Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark photophores
Counterilluminating animals produce a ventral light to hide their silhouette in the water column. This midwater camouflage technique requires a fine and dynamic control of the wavelength, angular distribution, and intensity of their luminescence, which needs to continuously match ambient downwelling light. Recently, extraocular opsins have been suggested to play a role in the bioluminescence control of several organisms, such as squids, comb jellies, or brittle stars, providing a way for photogenic structures to perceive their own light output. By analysing a growing embryonic series of the velvet belly lanternshark, Etmopterus spinax, we show that the development of lanternshark luminescence competence is associated with the expression of encephalopsin within epidermal cells and in the light-regulating structure of the photogenic organs. Such an intra-uterine expression of encephalopsin strongly supports this blue-sensitive extraocular opsin to allow bioluminescence perception in lanternshark photophores and suggests a clear physiological interaction between photoemission and photoperception.
The authors would like to thank T. Sorlie from the Espegrend Marine Biological Station (University of Bergen, Norway) for the help during E. spinax collection. We also acknowledge Olivia Vinolo for the help provided during immunodetection experiments. The authors want to acknowledge Dr. G. Naylor for helpful reading and corrections as well as the anonymous reviewers whose comments improve the present manuscript. LD is PhD students under a FRIA fellowship, JC is scientific collaborator of the Université Catholique de Louvain Marine Biology Laboratory and JM is Research Associate to FRS–FNRS. This paper is a contribution to the Biodiversity Research Center (BDIV) and the Center Interuniversitaire de Biologie Marine (CIBIM).
LD performed, analysed, and interpreted the immunodetection and was a major contributor in writing and revising the manuscript. JC revised the manuscript. JM took live pictures, supervised the work, contributed to, and revised the manuscript. Both authors read and approved the final manuscript.
This work was supported by a grant from the Fonds de la Recherche Scientifique (FRIA/FRS–FNRS, Belgium) to LD and an FRS–FNRS Grant (FRFC 2.4516.01) awarded to the Université Catholique de Louvain Marine Biology Laboratory and the Université de Mons Biology of Marine Organisms and Biomimetics Laboratory.
Compliance with ethical standards
Conflict of interest
All authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. The shark collection and experiments were performed under the “Experimental fish care PERMIT” Number 12/14048. Following the local instructions for experimental fish care (Permit 12/14048), captive animals were euthanized by a blow to the head followed by a full incision of the spinal cord at the back of the head. Animal procedures were conducted in compliance with the Belgian national guidelines and in agreement with the European directive 2010/63/UE, under the approval of the Animal Ethics Committee of the Catholic University of Louvain in Louvain-la-Neuve. This article does not contain any studies with human participants performed by any of the authors.
All data supporting the paper are presented in the main manuscript.
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