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Jérôme Mallefet - One of the best experts on this subject based on the ideXlab platform.
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Photophore distribution and enzymatic diversity within the photogenic integument of the cookie cutter shark isistius brasiliensis chondrichthyes dalatiidae
Frontiers in Marine Science, 2021Co-Authors: Jérôme Delroisse, Laurent Duchatelet, Patrick Flammang, Jérôme MallefetAbstract:The cookie-cutter shark Isistius brasiliensis (Squaliformes: Dalatiidae) is a deep-sea species that emits a blue luminescence ventrally, except at the level of a black band beneath the jaw. This study aims to investigate the distribution and histology of the light-emitting organs along the shark body, describe the tissue-specific transcriptomes of the non-photogenic and photogenic ventral integument, describe the repertoire of enzyme-coding transcripts expressed in the two integument regions, and analyse the potential expression of transcripts coding for luciferase-like enzymes (i.e., close homologues of known luciferases involved in the bioluminescence of other organisms). Our analyses confirm the black band’s non-photogenic status and Photophore absence within this region. The sub-rostral area is the region where the Photophore density is the highest. In parallel, paired-end Illumina sequencing has been used to generate pilot transcriptomes, from the black band and the ventral integument tissues of one individual. In total, 68,943 predicted unigenes have been obtained (i.e., 64,606 for the black band transcriptome, 43,996 for the ventral integument transcriptome) with 43,473 unigenes showing significant similarities to known sequences from public databases. BLAST search analyses of known luciferases, coupled with comparative predicted gene expression (i.e., photogenic, non-photogenic), support the hypothesis that the species uses an unknown luciferase system. An enzymatic repertoire was predicted based on the PRIAM database, and Enzyme Commission numbers were assigned for all detected enzyme-coding unigenes. These transcriptomes based on a single specimen, and the predicted enzyme repertoire, constitute a valuable resource for future investigations on the biology of this enigmatic luminous shark.
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Etmopteridae bioluminescence: dorsal pattern specificity and aposematic use
Zoological Letters, 2019Co-Authors: Laurent Duchatelet, Nicolas Pinte, Taketeru Tomita, Keiichi Sato, Jérôme MallefetAbstract: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.
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The lanternshark Etmopterus spinax.
2018Co-Authors: Jérôme Delroisse, Laurent Duchatelet, Patrick Flammang, Jérôme MallefetAbstract:A-B, E: lateral views of the shark (2018 Shark Trust, www.sharktrust.org). B: lateral bioluminescence emission pattern. C: ventral and dorsal views of the shark. D: ventral bioluminescence emission pattern. F: Eye of the shark. G: histological section through the shark retina. H, J: histological sections through the shark skin. I: in vivo observation of ventral skin Photophores, K: Schematic reconstruction of a Photophore (modified from [95, 96]). Annotations: C: connective tissue, CTI: cellular type I, CTII: cellular type II, D: denticle, L: lens, G: ganglionic layer, E: epidermis, INL: inner nuclear layer, Ir: iris, ONL: outer nuclear layer, P: pigmented layer, Ph: photocyte, PS: pigmented shield, RL: reticulated layer.
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Encephalopsin immunodetection in E. spinax.
2018Co-Authors: Jérôme Delroisse, Laurent Duchatelet, Patrick Flammang, Jérôme MallefetAbstract:A. photosensitive film of immunoblotting performed on the protein extract of E. spinax ventral and dorsal skin as well as retina with an antibodies directed against extraocular opsin: anti-encephalopsin PAb from Genetex, GTX 70609, lot number 821 400 929, 1/2000. 50 μg of total protein were used in each well. B. Cryosection immunofluorescence directed against extraocular opsins in different tissues of the lanternshark, E. spinax. Visualization of a Photophore paraffin section (A). Visualization of the labelling on cryosections of a ventral skin section with Photophores (B), a section of the retina (C). The B and C sections were given the primary antibody GTX (primary antibody: anti-encephalopsin PAb from Genetex, GTX 70609, lot number 821 400 929, 1/50). The secondary antibody was coupled with a red fluorochrome (Alexa Fluor 594 Goat Anti-Rabbit IgG (H+L) Antibody, highly cross-adsorbed (A-11037), 1/300 from Life Technologies Limited). C, conjunctive tissue; E, epidermis; Ir: iris-like structure related pigmented cell; L, lens cell; Ph: photocyte; Ps: pigmented sheath; D: dermal denticle; R: rod, C: cone layer. Scale bar: 50 μm.
