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Sci Rep
2024 Dec 30;141:31803. doi: 10.1038/s41598-024-82811-y.
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Availability and occurrence of coelenterazine in a Swedish fjord to maintain Amphiura filiformis bioluminescence.
Coubris C
,
Mirzaei K
,
Duchatelet L
,
Mallefet J
.
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The bioluminescent European brittle star Amphiura filiformis produces blue light at the arm-spine level thanks to a biochemical reaction involving coelenterazine as substrate and a Renilla-like luciferase as an enzyme. This echinoderm light production depends on a trophic acquisition of the coelenterazine substrate. Without an exogenous supply of coelenterazine, this species loses its luminous capabilities. Moreover, this species was recently shown not to produce coelenterazine storage forms. As an infaunal suspensive feeder, A. filiformis is assumed to find enough substrate to maintain its bioluminescence capabilities efficiently. To date, no studies have investigated the putative source of coelenterazine in the brittle star diet. A combined analysis using listing based on visual observations and metabarcoding on the planktonic communities highlights planktonic species known as light emitters using coelenterazine. Besides, the A. filiformis stomach content was analyzed seasonally via metabarcoding technique, and coelenterazine-related preys were underlined. Results provide evidence of the presence of preys containing coelenterazine in the fjord environment and within the stomach content of the ophiuroid throughout the year. The results are consistent with the demonstration of the trophic acquisition of luminous capabilities in A. filiformis and give a new step by underlying the constant presence of coelenterazine suppliers throughout the year for the luminescence reaction occurring within this species.
Fig. 1. Bioluminescence of the brittle star Amphiura filiformis. (a) Bright light, and (b) bioluminescent pictures of A. filiformis. (c) Schematic illustration of the bioluminescence reaction occurring in A. filiformis in which coelenterazine is oxidized via the enzymatic activity of a luciferase homologous to the Renilla luciferase19,20 to form the oxyluciferin in an excited state. Going down to a stable state, the oxyluciferin (i.e., coelenteramide) releases photons and carbon dioxide8,9. Scale bars: 0.5 cm.
Fig. 2. Seasonal luminometric measurements on the plankton mixture collected in the Gullmarsfjord (a) coelenterazine content, and (b) luciferase activity. (c) Principal component analysis (PCA) showing correlations between luminometric measurements. Different lettering indicates statistical differences. Error bars correspond to s.e.m.
Fig. 3. Zooplankton and phytoplankton percent frequency of occurrence in the Gullmarsfjord evaluated seasonally on the online plankton list (https://sharkweb.smhi.se/hamta-data/). Percent frequency of occurrence over the seasons of (a) the total phyto- and zooplankton, (b) luminous genus only, (c) retrieved phytoplankton luminous, and (d) retrieved zooplankton luminous genera.
Fig. 4. Zooplankton percent frequency of occurrence in the Gullmarsfjord. Zooplanktonic communities evaluated on (a–c) the plankton list available online (https://sharkweb.smhi.se/hamta-data/) and through (d–f) metabarcoding method using COI and 18 S sequences. Percent frequency of occurrence over the year of (a,d) zooplankton, (b,e) luminous genus only and (c,f) luminous genus using coelenterazine only.
Fig. 5. Analysis of Amphiura filiformis stomach content. (a) Percent frequency of occurrence in the stomach content DNA samples across all seasons; bold species name indicates the luminous status, and asterisk signifies the use of coelenterazine for light production. (b–d) Time-lapse pictures of cannibalism behavior observed in A. filiformis; interval time of 2 min between each picture. (e) Picture showing arms extending in the water column to catch suspended materials. G: gonad, M: mouth, sp: spine. Scale bar: 0.5 cm.
