[en] 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.
Coubris, Constance; Marine Biology Laboratory, Earth and Life Institute, UCLouvain, Croix du Sud 3, 1348, Louvain-la-Neuve, Belgium. constance.coubris@uclouvain.be
Duchatelet, Laurent; Marine Biology Laboratory, Earth and Life Institute, UCLouvain, Croix du Sud 3, 1348, Louvain-la-Neuve, Belgium
Delroisse, Jérôme ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Biochimie et biologie moléculaire ; Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, UMONS, 23 Place du Parc, 7000, Mons, Belgium ; Laboratory of Cellular and Molecular Biology, GIGA Institute, 4000, Liège, Belgium
Bayaert, Wendy Shirley; Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, UMONS, 23 Place du Parc, 7000, Mons, Belgium
Parise, Laura; Marine Biology Laboratory, Earth and Life Institute, UCLouvain, Croix du Sud 3, 1348, Louvain-la-Neuve, Belgium
Eloy, Marie Christine; Institut des Sciences de la Vie, UCLouvain, Croix du Sud 4-5, 1348, Louvain-la-Neuve, Belgium
Pels, Christophe; Marine Biology Laboratory, Earth and Life Institute, UCLouvain, Croix du Sud 3, 1348, Louvain-la-Neuve, Belgium
Mallefet, Jérôme; Marine Biology Laboratory, Earth and Life Institute, UCLouvain, Croix du Sud 3, 1348, Louvain-la-Neuve, Belgium
Language :
English
Title :
Maintain the light, long-term seasonal monitoring of luminous capabilities in the brittle star Amphiura filiformis.
The authors acknowledge U. Schwarz, captain of the Alice vessel, and the skillful members of the Kristineberg Center (Goteborg University, Sweden) for their help during the Amphiura filiformis collections. The authors acknowledge Prof. S. Dupont for all the advice and helpful skills during this study. The authors also want to thank T. Wiegand from advanced the mobile lab (TREC- EMBL) for her help in visualizing coelenterazine autofluorescence and immunolabeling in the wild-caught specimens. Acknowledgment also goes to V. Delannay for the constant support during the monitoring experiments. CC is a Ph.D. student under an FRIA fellowship, LD is a postdoctoral researcher funded by a PDR project from FNRS (BiolumExtraPho \u2013 40021304), JD is a postdoctoral researcher funded by a PDR project from FNRS (Protectobiome in sea cucumbers\u201440013965), WSB is a Ph.D. student under an FRIA fellowship, LP is a Master student at UCLouvain, MCE is IMABIOL platform microscopy technician from the LIBST Institute, CP is Earth and Life Institute technician and JM is a research associate FRS-FNRS. This study is the contribution of BRC 417 of the Biodiversity Research Center (UCLouvain) from the Earth and Life Institute Biodiversity (ELIV) and the \u201CCentre Interuniversitaire de Biologie Marine\u201D (CIBIM).This work was supported by a FRIA grant (40014530) awarded to CC and an FRS-FNRS grant (T.0169.20) awarded to the Universit\u00E9 de Louvain\u2014UCLouvain Marine Biology Laboratory and the Universit\u00E9 de Mons Biology of Marine Organisms and Biomimetics Laboratory. The research that led to these results also received funding from the European program No 231, the ASSEMBLE Plus project.