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iso luminance counterillumination drove bioluminescent shark radiation
Scientific Reports, 2015Co-Authors: Julien M. Claes, Nicolas Straube, Daneric Nilsson, Shaun P Collin, Jérôme MallefetAbstract:Counterilluminating animals use ventral photogenic organs (Photophores) to mimic the residual downwelling light and cloak their silhouette from upward-looking predators. To cope with variable conditions of pelagic light environments they typically adjust their luminescence intensity. Here, we found evidence that bioluminescent sharks instead emit a constant light output and move up and down in the water column to remain cryptic at iso-luminance depth. We observed, across 21 globally distributed shark species, a correlation between capture depth and the proportion of a ventral area occupied by Photophores. This information further allowed us, using visual modelling, to provide an adaptive explanation for shark Photophore pattern diversity: in species facing moderate predation risk from below, counterilluminating Photophores were partially co-opted for bioluminescent signalling, leading to complex patterns. In addition to increase our understanding of pelagic ecosystems our study emphasizes the importance of bioluminescence as a speciation driver.
Mallefet Jérôme - One of the best experts on this subject based on the ideXlab platform.
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Photophore Distribution and Enzymatic Diversity Within the Photogenic Integument of the Cookie-Cutter Shark Isistius brasiliensis (Chondrichthyes: Dalatiidae)
'Frontiers Media SA', 2021Co-Authors: Delroisse Jérôme, Duchatelet Laurent, Flammang Patrick, Mallefet JérômeAbstract:The cookie-cutter shark Isistius brasiliensis (Squaliformes: Dalatiidae) is a deep-sea species that emits a blue luminescence ventrally, except at the level of a black band located beneath the jaw. This study aims to (i) investigate the distribution and histology of the Photophores (i.e., light-emitting organs) along the shark body, (ii) describe the tissue-specific transcriptomes of the black band integument region (i.e., non-photogenic) and the ventral integument region (i.e., photogenic), (iii) describe the repertoire of enzyme-coding transcripts expressed the two integument regions, and (iv) analyze the potential expression of transcripts coding for luciferase-like enzymes (i.e., close homologs of known luciferases involved in the bioluminescence of other organisms). Our analyses confirm the black band’s non-photogenic status and Photophore absence within this region. The sub-rostral area is the region where the Photophore density is the highest. In parallel, paired-end Illumina sequencing has been used to generate two pilot transcriptomes, from the black band and the ventral integument tissues of one individual. In total, 68,943 predicted unigenes have been obtained (i.e., 64,606 for the black band transcriptome, 43,996 for the ventral integument transcriptome) with 43,473 unigenes showing significant similarities to known sequences from public databases. BLAST search analyses of known luciferases, coupled with comparative predicted gene expression (i.e., photogenic versus non-photogenic), support the hypothesis that the species uses an unknown luciferase system. An enzymatic repertoire was predicted based on the PRIAM database, and Enzyme Commission numbers were assigned for all detected enzyme-coding unigenes. These pilot transcriptomes based on a single specimen, and the predicted enzyme repertoire, constitute a valuable resource for future investigations on the biology of this enigmatic luminous shark
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From extraocular photoreception to pigment movement regulation: a new control mechanism of the lanternshark luminescence
'Springer Science and Business Media LLC', 2020Co-Authors: Duchatelet Laurent, Delroisse Jérôme, Sugihara Tomohiro, Koyanagi Mitsumasa, Rezsohazy René, Terakita Akihisa, Mallefet JérômeAbstract: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
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Bioluminescence in lanternsharks: Insight from hormone receptor localization
Academic Press, 2020Co-Authors: Duchatelet Laurent, Delroisse Jérôme, Mallefet JérômeAbstract:As part of the study of their bioluminescence, the deep-sea lanternshark Etmopterus spinax and Etmopterus molleri (Chondrichthyes, Etmopteridae) received growing interest over the past ten years. These mesopelagic sharks produce light thanks to a finely tuned hormonal control involving melatonin, adrenocorticotropic hormone and α-melanocyte-stimulating hormone. Receptors of these hormones, respectively the melatonin receptors and the melanocortin receptors, are all members of the G-protein coupled receptor family i.e. coupled with specific G proteins involved in the preliminary steps of their transduction pathways. The present study highlights the specific localization of the hormonal receptors, as well as of their associated G-proteins within the light organs, the so-called Photophores, in E. spinax and E. molleri through immunohistofluorescence technic. Our results allow gaining insight into the molecular actors and mechanisms involved in the control of the light emission in Etmopterid sharks
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Luminescence control of Stomiidae Photophores
