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Marine Biology

, 166:21 | Cite as

Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark photophores

  • Laurent DuchateletEmail author
  • Julien M. Claes
  • Jérôme Mallefet
Short note

Abstract

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.

Notes

Acknowledgements

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).

Author contributions

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.

Funding

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.

Ethical statement

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.

Data accessibility

All data supporting the paper are presented in the main manuscript.

References

  1. Bertolesi GE, Vazhappilly ST, Herh CL, McFarlane S (2015) Pharmacological induction of skin pigmentation unveils the neuroendocrine circuit regulated by light. Pigment Cell Melanoma Res. 29(2):186–198.  https://doi.org/10.1111/pcmr.12442 CrossRefGoogle Scholar
  2. Claes JM, Mallefet J (2008) Early development of bioluminescence suggests camouflage by counter-illumination in the velvet belly lantern shark Etmopterus spinax (Squaloidea: Etmopteridae). J Fish Biol 73(6):1337–1350.  https://doi.org/10.1111/j.10958649.2008.02006.x CrossRefGoogle Scholar
  3. Claes JM, Mallefet J (2009) Hormonal control of luminescence from lantern shark (Etmopterus spinax) photophores. J Exp Biol 212(22):3684–3692.  https://doi.org/10.1242/jeb.034363 CrossRefPubMedGoogle Scholar
  4. Claes JM, Mallefet J (2010) The lantern shark’s light switch: turning shallow water crypsis into midwater camouflage. Biol Lett 6(5):685–687.  https://doi.org/10.1098/rsbl.2010.0167 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Claes JM, Mallefet J (2014) Ecological functions of shark luminescence. Luminescence 29(1):13–15CrossRefGoogle Scholar
  6. Claes JM, Aksnes DL, Mallefet J (2010a) Phantom hunter of the fjords: camouflage by counterillumination in a shark (Etmopterus spinax). J Exp Mar Biol Ecol 388(1–2):28–32.  https://doi.org/10.1016/j.jembe.2010.03.009 CrossRefGoogle Scholar
  7. Claes JM, Krönström J, Holmgren S, Mallefet J (2010b) Nitric oxide in the control of luminescence from lantern shark (Etmopterus spinax) photophores. J Exp Mar Biol. 213:3005–3011.  https://doi.org/10.1242/jeb.040410 CrossRefGoogle Scholar
  8. Claes JM, Krönström J, Holmgren S, Mallefet J (2011) GABA inhibition of luminescence from lantern shark (Etmopterus spinax) photophores. Comp Biochem Physiol C Toxicol Pharmacol 153(2):231–236.  https://doi.org/10.1016/j.cbpc.2010.11.002 CrossRefPubMedGoogle Scholar
  9. Claes JM, Nilsson D-E, Mallefet J, Straube N (2015) The presence of lateral photophores correlates with increased speciation in deep-sea bioluminescent sharks. R Soc Open Sci. 2(7):150219.  https://doi.org/10.1098/rsos.150219 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Clarke WD (1963) Function of bioluminescence in mesopelagic organisms. Nature 198:1244–1246.  https://doi.org/10.1038/1981244a0 CrossRefGoogle Scholar
  11. Delroisse J, Ullrich-Lüter E, Ortega-Martinez O, Dupont S, Arnone MI, Mallefet J, Flammang P (2014) High opsin diversity in a non-visual infaunal brittle star. BMC Genom 15(1):1035.  https://doi.org/10.1186/1471-2164-15-1035 CrossRefGoogle Scholar
  12. Delroisse J, Duchatelet L, Flammang P, Mallefet J (2018) De novo transcriptome analyses provide insights into opsin-based photoreception in the lanternshark Etmopterus spinax. PLoS One 13(12):e0209767.  https://doi.org/10.1371/journal.pone.0209767 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Denton EJ, Gilpin-Brown JB, Wright PG (1972) The angular distribution of the light produced by some mesopelagic fish in relation to their camouflage. Proc R Soc B 182:145–158.  https://doi.org/10.1098/rspb.1972.0071 CrossRefGoogle Scholar
  14. Denton EJ, Herring PJ, Widder EA, Latz MF, Case JF (1985) The role of filters in the photophore of oceanic animals and their relation to vision in the oceanic environment. Proc R Soc B 225:63–97.  https://doi.org/10.1098/rspb.1985.0051 CrossRefGoogle Scholar
  15. Haddock SDH, Moline MA, Case JF (2010) Bioluminescence in the sea. Annu Rev Mar Sci. 2:443–493.  https://doi.org/10.1146/annurev-marine-120308-081028 CrossRefGoogle Scholar
  16. Harper RD, Case JF (1999) Disruptive counterillumination and its anti-predatory value in the plainfish midshipman Porichthys notatus. Mar Biol 134(3):529–540.  https://doi.org/10.1007/s002270050568 CrossRefGoogle Scholar
