Functional Characterization of Luciferase in a Brittle Star Indicates Parallel Evolution Influenced by Genomic Availability of Haloalkane Dehalogenase. - 2025
Functional Characterization of Luciferase in a Brittle Star Indicates Parallel Evolution Influenced by Genomic Availability of Haloalkane Dehalogenase.
Lau, Emily S; Majerova, Marika; Hensley, Nicholai Met al.
[en] Determining why convergent traits use distinct versus shared genetic components is crucial for understanding how evolutionary processes generate and sustain biodiversity. However, the factors dictating the genetic underpinnings of convergent traits remain incompletely understood. Here, we use heterologous protein expression, biochemical assays, and phylogenetic analyses to confirm the origin of a luciferase gene from haloalkane dehalogenases in the brittle star Amphiura filiformis. Through database searches and gene tree analyses, we also show a complex pattern of the presence and absence of haloalkane dehalogenases across organismal genomes. These results first confirm parallel evolution across a vast phylogenetic distance, because octocorals like Renilla also use luciferase derived from haloalkane dehalogenases. This parallel evolution is surprising, even though previously hypothesized, because many organisms that also use coelenterazine as the bioluminescence substrate evolved completely distinct luciferases. The inability to detect haloalkane dehalogenases in the genomes of several bioluminescent groups suggests that the distribution of this gene family influences its recruitment as a luciferase. Together, our findings highlight how biochemical function and genomic availability help determine whether distinct or shared genetic components are used during the convergent evolution of traits like bioluminescence.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Lau, Emily S ; Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA
Majerova, Marika ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Hensley, Nicholai M ; Department of Zoology, University of Cambridge, Cambridge CB2 1TN, UK
Mukherjee, Arnab ; Department of Chemical Engineering, University of California Santa Barbara, Santa Barbara, CA 93106, USA ; Department of Biological Engineering, University of California Santa Barbara, Santa Barbara, CA 93106, USA ; Department of Chemistry, University of California Santa Barbara, Santa Barbara, CA 93106, USA ; Neuroscience Research Institute, University of California Santa Barbara, Santa Barbara, CA 93106, USA
Vasina, Michal ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Pluskal, Daniel ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Damborsky, Jiri ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Prokop, Zbynek ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Delroisse, Jérôme ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Biochimie et biologie moléculaire ; Biology of Marine Organisms and Biomimetics Unit, Biosciences Research Institute, University of Mons, 7000 Mons, Belgium
Bayaert, Wendy-Shirley ; Biology of Marine Organisms and Biomimetics Unit, Biosciences Research Institute, University of Mons, 7000 Mons, Belgium
Parey, Elise ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK
Oliveri, Paola ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK
Marlétaz, Ferdinand ; Centre for Life's Origins and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK
Marek, Martin ; Loschmidt Laboratories, Department of Experimental Biology and RECETOX, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic ; International Clinical Research Center, St. Anne's University Hospital Brno, 656 91 Brno, Czech Republic
Oakley, Todd H ; Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93106, USA
Functional Characterization of Luciferase in a Brittle Star Indicates Parallel Evolution Influenced by Genomic Availability of Haloalkane Dehalogenase.
We thank Alexander Mikhailovsky for assisting with emission data collection and Vannie L. Liu for assisting with recombinant protein expression. We would like to thank the anonymous reviewers for providing useful feedback, which helped strengthen and clarify this manuscript. The work was supported by US National Science Foundation DEB-2153773 awarded to T.H.O. The authors acknowledge the use of Biological Nanostructures Laboratory (led by J. Smith) within the California NanoSystems Institute, supported by the UCSB and UCOP. This work was also supported by the Center for Scientific Computing (CSC), with computational facilities funded by the National Science Foundation (CNS-1725797). The CSC is supported by the California NanoSystems Institute and the Materials Research Science and Engineering Center (MRSEC; NSF DMR 1720256) at UC Santa Barbara. The work on this paper was supported by the Czech Science Foundation (GA22-09853S) and the Czech Ministry of Education, Youth and Sports (RECETOX RI LM2023069, e-INFRA LM2018140). This project was supported by the European Union's Horizon 2020 research and innovation program under grant agreement no. 857560 (CETOCOEN Excellence). This publication reflects only the author's view, and the European Commission is not responsible for any use that may be made of the information it contains. D.P. is a Brno Ph.D. Talent Scholarship holder funded by the Brno City Municipality. J\u00E9.D. is supported by an F.R.S.-FNRS research project (PDR, T.0071.23), previously held an F.R.S.-FNRS \u201CCharg\u00E9 de recherche\u201D fellowship (CR, 34761044), and also received financial support from an F.R.S.-FNRS research project (PDR, T.0169.20) and the Biosciences Research Institute of the University of Mons. W.-S.B. is a PhD student under a FRIA fellowship (ID 40022483). E.S.L. was funded by the National Science Foundation (GRFP 1650114). E.P. was supported by a Newton International Fellowship from the Royal Society (NIF\\R1\\222125). F.M. is supported by a Royal Society University Research Fellowship (URF\\R1\\191161) and a BBSRC research grant (BB/V01109X/1). N.M.H. was funded by the National Science Foundation (PRFB 2011040). A.M. was funded by the National Institute of Health (R35-GM133530).
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