Urban und Fischer Verlag, 2019Co-Authors: Mallefet Jérôme, Duchatelet Laurent, Hermans Claire, Baguet FernandAbstract:Nervous control of light emission from deep-sea mesopelagic fishes has been documented for several species. Studies on the nervous control of Photophores from deep-sea luminescent fish, are mainly restricted to a pharmacological approach. For example, the light organs, called Photophores, isolated from Argyropelecus hemygimnus and Maurolicus muelleri show a much higher sensitivity to adrenaline than to noradrenaline. According to these results and other information in different species, catecholamines are considered as main neurotransmitters triggering bioluminescence in deep-sea fishes. The present work is a study of the nervous control of the isolated Photophores from two Stomiid fishes, Chauliodus sloani (the viperfish) and Stomias boa (the dragonfish) with the aim to determine the nature of the nervous control by pharmacological, biochemical and morphological approaches. Results show that, although the Photophores of both species are sensitive to catecholamines, adrenaline is present in larger amount than noradrenaline in the light organs of C. sloani. Both catecholamines have different immunoreactive (IR) sites, noradrenaline showing a very diffuse localization as compared to adrenaline in C. sloani. On the contrary, only adrenaline is detected in the photocytes chamber and nerves innervating the Photophore in S. boa. Knowing that the majority of dragonfishes exhibit a luminescent chin barbel, we also investigated the presence of catecholamines in this specific tissue in S. boa. Immunohistology reveals the presence of adrenaline within the tissue forming the chin barbel; adrenaline–IR is found in the connective tissue surroundings two group of muscle fibers and blood vessels in the stem but also around the multiple blood vessels located within the barbel bulb. Our results strongly support the adrenergic control of light emission in bioluminescent stomiid fishes
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Embryonic expression of encephalopsin supports bioluminescence perception in lanternshark Photophores
'Springer Science and Business Media LLC', 2019Co-Authors: Duchatelet Laurent, Claes Julien, Mallefet JérômeAbstract:Counterilluminating animals produce a ventral light to hide their silhouette in the water column. This midwater camouflage technique requires a fine and dynamic control of the wavelength, angular distribution, and intensity of their luminescence, which needs to continuously match ambient downwelling light. Recently, extraocular opsins have been suggested to play a role in the bioluminescence control of several organisms, such as squids, comb jellies, or brittle stars, providing a way for photogenic structures to perceive their own light output. By analysing a growing embryonic series of the velvet belly lanternshark, Etmopterus spinax, we show that the development of lanternshark luminescence competence is associated with the expression of encephalopsin within epidermal cells and in the light-regulating structure of the photogenic organs. Such an intra-uterine expression of encephalopsin strongly supports this blue-sensitive extraocular opsin to allow bioluminescence perception in lanternshark Photophores and suggests a clear physiological interaction between photoemission and photoperception
Roger Villanueva - One of the best experts on this subject based on the ideXlab platform.
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towards the identification of the ommastrephid squid paralarvae mollusca cephalopoda morphological description of three species and a key to the north east atlantic species
Zoological Journal of the Linnean Society, 2016Co-Authors: Fernando Angel Fernandezalvarez, Catarina P P Martins, Erica A G Vidal, Roger VillanuevaAbstract:Oceanic squids of the family Ommastrephidae are an important fishing resource worldwide. Although cumulative knowledge exists on their subadult and adult forms, little is known about their young stages. Their hatchlings are among the smaller cephalopod paralarvae. They are characterized by the fusion of their tentacles into a proboscis and are very difficult to identify to species level, especially in areas where more than one species coexist. Seven species are found in the north-east (NE) Atlantic. In this study, mature oocytes of Illex coindetii, Todarodes sagittatus and Todaropsis eblanae were fertilized in vitro to obtain and describe hatchlings. Full descriptions based on morphometric characters, chromatophore patterns, skin sculpture and the structure of proboscis suckers are provided based on live specimens. This information was combined with previous descriptions of paralarvae, not necessarily based on DNA or known parentage, from four other ommastrephid species distributed in the same area and a dichotomous key was developed for the identification of paralarvae of the NE Atlantic. The most useful taxonomic characters were: the relative size of the lateral and medial suckers of the proboscis, the presence/absence of Photophores and the arrangement of pegs on the proboscis suckers. This key was successfully used to identify wild collected rhynchoteuthion paralarvae from the NE Atlantic. Reliable identification of wild paralarvae can foster a better understanding of the population dynamics and life cycles of ommastrephid squids.
Erica A G Vidal - One of the best experts on this subject based on the ideXlab platform.
