Skip to main content
SpringerLink
Log in

Cytological changes during luminescence production in lanternshark (Etmopterus spinax Linnaeus, 1758) photophores

  • Original Paper
  • Published:
Zoomorphology Aims and scope Submit manuscript

Abstract

Studying an organism’s photogenic structures at the ultrastructural level is a key step in the understanding of its light-emission process. Recently, the photophore ultrastructure of the deep-sea lanternshark Etmopterus spinax Linnaeus, 1758 was described. The photocytes appeared to be divided into three areas including an apical granular area, which contains inclusions and was hypothesized to be the light-producing reaction site. In this study, we investigated the morphological changes occurring within the granular area during the bioluminescent emissions induced by two hormones: prolactin and melatonin. Prolactin provoked the formation of new structures in the granular area, the “grey particles”, whose number was proportional to the amount of light produced by the reaction. An increase in the number of granular inclusions was also detected at the end of the prolactin-induced light emission. Conversely, melatonin induced a decrease in the number of granular inclusions and an increase in their diameter. An effect of hormones was also observed on the iris-like structure where they triggered pigment retraction and hence an increase in the iris aperture diameter. This is consistent with previous findings and is shown for the first time at the cellular level. The possible role of grey particles in E. spinax light-emission mechanism is discussed, while granular inclusion is considered to be E. spinax’s intracellular luminescence site. Regarding typical shark long-lasting glows, a new term (“glowon”) is proposed to characterize this novel membrane-free microsource.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anctil M (1977) Development of bioluminescence and photophores in the midshipman fish, Porichthys notatus. J Morphol 151:363–396

    Article  CAS  PubMed  Google Scholar 

  • Anctil M (1979) Ultrastructural correlates of luminescence in Porichthys photophores. I. Effects of spinal cord stimulation and exogenous noradrenaline. Rev Can Biol 38:67–80

    CAS  PubMed  Google Scholar 

  • Anderson JM, Cormier MJ (1973) Lumisomes, the cellular site of bioluminescence in coelenterates. J Biol Chem 248:2937–2943

    CAS  PubMed  Google Scholar 

  • Bassot J-M, Bilbaut A (1977) Bioluminescence des élytres d’Acholoe. IV. Luminescence et fluorescence des photosomes. Biol Cellulaire 28:163–168

    Google Scholar 

  • Bassot J-M, Nicolas G (1987) An optional dyadic junctional complex revealed by fast-freeze fixation in the bioluminescent system of the scale worm. J Cell Biol 105:2245–2256

    Article  CAS  PubMed  Google Scholar 

  • Bernal D, Donley JM, Shadwick RE, Syme DA (2005) Mammal-like muscles power swimming in a cold-water shark. Nature 437:1349–1352

    Article  CAS  PubMed  Google Scholar 

  • 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 73:1337–1350

    Article  Google Scholar 

  • Claes JM, Mallefet J (2009a) Bioluminescence of sharks: first synthesis. In: Meyer-Rochow VB (ed) Bioluminescence in focus—a collection of illuminating essays. Research Signpost, Kerala, pp 51–65

    Google Scholar 

  • Claes JM, Mallefet J (2009b) Hormonal control of luminescence from lantern shark (Etmopterus spinax) photophores. J Exp Biol 212:3684–3692

    Article  CAS  PubMed  Google Scholar 

  • Claes JM, Mallefet J (2010a) Functional physiology of lantern shark (Etmopterus spinax) luminescent pattern: differential hormonal regulation of luminous zones. J Exp Biol 213:1852–1858

    Article  PubMed  Google Scholar 

  • Claes JM, Mallefet J (2010b) The lantern shark’s light switch: turning shallow water crypsis into midwater camouflage. Biol Lett 6:685–687

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 388:28–32

    Article  Google Scholar 

  • Claes JM, Krönström J, Holmgren S, Mallefet J (2010b) Nitric oxide in the control of luminescence from lantern shark (Etmopterus spinax) photophores. J Exp Biol 213:3005–3011

    Article  CAS  PubMed  Google Scholar 

  • Claes JM, Krönström J, Holmgren S, Mallefet J (2011) GABA inhibition of luminescence from lantern shark (Etmopterus spinax) photophores. Comp Biochem Physiol 153C:231–236

    CAS  Google Scholar 

  • Claes JM, Dean MN, Nilsson D-E, Hart NS, Mallefet J (2013) A deepwater fish with ‘lightsabers’—dorsal spine-associated luminescence in a counterilluminating lanternshark. Sci Rep 3:1308

