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

Claes, Julien; Delroisse, Jérôme; Grace, Mark A.; Doosey, Michael H.; Duchatelet, Laurent; Mallefet, Jérôme

doi:10.1038/s41598-020-75656-8

Cited by 11 publications

(13 citation statements)

References 46 publications

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“…Blue star indicates the expected origin of luminescence in sharks. [34,74]. Photographs courtesy by D. Perrine (E. bispinatus), T. Raczynski (E. zantedeschia [49]) and J. Mallefet (other species; [36,41,65], Mallefet, unpublished).…”

Section: Luminous Shark Diversitymentioning

confidence: 99%

“…Given the morphological similarity of the pectoral glands, an identical function has been suggested for the pocket sharks, Mollisquama spp. [55,74]. The ocular and frontal photophores of E. spinax [103] and the ventral photophore of D. licha [41] could be used as a vision aid (Figure 3c).…”

Section: Ecology Of Shark Luminescencementioning

confidence: 99%

“…Shark photogenic organs. (a) Photophores (modified from [32,34]); (b) secretory photogenic structures: lightproducing columnar epithelium from pouch of the taillight shark (modified from [34]; left) and putative light-producing cubic tissue from pocket shark's pectoral pockets (modified from [74]; right); (c) histological section of I. brasiliensis photophore; (d) histological section of E. lucifer photophore; (e) ultrastructure of E. spinax photophore; (f) ultrastructure of E. spinax photocyte; (g) autofluorescence from E. lucifer photophore; (h) autofluorescence from photocyte vesicle from E. lucifer; (i) autofluorescence from pocket shark's pocket epithelium. A, apical cells; B, basal cells; Ba, basal lamina; Bs, blood sinus; Ca, cartilage rod from pectoral fin.…”

Section: Photogenic Structures and Specialized Squamation Of Bioluminescent Sharksmentioning

confidence: 99%

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Glow on Sharks: State of the Art on Bioluminescence Research

Duchatelet

Claes

Delroisse

et al. 2021

Oceans

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This review presents a synthesis of shark bioluminescence knowledge. Up to date, bioluminescent sharks are found only in Squaliformes, and specifically in Etmopteridae, Dalatiidae and Somniosidae families. The state-of-the-art knowledge about the evolution, ecological functions, histological structure, the associated squamation and physiological control of the photogenic organs of these elusive deep-sea sharks is presented. Special focus is given to their unique and singular hormonal luminescence control mechanism. In this context, the implication of the photophore-associated extraocular photoreception—which complements the visual adaptations of bioluminescent sharks to perceive residual downwelling light and luminescence in dim light environment—in the hormonally based luminescence control is depicted in detail. Similarities and differences between shark families are highlighted and support the hypothesis of an evolutionary unique ancestral appearance of luminescence in elasmobranchs. Finally, potential areas for future research on shark luminescence are presented.

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Section: Luminous Shark Diversitymentioning

confidence: 99%

Section: Ecology Of Shark Luminescencementioning

confidence: 99%

Section: Photogenic Structures and Specialized Squamation Of Bioluminescent Sharksmentioning

confidence: 99%

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Glow on Sharks: State of the Art on Bioluminescence Research

Duchatelet

Claes

Delroisse

et al. 2021

Oceans

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“…For instance, lanternfish, dragonfish and viperfish luminous systems were demonstrated to use coelenterazine as luciferin, but no luciferase/photoprotein has been identified to date (Tsuji and Haneda, 1971;Mallefet and Shimomura, 1995;Duchatelet et al, 2019). Similarly, shark bioluminescence systems-while these organisms have been extensively studied these last years (e.g., Claes et al, 2020;Mallefet et al, 2021)remain totally enigmatic, even though attempts were made to decipher the bioluminescent compound in the lanternshark Etmopterus spinax (Renwart and Mallefet, 2013). Cross-reactivity with known luciferin failed to trigger light production, and preliminary search for luciferase homologues within the available transcriptomic data did not yield any results suggesting the involvement of an unknown bioluminescent system in luminous sharks (Renwart and Mallefet, 2013;Delroisse et al, 2018Delroisse et al, , 2021.…”

