Bioluminescence induction in the ophiuroid Amphiura filiformis (Echinodermata).

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 coelenterazine-supplemented food. The present work demonstrates for the first time a trophic acquisition of coelenterazine in A. filiformis to maintain light emission capabilities.

A brittle star is born: Ontogeny of luminous capabilities in Amphiura filiformis.

Bioluminescence is the production of visible light by living organisms thanks to a chemical reaction, implying the oxidation of a substrate called luciferin catalyzed by an enzyme, the luciferase. The luminous brittle star Amphiura filiformis depends on coelenterazine (i.e., the most widespread luciferin in marine ecosystems) and a luciferase homologous to the cnidarian Renilla luciferase to produce blue flashes in the arm's spine. Only a few studies have focused on the ontogenic apparitions of bioluminescence in marine organisms. Like most ophiuroids, A. filiformis displays planktonic ophiopluteus larvae for which the ability to produce light was not investigated. This study aims to document the apparition of the luminous capabilities of this species during its ontogenic development, from the egg to settlement. Through biochemical assays, pharmacological stimulation, and Renilla-like luciferase immunohistological detection across different developing stages, we pointed out the emergence of the luminous capabilities after the ophiopluteus larval metamorphosis into a juvenile. In conclusion, we demonstrated that the larval pelagic stage of A. filiformis is not bioluminescent compared to juveniles and adults.

Systematic Distribution of Bioluminescence in Marine Animals: A Species-Level Inventory.

Bioluminescence is the production of visible light by an organism. This phenomenon is particularly widespread in marine animals, especially in the deep sea. While the luminescent status of numerous marine animals has been recently clarified thanks to advancements in deep-sea exploration technologies and phylogenetics, that of others has become more obscure due to dramatic changes in systematics (themselves triggered by molecular phylogenies). Here, we combined a comprehensive literature review with unpublished data to establish a catalogue of marine luminescent animals. Inventoried animals were identified to species level in over 97% of the cases and were associated with a score reflecting the robustness of their luminescence record. While luminescence capability has been established in 695 genera of marine animals, luminescence reports from 99 additional genera need further confirmation. Altogether, these luminescent and potentially luminescent genera encompass 9405 species, of which 2781 are luminescent, 136 are potentially luminescent (e.g., suggested luminescence in those species needs further confirmation), 99 are non-luminescent, and 6389 have an unknown luminescent status. Comparative analyses reveal new insights into the occurrence of luminescence among marine animal groups and highlight promising research areas. This work will provide a solid foundation for future studies related to the field of marine bioluminescence.

Maintain the light, long-term seasonal monitoring of luminous capabilities in the brittle star Amphiura filiformis.

The European brittle star Amphiura filiformis emits blue light, via a Renilla-like luciferase, which depends on the dietary acquisition of coelenterazine. Questions remain regarding luciferin availability across seasons and the persistence of luminous capabilities after a single boost of coelenterazine. To date, no study has explored the seasonal, long-term monitoring of these luminous capabilities or the tracking of luciferase expression in photogenic tissues. Through multidisciplinary analysis, we demonstrate that luminous capabilities evolve according to the exogenous acquisition of coelenterazine throughout adult life. Moreover, no coelenterazine storage forms are detected within the arms tissues. Luciferase expression persists throughout the seasons, and coelenterazine's presence in the brittle star diet is the only limiting factor for the bioluminescent reaction. No seasonal variation is observed, involving a continuous presence of prey containing coelenterazine. The ultrastructure description provides a morphological context to investigate the green autofluorescence signal attributed to coelenterazine during luciferin acquisition. Finally, histological analyses support the hypothesis of a pigmented sheath leading light to the tip of the spine. These insights improve our understanding of the bioluminescence phenomenon in this burrowing brittle star.

Catecholamine Involvement in the Bioluminescence Control of Two Species of Anthozoans.

Bioluminescence, the ability of living organisms to emit visible light, is an important ecological feature for many marine species. To fulfil the ecological role (defence, offence, or communication), bioluminescence needs to be finely controlled. While many benthic anthozoans are luminous, the physiological control of light emission has only been investigated in the sea pansy, Renilla koellikeri. Through pharmacological investigations, a nervous catecholaminergic bioluminescence control was demonstrated for the common sea pen, Pennatula phosphorea, and the tall sea pen, Funiculina quadrangularis. Results highlight the involvement of adrenaline as the main neuroeffector triggering clusters of luminescent flashes. While noradrenaline and octopamine elicit flashes in P. phosphorea, these two biogenic amines do not trigger significant light production in F. quadrangularis. All these neurotransmitters act on both the endodermal photocytes located at the base and crown of autozooids and specific chambers of water-pumping siphonozooids. Combined with previous data on R. koellikeri, our results suggest that a catecholaminergic control mechanisms of bioluminescence may be conserved in Anthozoans.

Red and white muscle proportions and enzyme activities in mesopelagic sharks.

In the last decade, there has been an increase in the study of the ecology of deep-sea organisms. One way to understand an organism's ecology is the study of its metabolism. According to literature, deep-sea sharks possess a lower anaerobic enzyme activity than their shallow-water counterparts, but no difference has been observed regarding their aerobic enzyme activities. These studies have suggested deep-sea sharks should be slow and listless swimmers. However, other studies based on video observations have revealed differences in cruise swimming speed between different species. The present study examined muscles of squaliform sharks, including both luminous and non-luminous species. We combined measurements of the relative amounts of red and white muscle with assays of enzymes that are used as markers for aerobic (citrate synthase, malate dehydrogenase) and anaerobic (lactate dehydrogenase) metabolism, searching for a relationship with cruising speeds. Non-luminous deep-sea species displayed lower aerobic enzyme activities but similar anaerobic enzyme activities than the benthic shallow-water counterpart (Squalus acanthias). Conversely, luminous Etmopteridae species were found to have similar aerobic enzyme activities to S. acanthias but displayed lower anaerobic enzyme activities. Analyses revealed that red muscle proportion and aerobic enzyme activities were positively related to the cruise swimming speed. In contrast, Dalatias licha, which swims at the slowest cruise swimming speed ever recorded, presented a very low aerobic metabolic phenotype (lower aerobic marker enzymes and less red muscle). Finally, the values obtained for white muscle proportion and anaerobic metabolic phenotype suggested a high burst capacity for D. licha and non-luminous sharks.