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Claes JM, Nilsson D-E, Straube N, Collin SP, Mallefet J (2014) Iso-luminance counterillumination drove bioluminescent shark radiation. Sci Rep 4:4328

    Article  PubMed Central  PubMed  Google Scholar 

  • Deheyn D, Mallefet J, Jangoux M (2000) Cytological changes during bioluminescence production in dissociated photocytes from the ophiuroid Amphipholis squamata (Echinodermata). Cell Tissue Res 299:115–128

    Article  CAS  PubMed  Google Scholar 

  • DeSa R, Hastings JW, Vatter AE (1963) “Crystalline” particles: an organized subcellular bioluminescent system. Science 141:1269–1270

    Article  CAS  PubMed  Google Scholar 

  • Ebert DA, Fowler SL, Compagno LJ (2013) Sharks of the world: a fully illustrated guide. Wild Nature Press, Plymouth

    Google Scholar 

  • Hamanaka T, Michinomae M, Seidou M, Miura K, Inoue K, Kito Y (2011) Luciferase activity of the intracellular microcrystal of the firefly squid, Watasenia scintillans. FEBS Lett 585:2735–2738

    Article  CAS  PubMed  Google Scholar 

  • Hanson FE, Miller J, Reynolds GT (1969) Subunit coordination in the firefly light organ. Biol Bull 137:447–464

    Article  Google Scholar 

  • Renwart M, Delroisse J, Claes JM, Mallefet J (2014) Ultrastructural organization of lantern shark (Etmopterus spinax Linnaeus, 1758) photophores. Zoomorphology. doi:10.1007/s00435-014-0230-y

    Google Scholar 

  • Shimomura O (2006) Bioluminescence: chemical principles and methods. World Scientific, Singapore

    Book  Google Scholar 

  • Shimomura O, Flood PR (1998) Luciferase of the scyphozoan medusa Periphylla periphylla. Biol Bull 194:244–252

    Article  CAS  Google Scholar 

  • Smalley KN, Tarwater DE, Davidson TL (1980) Localization of fluorescent compounds in the firefly light organ. J Histochem Cytochem 28:323–329

    Article  CAS  PubMed  Google Scholar 

  • Straube N, Iglésias SP, Sellos DY, Kriwet J, Schliewen UK (2010) Molecular phylogeny and node time estimation of bioluminescent Lantern Sharks (Elasmobranchii: Etmopteridae). Mol Phylogenet Evol 56:905–917

    Article  CAS  PubMed  Google Scholar 

  • Widder EA, Latz MI, Herring PJ, Case JF (1984) Far red bioluminescence from two deep-sea fishes. Science 225:512–514

    Article  CAS  PubMed  Google Scholar 

  • Wilson T, Hastings JW (1998) Bioluminescence. Annu Rev Cell Dev Biol 14:197–230

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Fonds de la Recherche Scientifique (FRS-FNRS, Belgium) to M.R. and a grant from the Fonds de la Recherche Fondamentale Collective (FRFC—2.4525.12). J.D., P.F., J.M.C. and J.M. are, respectively, Research Fellow, Research Director, Postdoctoral Researcher and Research Associate of the FRS-FNRS. We would like to thank A. Aadnesen, manager of the Espegrend Marine Biological Station (University of Bergen, Norway) where animals were kept, and T. Sorlie for the help during field collections. This paper is a contribution to the Biodiversity Research Center (BDIV) and to the Centre Interuniversitaire de Biologie Marine (CIBIM).

Author information

Authors and Affiliations

  1. Laboratory of Marine Biology, Earth and Life Institute, Catholic University of Louvain (UCL), Place Croix du Sud 3, bt L7.06.04, 1348, Louvain-la-Neuve, Belgium

    Marie Renwart, Julien M. Claes & Jérôme Mallefet

  2. Biology of Marine Organisms and Biomimetics, University of Mons (UMONS), Avenue du Champ de Mars 6, 7000, Mons, Belgium

    Jérôme Delroisse & Patrick Flammang

Authors
  1. Marie Renwart
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jérôme Delroisse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrick Flammang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Julien M. Claes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jérôme Mallefet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marie Renwart.

Additional information

Communicated by Andreas Schmidt-Rhaesa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Renwart, M., Delroisse, J., Flammang, P. et al. Cytological changes during luminescence production in lanternshark (Etmopterus spinax Linnaeus, 1758) photophores. Zoomorphology 134, 107–116 (2015). https://doi.org/10.1007/s00435-014-0235-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-014-0235-6

Keywords

Search

Navigation