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

Abstract

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.

Glow on Sharks: State of the Art on Bioluminescence Research

“…Nevertheless, Z. squamulosus is the only somniosid shark known to possess photophores (Figure 1; Table S1). In parallel, luminescence has been observed in live in 15 species only, however, covering most clades, i.e., the blurred smooth lanternshark, Etmopterus bigelowi [40]; the southern lanternshark, Etmopterus granulosus [41]; the blackbelly lanternshark, Etmopterus lucifer [41]; the slendertail lanternshark, Etmopterus molleri [42,43]; the smooth lanternshark, Etmopterus pusillus [44]; E. spinax [45,46]; the splendid lanternshark, Etmopterus splendidus [47]; the green lanternshark, Etmopterus virens [40]; the smalleye pygmy shark, Squaliolus aliae [43,48]; the kitefin shark, Dalatias licha [41]; the taillight shark, Euprotomicroides zantedeschia [49]; the pygmy shark, Euprotomicrus bispina-tus [50]; the cookiecutter shark, Isistius brasiliensis [51,52]; Z. squamulosus [36]; the viper dogfish, Trigonognathus kabeyai (Mallefet, unpublished data); Figures 1 and 2; Table S1. In addition, expected luminous species are encountered in Etmopteridae and Dalatiidae, based on the presence of photophore structures and/or flank marks in the holotype description [33,35,36,38,[40][41][42][43][44][45][46][47][48][49]; Table S1.…”

“…The second most widespread and well-supported function of shark luminescence is intraspecific communication. Although Dalatiidae and Somniosidae present "simple" luminescent patterns where photophores follow a dorsoventral density gradient [33,34,36,41,52] (Figures 2 and 3), etmopterid sharks display complex luminescent photophore aggregations on the ventral area, but also on the flanks, the fins, the tail, around the eyes, the spiracles, the gills, and the epidermal tissue surrounding dorsal spines [34,[104][105][106]111] (Figures 2 and 3). Since these patterns are species-specific and do not show sexual dimorphism (except photophores associated with primary sexual characters, e.g., male claspers, as explained below [112]), they are often used as taxonomic determination tools [34,54,63,68].…”

“…Shark photophores are small, reaching a maximum diameter of ~50, ~100, and ~200 µm for Somniosidae, Dalatiidae, and Etmopteridae, respectively [34,36,41,48,52,65,76]. Comparatively, the photophores of bony fishes can reach up to 1 cm [119].…”

Leaving the Dark Side? Insights Into the Evolution of Luciferases

“…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.…”

Leaving the Dark Side? Insights Into the Evolution of Luciferases

“…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).…”