Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark photophores

Duchatelet, Laurent; Claes, Julien; Mallefet, Jérôme

doi:10.1007/s00227-019-3473-9

Cited by 17 publications

(21 citation statements)

References 33 publications

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“…Conversely, our results also highlighted the implication of an α-MSH/ACTH pathway involving kinesin to regulate the ILS cell pigment dispersion. www.nature.com/scientificreports www.nature.com/scientificreports/ Based on previous pilot studies revealing an abundant and singular presence of Es-Opn3 within the photogenic ventral skin tissue 77,78 , the opsin absorbance spectrum was measured and revealed a blue-green absorption wavelength: between 410 and 490 nm, with a maximum value of 445 nm. This result is consistent with recent studies that have determined and characterized photoreceptive properties for several vertebrate Opn3 homologs (Table 1) such as fishes 88 or other vertebrates 88,89 .…”

Section: Discussionmentioning

confidence: 99%

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

Duchatelet

Sugihara

Delroisse

et al. 2020

Sci Rep

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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

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Section: Discussionmentioning

confidence: 99%

“…Opn3 absorbance measurement. Recent studies highlight the presence of an opsin 3 colocalized with E. spinax photophores 77,78 . Following this research, the opsin 3 mRNA sequence was in silico extracted from the transcriptome, and cDNA was created.…”

Section: Methodsmentioning

confidence: 99%

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

Duchatelet

Sugihara

Delroisse

et al. 2020

Sci Rep

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“…Surprisingly, however, the stratified cubic and putatively holocrine epithelium of the pocket shark pockets appears dramatically different from the pseudostratified columnar and putatively apocrine (based on morphology) epithelium of the pelvic photogenic pouch of the Taillight Shark 5 , suggesting an independent origin of the two organs in these closely related species. Reaching close to 10 μm in diameter, apical cells of the villiform structures reach a similar size as photocytes of juvenile dalatiid ( Squaliolus aliae ; J. M. Claes, personal observation) and etmopterid sharks ( Etmopterus spinax ) 34 . In the Slendertail Lantern Shark ( Etmopterus molleri ), photophores are known to form enlarged photogenic structure at the base of the dorsal fin 35 .…”

Section: Discussionmentioning

confidence: 86%

Histological evidence for secretory bioluminescence from pectoral pockets of the American Pocket Shark (Mollisquama mississippiensis)

Claes

Delroisse

Grace

et al. 2020

Sci Rep

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The function of pocket shark pectoral pockets has puzzled scientists over decades. Here, we show that the pockets of the American Pocket Shark (Mollisquama mississippiensis) contain a brightly fluorescent stratified cubic epithelium enclosed in a pigmented sheath and in close contact with the basal cartilage of the pectoral fins; cells of this epithelium display a centripetal gradient in size and a centrifuge gradient in fluorescence. These results strongly support the idea that pocket shark’s pockets are exocrine holocrine glands capable of discharging a bioluminescent fluid, potentially upon a given movement of the pectoral fin. Such capability has been reported in many other marine organisms and is typically used as a close-range defensive trick. In situ observations would be required to confirm this hypothesis.

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“…We consider that Etmopterus lantern sharks obtained coelenterazine for bioluminescence from fishes and crustaceans diets; they also obtained coelenterazine from their diets, such as copepods. In E. spinax , in vivo luminescence from ventral photophores was also detected in the late embryonic stage 27 , suggesting that coelenterazine is transferred vertically from the mother.…”

Section: Discussionmentioning

confidence: 97%

Etmopteruslantern sharks use coelenterazine as the substrate for their luciferin-luciferase bioluminescence system

Mizuno

Yano

Paitio

et al. 2021

Preprint

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The lantern shark, Etmopterus, are a group of deep-sea bioluminescent species. They emit blue light mainly from ventral body surface, and the major biological function is considered to be a counterillumination. In this study, we detected both coelenterazine and coelenterazine-specific luciferase activity in the ventral photophore tissue. These results suggested that the lantern shark use coelenterazine as a substrate for the luciferin-luciferase reaction of their bioluminescence.

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Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark photophores

Cited by 17 publications

References 33 publications

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

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

Histological evidence for secretory bioluminescence from pectoral pockets of the American Pocket Shark (Mollisquama mississippiensis)

Etmopteruslantern sharks use coelenterazine as the substrate for their luciferin-luciferase bioluminescence system

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