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

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 (ip 3), 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. Camouflage is one of the most powerful anti-predatory tools on earth 1. By mimicking the colour of the environment background, many organisms successfully escape predation 1,2. An efficient camouflage strategy needs two essential and interconnected mechanisms: (i) an accurate sensory machinery to evaluate the environment and (ii) the genetic determination for expressing a phenotypic trait mimicking the environment or/and the capability to modulate the skin colouration to match with the background colour. Countershading, a type of camouflage strategy which consists of the gradation of colour from dark on the dorsal side to light on the ventral area, is generally considered as an efficient hiding strategy spread mainly in the marine environment 1-4. The cryptic strategy aims to facilitate the concealment of the projected shadow by the body adding a clear betterment to the organism's survival 5. This mechanism may be passive, with no colour modification during the organism life, or active, with the ability to gradually modify the skin colour to adapt the background colour (i.e. in terms of dark-grey scale or colour). Skin colour modifications need to be under fine-tuned modulation to display an efficient camouflage. Pathways controlling colour modifications involve the motion of pigmented granule (i.e. aggregation and

Photophore Distribution and Enzymatic Diversity Within the Photogenic Integument of the Cookie-Cutter Shark Isistius brasiliensis (Chondrichthyes: Dalatiidae)

“…In parallel, this study presents the first analysis of the photophore morphology and coverage in I. brasiliensis (and, more generally, in Dalatiidae). As recently observed in other luminous sharks (Claes and Mallefet, 2009;Claes et al, 2015;Duchatelet et al, 2020b;Mallefet et al, 2021), I. brasiliensis photophores, visible as black dots between placoid scales, are mainly distributed within the ventral epidermis with a clear dorso-ventral gradient. Counterillumination (i.e., ventral light emission that mimic the residual downwelling light in terms of intensity, wavelength and angular distribution to avoid being spotted by underneath swimming predators; Clarke, 1963;Johnsen et al, 2004), as an anti-predatory tool, was suggested to be the bioluminescence function for Dalatiidae species (Widder, 1998.…”

Bioluminescence of the Largest Luminous Vertebrate, the Kitefin Shark, Dalatias licha: First Insights and Comparative Aspects

“…For both families, luminescence appears to be dually controlled at the level of (i) the photocyte, site of luminescent reaction, and (ii) the ILS cells, acting as a diaphragm capable of occluding light produced by the photocytes, via melanophore-associated pigment movements (Duchatelet et al, 2020b,d). This was recently demonstrated within ILS cells of the lanternshark, E. spinax (Duchatelet et al, 2020d) i.e., transduction pathways that activate cellular motors such as dynein and kinesin, leading pigment movements within ILS melanophores. The bioluminescence control mechanisms in the two studied etmopterids, as well as in D. licha, might share common features.…”

“…The bioluminescence control mechanisms in the two studied etmopterids, as well as in D. licha, might share common features. Moreover, the involvement of extraocular photoreception events in the light emission control of photophores (Duchatelet et al, 2020d), remains to be deciphered for these sharks. Further research are necessary to fully demonstrate the evolutive conservation of luminescence control within etmopterids and dalatiids.…”

A Third Luminous Shark Family: Confirmation of Luminescence Ability for Zameus squamulosus (Squaliformes; Somniosidae)

“…At the photophore top, facing the outside, an iris‐like structure (ILS) made of interspersed pigmented cells surmounted by lens cells is present (6,7). The ILS serves as a photophore shutter via pigment motions (8,9). Etmopteridae luminescence is produced intrinsically even if the luminous system remains to be discovered (10).…”

“…Comparatively, in Dalatiidae, luminescence is mainly produced ventrally hence the function seems to be only restricted to counterillumination (11); light emission occurs in photophores presenting a unique photocyte and a less dense or absent ILS (12–14). Up to now, all studied luminous sharks present a singular hormonal control of the light emission (8,9).…”