author Delroisse, Jérôme
Ullrich-Lüter, Esther
Blaue, Stefanie
Ortega-Martinez, Olga
Eeckhaut, Igor
Flammang, Patrick
Mallefet, Jérôme
author_facet Delroisse, Jérôme
Ullrich-Lüter, Esther
Blaue, Stefanie
Ortega-Martinez, Olga
Eeckhaut, Igor
Flammang, Patrick
Mallefet, Jérôme
author_sort Delroisse, Jérôme
collection PubMed
description Bioluminescence relies on the oxidation of a luciferin substrate catalysed by a luciferase enzyme. Luciferins and luciferases are generic terms used to describe a large variety of substrates and enzymes. Whereas luciferins can be shared by phylogenetically distant organisms which feed on organisms producing them, luciferases have been thought to be lineage-specific enzymes. Numerous light emission systems would then have co-emerged independently along the tree of life resulting in a plethora of non-homologous luciferases. Here, we identify for the first time a candidate luciferase of a luminous echinoderm, the ophiuroid Amphiura filiformis. Phylogenomic analyses identified the brittle star predicted luciferase as homologous to the luciferase of the sea pansy Renilla (Cnidaria), contradicting with the traditional viewpoint according to which luciferases would generally be of convergent origins. The similarity between the Renilla and Amphiura luciferases allowed us to detect the latter using anti-Renilla luciferase antibodies. Luciferase expression was specifically localized in the spines which were demonstrated to be the bioluminescent organs in vivo. However, enzymes homologous to the Renilla luciferase but unable to trigger light emission were also identified in non-luminous echinoderms and metazoans. Our findings strongly indicate that those enzymes, belonging to the haloalkane dehalogenase family, might then have been convergently co-opted into luciferases in cnidarians and echinoderms. In these two benthic suspension-feeding species, similar ecological pressures would constitute strong selective forces for the functional shift of these enzymes and the emergence of bioluminescence.
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spelling pubmed-54139022017-05-08 A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence Delroisse, Jérôme Ullrich-Lüter, Esther Blaue, Stefanie Ortega-Martinez, Olga Eeckhaut, Igor Flammang, Patrick Mallefet, Jérôme Open Biol Research Bioluminescence relies on the oxidation of a luciferin substrate catalysed by a luciferase enzyme. Luciferins and luciferases are generic terms used to describe a large variety of substrates and enzymes. Whereas luciferins can be shared by phylogenetically distant organisms which feed on organisms producing them, luciferases have been thought to be lineage-specific enzymes. Numerous light emission systems would then have co-emerged independently along the tree of life resulting in a plethora of non-homologous luciferases. Here, we identify for the first time a candidate luciferase of a luminous echinoderm, the ophiuroid Amphiura filiformis. Phylogenomic analyses identified the brittle star predicted luciferase as homologous to the luciferase of the sea pansy Renilla (Cnidaria), contradicting with the traditional viewpoint according to which luciferases would generally be of convergent origins. The similarity between the Renilla and Amphiura luciferases allowed us to detect the latter using anti-Renilla luciferase antibodies. Luciferase expression was specifically localized in the spines which were demonstrated to be the bioluminescent organs in vivo. However, enzymes homologous to the Renilla luciferase but unable to trigger light emission were also identified in non-luminous echinoderms and metazoans. Our findings strongly indicate that those enzymes, belonging to the haloalkane dehalogenase family, might then have been convergently co-opted into luciferases in cnidarians and echinoderms. In these two benthic suspension-feeding species, similar ecological pressures would constitute strong selective forces for the functional shift of these enzymes and the emergence of bioluminescence. The Royal Society 2017-04-05 /pmc/articles/PMC5413902/ /pubmed/28381628 http://dx.doi.org/10.1098/rsob.160300 Text en © 2017 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research
Delroisse, Jérôme
Ullrich-Lüter, Esther
Blaue, Stefanie
Ortega-Martinez, Olga
Eeckhaut, Igor
Flammang, Patrick
Mallefet, Jérôme
A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title_full A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title_fullStr A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title_full_unstemmed A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title_short A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
title_sort puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5413902/
https://www.ncbi.nlm.nih.gov/pubmed/28381628
http://dx.doi.org/10.1098/rsob.160300
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