  17. Johnsen S, Widder EA, Mobley CD (2004) Propagation and perception of bioluminescence: factors affecting counterillumination as a cryptic strategy. Biol Bull 207(1):1–16.  https://doi.org/10.2307/1543624 CrossRefPubMedGoogle Scholar
  18. Jones BW, Nishiguchi MK (2004) Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar Biol 144:1151–1155.  https://doi.org/10.1007/s00227-003-1285-3 CrossRefGoogle Scholar
  19. Krönström J, Holmgren S, Baguet F, Salpietro L, Mallefet J (2005) Nitric oxide in control of luminescence from hatchetfish (Argyropelecus hemigymnus) photophores. J Exp Biol 208(15):2951–2961.  https://doi.org/10.1242/jeb.01712 CrossRefPubMedGoogle Scholar
  20. Krönström J, Dupont S, Mallefet J, Thorndyke M, Holmgren S (2007) Serotonin and nitric oxide interaction in the control of bioluminescence in northern krill, Meganyctiphanes norvegica (M. Sars). J Exp Biol 210:3179–3187.  https://doi.org/10.1242/jeb.002394 CrossRefPubMedGoogle Scholar
  21. Krönström J, Karlsson W, Johansson BR, Holmgren S (2009) Involvement of contractile elements in control of bioluminescence in Northern krill, Meganyctiphanes norvegica (M. Sars). Cell Tissue Res 336:299.  https://doi.org/10.1007/s00441-009-0774-1 CrossRefPubMedGoogle Scholar
  22. Latz MI (1995) Physiological mechanisms in the control of bioluminescent countershading in a midwater shrimp. Mar Freshw Behav Phys. 26(2–4):207–218.  https://doi.org/10.1080/10236249509378940 CrossRefGoogle Scholar
  23. Nealson KH, Hastings JW (1979) Bacterial bioluminescence: its control and ecological significance. Microbiol Rev 43(4):496–518PubMedPubMedCentralGoogle Scholar
  24. Oba Y, Stevani CV, Oliveira AG, Tsarkova AS, Chepurnykh TV, Yampolsky IV (2016) Selected least studied but not forgotten bioluminescent systems. Photochem Photobiol 93(2):405–415.  https://doi.org/10.1111/php.12704 CrossRefGoogle Scholar
  25. Regazzetti C, Sormani L, Debayle D, Bernerd F, Tulic MK, De Donatis GM, Chignon-Sicard B, Rocchi S, Passeron T (2018) Melanocytes sense blue light and regulate pigmentation through opsin-3. J Invest Dermatol 138(1):171–178.  https://doi.org/10.1016/j.jid.2017.07.833 CrossRefPubMedGoogle Scholar
  26. Renwart M, Mallefet J (2013) First study of the chemistry of the luminous system in a deep- sea shark, Etmopterus spinax Linnaeus, 1758 (Chondrichthyes: Etmopteridae). J Exp Mar Biol Ecol 448:214–219.  https://doi.org/10.1016/j.jembe.2013.07.010 CrossRefGoogle Scholar
  27. Renwart M, Delroisse J, Claes JM, Mallefet J (2014) Ultrastructural organization of lantern shark (Etmopterus spinax Linnaeus, 1758) photophores. Zoomorphology 133(4):405–416.  https://doi.org/10.1007/s00435-014-0230-y CrossRefGoogle Scholar
  28. Renwart M, Delroisse J, Flammang P, Claes JM, Mallefet J (2015) Cytological changes during luminescence production in lanternshark (Etmopterus spinax Linnaeus, 1758) photophores. Zoomorphology 134(1):107–116.  https://doi.org/10.1007/s00435-014-0235-6 CrossRefGoogle Scholar
  29. Schnitzler CE, Pang K, Powers ML, Reitzel AM, Ryan JF, Simmons D, Tada T, Park M, Gupta J, Brooks SY et al (2012) Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. BMC Biol 10(1):107.  https://doi.org/10.1186/1741-7007-10-107 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ (2009) Evidence for light perception in a bioluminescent organ. Proc Natl Acad Sci USA. 106(24):9836–9841.  https://doi.org/10.1073/pnas.0904571106 CrossRefPubMedGoogle Scholar
  31. Warner JA, Latz MI, Case JF (1979) Cryptic bioluminescence in a midwater shrimp. Science 203:1109–1110.  https://doi.org/10.1126/science.203.4385.1109 CrossRefPubMedGoogle Scholar
  32. Young RE, Mencher FM (1980) Bioluminescence in mesopelagic squid: diel color change during counterillumination. Science 208:1286–1288.  https://doi.org/10.1126/science.208.4449.1286 CrossRefPubMedGoogle Scholar
  33. Young RE, Roper CF, Walters JF (1979) Eyes and extraocular photoreceptors in midwater cephalopods and fishes: their roles in detecting downwelling light for counterillumination. Mar Biol 51(4):371–380.  https://doi.org/10.1007/BF00389215 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Marine Biology Laboratory, Earth and Life InstituteUniversité Catholique de LouvainLouvain-La-NeuveBelgium

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