Section: Other Groups Of Luciferases or Photoproteinsmentioning

confidence: 99%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

et al. 2021

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Bioluminescence—i.e., the emission of visible light by living organisms—is defined as a biochemical reaction involving, at least, a luciferin substrate, an oxygen derivative, and a specialised luciferase enzyme. In some cases, the enzyme and the substrate are durably associated and form a photoprotein. While this terminology is educatively useful to explain bioluminescence, it gives a false idea that all luminous organisms are using identical or homologous molecular tools to achieve light emission. As usually observed in biology, reality is more complex. To date, at least 11 different luciferins have indeed been discovered, and several non-homologous luciferases lato sensu have been identified which, all together, confirms that bioluminescence emerged independently multiple times during the evolution of living organisms. While some phylogenetically related organisms may use non-homologous luciferases (e.g., at least four convergent luciferases are found in Pancrustacea), it has also been observed that phylogenetically distant organisms may use homologous luciferases (e.g., parallel evolution observed in some cnidarians, tunicates and echinoderms that are sharing a homologous luciferase-based system). The evolution of luciferases then appears puzzling. The present review takes stock of the diversity of known “bioluminescent proteins,” their evolution and potential evolutionary origins. A total of 134 luciferase and photoprotein sequences have been investigated (from 75 species and 11 phyla), and our analyses identified 12 distinct types—defined as a group of homologous bioluminescent proteins. The literature review indicated that genes coding for luciferases and photoproteins have potentially emerged as new genes or have been co-opted from ancestral non-luciferase/photoprotein genes. In this latter case, the homologous gene’s co-options may occur independently in phylogenetically distant organisms.

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“…For instance, lanternfish, dragonfish and viperfish luminous systems were demonstrated to use coelenterazine as luciferin, but no luciferase/photoprotein has been identified to date (Tsuji and Haneda, 1971;Mallefet and Shimomura, 1995;Duchatelet et al, 2019). Similarly, shark bioluminescence systems -while these organisms have been extensively studied these last years (e.g., Mallefet et al, 2021;Claes et al, 2020) -remain totally enigmatic, even though attempts were made to decipher the bioluminescent compound in the lanternshark Etmopterus spinax (Renwart and Mallefet, 2013). Cross-reactivity with known luciferin failed to trigger light production, and preliminary search for luciferase homologues within the available transcriptomic data did not yield any results suggesting the involvement of an unknown bioluminescent system in luminous sharks (Renwart and Mallefet, 2013;Delroisse et al, 2018;Delroisse et al, 2021).…”

Section: Other Groups Of Luciferases or Photoproteinsmentioning

confidence: 99%

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Delroisse¹,

Duchatelet²,

Flammang³

et al. 2021

Preprint

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Bioluminescence – i.e., the emission of visible light by living organisms - is defined as a biochemical reaction involving, at least, a luciferin substrate, an oxygen derivative, and a specialised luciferase enzyme. In some cases, the enzyme and the substrate are durably associated and form a photoprotein. While this terminology is educatively useful to explain bioluminescence, it gives a false idea that all luminous organisms are using identical or homologous molecular tools to achieve light emission. As usually observed in biology, reality is more complex. To date, 11 different luciferins have indeed been discovered, and several non-homologous luciferases lato sensu have been identified which, all together, confirms that bioluminescence emerged independently multiple times during the evolution of living organisms. While some phylogenetically related organisms may use non-homologous luciferases (e.g., at least four convergent luciferases are found in Pancrustacea), it has also been observed that phylogenetically distant organisms may use homologous luciferases (e.g., parallel evolution observed in some cnidarians, tunicates and echinoderms that are sharing a homologous luciferase-based system). The evolution of luciferases then appears puzzling. The present review takes stock of the diversity of known “bioluminescent proteins”, their evolution and potential evolutionary origins. A total of 134 luciferase and photoprotein sequences have been investigated (from 75 species and 11 phyla), and our analyses identified 12 distinct types – defined as a group of homologous bioluminescent proteins. The literature review indicated that genes coding for luciferases and photoproteins have potentially emerged as new genes or have been co-opted from ancestral non-luciferase/photoprotein genes. In this latter case, the homologous gene’s co-options may occur independently in phylogenetically distant organisms.

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

Cited by 11 publications

References 46 publications

Glow on Sharks: State of the Art on Bioluminescence Research

Glow on Sharks: State of the Art on Bioluminescence Research

Leaving the Dark Side? Insights Into the Evolution of Luciferases

Leaving the Dark Side? Insights Into the Evolution of Luciferases

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