From extraocular photoreception to pigment movement regulation: a new control mechanism of the lanternshark luminescence

Laurent Duchatelet,Akihisa Terakita,Jérôme Mallefet,René Rezsohazy,Tomohiro Sugihara,Mitsumasa Koyanagi,Jérôme Delroisse

doi:10.1038/s41598-020-67287-w

Laurent Duchatelet, Akihisa Terakita + Show 5 more

Open Access

https://doi.org/10.1038/s41598-020-67287-w

Copy DOI

Abstract

The velvet belly lanternshark, Etmopterus spinax, uses counterillumination to disappear in the surrounding blue light of its marine environment. This shark displays hormonally controlled bioluminescence in which melatonin (MT) and prolactin (PRL) trigger light emission, while α-melanocyte-stimulating hormone (α-MSH) and adrenocorticotropic hormone (ACTH) play an inhibitory role. The extraocular encephalopsin (Es-Opn3) was also hypothesized to act as a luminescence regulator. The majority of these compounds (MT, α-MSH, ACTH, opsin) are members of the rapid physiological colour change that regulates the pigment motion within chromatophores in metazoans. Interestingly, the lanternshark photophore comprises a specific iris-like structure (ILS), partially composed of melanophore-like cells, serving as a photophore shutter. Here, we investigated the role of (i) Es-Opn3 and (ii) actors involved in both MT and α-MSH/ACTH pathways on the shark bioluminescence and ILS cell pigment motions. Our results reveal the implication of Es-Opn3, MT, inositol triphosphate (IP3), intracellular calcium, calcium-dependent calmodulin and dynein in the ILS cell pigment aggregation. Conversely, our results highlighted the implication of the α-MSH/ACTH pathway, involving kinesin, in the dispersion of the ILS cell pigment. The lanternshark luminescence then appears to be controlled by the balanced bidirectional motion of ILS cell pigments within the photophore. This suggests a functional link between photoreception and photoemission in the photogenic tissue of lanternsharks and gives precious insights into the bioluminescence control of these organisms.

Highlights

The velvet belly lanternshark, Etmopterus spinax, uses counterillumination to disappear in the surrounding blue light of its marine environment
Our results revealed the implication of Es-Opn[3], MT, IP3, intracellular calcium, calcium-dependent calmodulin and dynein in the iris-like structure (ILS) cell pigment aggregation
Even if previous studies depicted an inefficient activation of Gq protein in Mos-Opn[3] expressing cells[90], our results suggested that Es-Opn[3] would rather be linked to a Gq than a Gi/o protein, or that β/γ subunit of the Gi/o protein might be able to trigger an IP3 intracellular modulation and do not modify cyclic adenosine monophosphate (cAMP) intracellular level

Summary

Introduction

The velvet belly lanternshark, Etmopterus spinax, uses counterillumination to disappear in the surrounding blue light of its marine environment. Pathways controlling colour modifications involve the motion of pigmented granule (i.e. aggregation and dispersion) These processes appeared to be conserved across metazoans with common use of multiple molecular actors (e.g. melatonin, melanocortin, prolactin, γ-aminobutyric acid, calcineurin, cyclic adenosine monophosphate, inositol triphosphate, dynein, kinesin, extraocular opsins, melanin) in a large diversity of organisms[6,7,8,9,10,11,12,13,14,15,16]. The remaining literature on E. spinax ecological traits mainly deal with parasitism[66,67,68] or highlight fishery issues[69,70]

Methods

Results

Discussion

Conclusion