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towards the identification of the ommastrephid squid paralarvae mollusca cephalopoda morphological description of three species and a key to the north east atlantic species
Zoological Journal of the Linnean Society, 2016Co-Authors: Fernando Angel Fernandezalvarez, Catarina P P Martins, Erica A G Vidal, Roger VillanuevaAbstract:Oceanic squids of the family Ommastrephidae are an important fishing resource worldwide. Although cumulative knowledge exists on their subadult and adult forms, little is known about their young stages. Their hatchlings are among the smaller cephalopod paralarvae. They are characterized by the fusion of their tentacles into a proboscis and are very difficult to identify to species level, especially in areas where more than one species coexist. Seven species are found in the north-east (NE) Atlantic. In this study, mature oocytes of Illex coindetii, Todarodes sagittatus and Todaropsis eblanae were fertilized in vitro to obtain and describe hatchlings. Full descriptions based on morphometric characters, chromatophore patterns, skin sculpture and the structure of proboscis suckers are provided based on live specimens. This information was combined with previous descriptions of paralarvae, not necessarily based on DNA or known parentage, from four other ommastrephid species distributed in the same area and a dichotomous key was developed for the identification of paralarvae of the NE Atlantic. The most useful taxonomic characters were: the relative size of the lateral and medial suckers of the proboscis, the presence/absence of Photophores and the arrangement of pegs on the proboscis suckers. This key was successfully used to identify wild collected rhynchoteuthion paralarvae from the NE Atlantic. Reliable identification of wild paralarvae can foster a better understanding of the population dynamics and life cycles of ommastrephid squids.
P J Herring - One of the best experts on this subject based on the ideXlab platform.
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the Photophore morphology of selenoteuthis scintillans voss and other lycoteuthids cephalopoda lycoteuthidae
Journal of Zoology, 2009Co-Authors: P J Herring, P N Dilly, Celia CopeAbstract:Females and juveniles of Selenoteuthis scintillans have Photophores of several structural types, distributed on the tentacles and eyeballs, and within the mantle cavity and tail. Three distinct Photophore types can be recognized on the basis of their accessory structures, though their photocytes are identical. The tail and some tentacular Photophores (Type 1) lack any accessory optical structures; other tentacular and abdominal Photophores (Type 2) have collagenous diffusing fibres; the anal and ocular Photophores (Type 3) have a variety of iridosomes but no collagen. The distal tentacular organ is a double structure composed of a unit each of Type 1 and Type 2. Ocular Photophores 1 and 5 are also double structures, composed of two Type 3 units. The Photophores closely resemble in structure those of Lycoteuthis diadema. The photocytes have a marked fluorescence and luminesce on treatment with dilute hydrogen peroxide. The bio-luminescence intensity of the tail organ may be modified by chromatophore movements and has a blue-green spectral emission. The Photophores of juvenile Lampadioteuthis megaleia are similar in structure to those of Selenoteuthis but somewhat less complex. A comparison between the morphology of the Photophores of lycoteuthid and enoploteuthid squids emphasizes the close similarity between the two families. At the ultrastructural level, certain Photophores of both families have very characteristic microvillous blood vessels associated with the photocytes.
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species abundance sexual encounter and bioluminescent signalling in the deep sea
Philosophical Transactions of the Royal Society B, 2000Co-Authors: P J HerringAbstract:The problems faced by deep-sea animals in achieving sexual and other encounters require sensory and effector systems the synergy of which can span the often very substantial distances that separate individuals. Bioluminescent systems provide one of the links between individuals, and the sexual dimorphism of some Photophores suggests that they are employed to attract a mate. However, nearest-neighbour values for many deep-sea animals put them beyond the effective range of bioluminescent signals and it is therefore likely that these signals are employed at intermediate ranges, once an initial contact (perhaps olfactory) has been made.
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different types of Photophore in the oceanic squids octopoteuthis and taningia cephalopoda octopoteuthidae
Journal of Zoology, 1992Co-Authors: P J Herring, P N Dilly, Celia CopeAbstract:The oceanic squid Octopoteuthis danue Joubin has one type of Photophore on the head, body and arms, but another type on the eight arm tips. The first type has acomplexcapillary network, with elastic walls and a thick reflector. The arm tip organs have no such capillary core but a dense matrix containing paracrystalline assemblies. Taningia danae Joubin (the only other genus in the family Octopoteuthidae) has only two large arm tip Photophores. These are similar in their general organization to the arm tip Photophores of Octopoteuthis, but their detailed structure is quite different. There has evidently been independent evolution of Photophores in this family of squids.