Where does your gene come from? Evolution of light‐emitting enzymes in luminous organisms

Delroisse, Jérôme;Duchatelet, Laurent;Flammang, Patrick;Mallefet, Jérôme
(2022) 21st International Symposium on Bioluminescence & ChemiluminescencE — Location: Gijon, Spain (31.May.2022)

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Authors
  • Delroisse, JérômeBiology of Marine Organisms and Biomimetics, Research Institute for Biosciences, University of Mons (UMONS), Mons, Belgium.
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  • Flammang, PatrickBiology of Marine Organisms and Biomimetics, Research Institute for Biosciences, University of Mons (UMONS), Mons, Belgium.
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Abstract
(en) Bioluminescence the emission of visible light by living organisms relies on the oxidation of a luciferin substrate catalysed by a luciferase enzyme ([1], for review). This famous terminology may give the false idea that all luminous organisms are using identical or homologous molecular tools to achieve bioluminescence. Instead, multiple light emission systems co‐emerged independently along the tree of life resulting in a plethora of non‐homologous luciferases ([2], for review). To investigate the diversity of known luciferase proteins (including luciferases stricto sensu and photoproteins), we analysed a total of 134 sequences coming from 75 species and 11 phyla. The global dataset was analysed using a sequence‐similarity‐based clustering approach based on BLASTp e‐values and using the CLANS software [3]. We identified 12 distinct groups of luciferases, each comprising homologous proteins but with no homology between groups [4]. In addition, non‐luciferase ‐ but homologous enzymes were added to the analyses to illustrate the evolutionary context of each identified group. It appears that phylogenetically related organisms may sometimes use non‐homologous luciferases (e.g., case of luminous decapods, ostracods, and copepods within Pancrustacea) but also that phylogenetically distant organisms may use homologous luciferases (e.g., case of the brittle star Amphiura filiformis and the sea pansy Renilla). Genes coding for luciferases may then have emerged as new genes or have been co‐opted from ancestral non‐luciferase genes (i.e., with an ancestral function unrelated to bioluminescence). Evolution (and natural selection, in particular) indeed often promotes evolutionary innovation by co‐opting preexisting genes for new functions. In this latter case, the homologous gene co‐ options may occur independently in phylogenetically distant organisms (i.e., parallel evolution) as observed in the case of the brittle star/sea pansy luciferases [5]. As already suggested for other types of proteins (e.g., [6]), our findings suggest that co‐option may be an underappreciated process underpinning protein neofunctionalisation , in particular in the context of luciferase evolution.
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Citations

Delroisse, J., Duchatelet, L., Flammang, P., & Mallefet, J. (2022). Where does your gene come from? Evolution of light‐emitting enzymes in luminous organisms. 21st International Symposium on Bioluminescence & ChemiluminescencE, Gijon, Spain. https://hdl.handle.net/2078.5/240750