Bioluminescence has often been seen as a spectacular yet uncommon event at sea but considering the vastness of the deep sea and the occurrence of luminous organisms in this zone, it is now more and more obvious that producing light at depth must play an important role structuring the biggest ecosystem on our planet. Three species of deepwater sharks (Dalatias licha, Etmopterus lucifer, and Etmopterus granulosus) were collected from the Chatham Rise, off New Zealand, and for the first time, we documented their luminescence. Comparison of glowing shark pictures, combined with histological description of light organs and hormonal control analysis, highlight the evolutive conservation of the bioluminescence process within Dalatiidae and Etmopteridae. A special emphasis is placed on the luminescence of D. licha, the largest known luminous vertebrate. This first experimental study of three luminous shark species from New Zealand provides an insight into the diversity of shark bioluminescence and highlights the need for more research to help understand these unusual deep-sea inhabitants: the glowing sharks.

Among Etmopteridae and Dalatiidae, luminous species use hormonal control to regulate bioluminescence. Melatonin (MT) triggers light emission and, conversely, alpha melanocyte‐stimulating hormone (α‐MSH) actively reduces ongoing luminescence. Prolactin (PRL) acts differentially, triggering light emission in Etmopteridae and inhibiting it in Dalatiidae. Interestingly, these hormones are also known as regulators of skin pigment movements in vertebrates. One other hormone, the adrenocorticotropic hormone (ACTH), also members of the skin pigmentation regulators, is here pharmacologically tested on the light emission. Results show that ACTH inhibits luminescence in both families. Moreover, as MT and α‐MSH/ACTH receptors are members of the G‐protein coupled receptor (GPCR) family, we investigated the effect of hormonal treatments on the cAMP level of photophores through specific cAMP assays. Our results highlight the involvement of ACTH and cAMP in the control of light emission in sharks and suggest a functional similarity between skin pigment migration and luminescence control, this latter being mediated by pigment movements in the light organ‐associated iris‐like structure cells.

No abstract

The velvet belly lanternshark (Etmopterus spinax) is a small deep-sea shark commonly found in the Eastern Atlantic and the Mediterranean Sea. This bioluminescent species is able to emit a blue-green ventral glow used in counter-illumination camouflage, mainly. In this study, paired-end Illumina HiSeqTM technology has been employed to generate transcriptome data from eye and ventral skin tissues of the lanternshark. About 64 and 49 million Illumina reads were generated from skin and eye tissues respectively. The assembly allowed us to predict 119,749 total unigenes including 94,569 for the skin transcriptome and 94,365 for the eye transcriptome while 74,753 were commonly found in both transcriptomes. A taxonomy filtering was applied to extract a reference transcriptome containing 104,390 unigenes among which 38,836 showed significant similarities to known sequences in NCBI non-redundant protein sequences database. Around 58% of the annotated unigenes match with predicted genes from the Elephant shark (Callorhinchus milii) genome. The transcriptome completeness has been evaluated by successfully capturing around 98% of orthologous genes of the « Core eukaryotic gene dataset » within the E. spinax reference transcriptome. We identified potential “light-interacting toolkit” genes including multiple genes related to ocular and extraocular light perception processes such as opsins, phototransduction actors or crystallins. Comparative gene expression analysis reveals eye-specific expression of opsins, ciliary phototransduction actors, crystallins and vertebrate retinoid pathway actors. In particular, mRNAs from a single rhodopsin gene and its potentially associated peropsin were detected in the eye transcriptome, only, confirming a monochromatic vision of the lanternshark. Encephalopsin mRNAs were mainly detected in the ventral skin transcriptome. In parallel, immunolocalization of the encephalopsin within the ventral skin of the shark suggests a functional relation with the photophores, i.e. epidermal light-producing organs. We hypothesize that extraocular photoreception might be involved in the bioluminescence control possibly acting on the shutter opening and/or the photocyte activity itself. The newly generated reference transcriptome provides a valuable resource for further understanding of the shark biology.

Since recently, shark’s bioluminescence has been recorded from two Squaliformes families, the Etmopteridae and Dalatiidae. Pictures of luminescence, light organ morphologies and physiology of the luminous control have been described for species of the Etmopteridae and Dalatiidae families. In 2015, a third luminous family, Somniosidae, was assumed to present a bioluminescent species, Zameus squamulosus. Up to now, confirmation of the luminous abilities of Z. squamulosus is lacking. Here, the luminescence of Z. squamulosus was in vivo recorded for the first time confirming the bioluminescence status of the third luminescent shark family. Additionally, photophore histology revealed the conservation of the light organ morphology across the luminous Squaliformes. Light transmittance analysis through the placoid scale added information on the luminescence efficiency and highlighted a new type of bioluminescent‐like squamation. All these data reinforced the likelihood that the common ancestor of Dalatiidae, Etmopteridae and Somniosidae may already have been luminescent for counterillumination purpose.

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

Background In the darkness of the ocean, an impressive number of taxa have evolved the capability to emit light. Many mesopelagic organisms emit a dim ventral glow that matches with the residual environmental light in order to camouflage themselves (counterillumination function). Sharks use their luminescence mainly for this purpose. Specific lateral marks have been observed in Etmopteridae sharks (one of the two known luminous shark families) suggesting an inter/intraspecific recognition. Conversely, dorsal luminescence patterns are rare within these deep-sea organisms. Results Here we report evidence that Etmopterus spinax, Etmopterus molleri and Etmopterus splendidus have dorsal luminescence patterns. These dorsal patterns consist of specific lines of luminous organs, called photophores, on the rostrum, dorsal area and at periphery of the spine. This dorsal light seems to be in contrast with the counterilluminating role of ventral photophores. However, skin photophores surrounding the defensive dorsal spines show a precise pattern supporting an aposematism function for this bioluminescence. Using in situ imaging, morphological and histological analysis, we reconstructed the dorsal light emission pattern on these species, with an emphasis on the photogenic skin associated with the spine. Analyses of video footage validated, for the first time, the defensive function of the dorsal spines. Finally, we did not find evidence that Etmopteridae possess venomous spine-associated glands, present in Squalidae and Heterondontidae, via MRI and CT scans. Conclusion This work highlights for the first time a species-specific luminous dorsal pattern in three deep-sea lanternsharks. We suggest an aposematic use of luminescence to reveal the presence of the dorsal spines. Despite the absence of venom apparatus, the defensive use of spines is documented for the first time in situ by video recordings. Electronic supplementary material The online version of this article (10.1186/s40851-019-0126-2) contains supplementary material, which is available to authorized users.

Bioluminescence is a widespread phenomenon in the marine environment. Among luminous substrates, coelenterazine is the most widespread luciferin, found in eight phyla. The wide phylogenetic coverage of this light-emitting molecule has led to the hypothesis of its dietary acquisition, which has so far been demonstrated in one cnidarian and one lophogastrid shrimp species. Within Ophiuroidea, the dominant class of luminous echinoderms, Amphiura filiformis is a model species known to use coelenterazine as substrate of a luciferin/luciferase luminous system. The aim of this study was to perform long-term monitoring of A. filiformis luminescent capabilities during captivity. Our results show (i) depletion of luminescent capabilities within 5 months when the ophiuroid was fed a coelenterazine-free diet and (ii) a quick recovery of luminescent capabilities when the ophiuroid was fed coelenterazinesupplemented food. The present work demonstrates for the first time a trophic acquisition of coelenterazine in A. filiformis to maintain light emission capabilities.