O. Shimomura Bioluminescence: Chemical Principles and Methods 2012 World Scientific, Singapore Hackensack, NJ 10.1142/8239
E.S. Lau T.H. Oakley Multi-level convergence of complex traits and the evolution of bioluminescence Biol. Rev. 2021 96 673 691 10.1111/brv.12672 33306257
Z.M. Kaskova A.S. Tsarkova I.V. Yampolsky 1001 lights: Luciferins, luciferases, their mechanisms of action and applications in chemical analysis, biology and medicine Chem. Soc. Rev. 2016 45 6048 6077 1:CAS:528:DC%2BC28XhsV2hu77P 10.1039/C6CS00296J 27711774
J. Delroisse L. Duchatelet P. Flammang J. Mallefet Leaving the dark side? Insights into the evolution of luciferases Front. Mar. Sci. 2021 8 673620 10.3389/fmars.2021.673620
M. Bessho-Uehara W.R. Francis S.H.D. Haddock Biochemical characterization of diverse deep-sea anthozoan bioluminescence systems Mar. Biol. 2020 167 114 1:CAS:528:DC%2BB3cXhtlKqu7bL 10.1007/s00227-020-03706-w
V.R. Viviani et al. A new brilliantly blue-emitting luciferin-luciferase system from Orfelia fultoni and Keroplatinae (Diptera) Sci. Rep. 2020 10 9608 2020NatSR.10.9608V 1:CAS:528:DC%2BB3cXhtF2lsrvK 10.1038/s41598-020-66286-1 32541805 7295969
C. Fajardo et al. New insights on expression and purification of a recombinant luciferase protein from the bioluminescence marine dinoflagellate Pyrocystis lunula Lat. Am. J. Aquat. Res. 2023 51 610 616 10.3856/vol51-issue4-fulltext-2898
O. Shimomura S. Daunert S.K. Deo The Photoproteins Photoproteins in Bioanalysis 2006 Wiley 1 23
A.S. Tsarkova Luciferins under construction: A review of known biosynthetic pathways Front. Ecol. Evol. 2021 9 667829 10.3389/fevo.2021.667829
A.A. Kotlobay et al. Bioluminescence chemistry of fireworm Odontosyllis Proc. Natl. Acad. Sci. U.S.A. 2019 116 18911 18916 2019PNAS.11618911K 1:CAS:528:DC%2BC1MXhvVSkurfL 10.1073/pnas.1902095116 31462497 6754589
J. Mallefet L. Duchatelet C. Coubris Bioluminescence induction in the ophiuroid Amphiura filiformis (Echinodermata) J. Exp. Biol. 2020 223 4 jeb218719 10.1242/jeb.218719 31974222
E.A. Widder Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity Science 2010 328 704 708 2010Sci..328.704W 1:CAS:528:DC%2BB3MXovVKksLs%3D 10.1126/science.abb5352 20448176
Duchatelet, L. et al. Coelenterazine detection in five myctophid species from the Kerguelen Plateau. in The Kerguelen Plateau: Marine Ecosystem + Fisheries: Proceedings of the Second Symposium (2019).
S. Inoue H. Taguchi M. Murata H. Kakoi T. Goto Squid bioluminescence IV. Isolation and structural elucidation of Watasenia dehydropreluciferin Chem. Lett. 1977 159 259 262 10.1246/cl.1977.259
J.A. Warner J.F. Case The zoogeography and dietary induction of bioluminescence in the midshipman fish Porichthys notatus Biol. Bull. 1980 159 231 246 10.2307/1541021
M. Bessho-Uehara et al. Kleptoprotein bioluminescence: Parapriacanthus fish obtain luciferase from ostracod prey Sci. Adv. 2020 6 eaax4942 2020SciA..6.4942B 1:CAS:528:DC%2BB3cXitFGgsLrL 10.1126/sciadv.aax4942 31934625 6949039
T.M. Frank E.A. Widder M.I. Latz J.F. Case Dietary maintenance of bioluminescence in a deep-sea mysid J. Exp. Biol. 1984 109 385 389 10.1242/jeb.109.1.385
S.H.D. Haddock T.J. Rivers B.H. Robison Can coelenterates make coelenterazine? Dietary requirement for luciferin in cnidarian bioluminescence Proc. Natl. Acad. Sci. U.S.A. 2001 98 11148 11151 2001PNAS..9811148H 1:CAS:528:DC%2BD3MXnt1yqsbY%3D 10.1073/pnas.201329798 11572972 58698
R. Rosenberg L. Lundberg Photoperiodic activity pattern in the brittle star Amphiura filiformis Mar. Biol. 2004 145 651 656 10.1007/s00227-004-1365-z
J. Delroisse et al. A puzzling homology: a brittle star using a putative cnidarian-type luciferase for bioluminescence Open Biol. 2017 7 160300 1:CAS:528:DC%2BC1cXpsleqsr8%3D 10.1098/rsob.160300 28381628 5413902
S. Delval J. Mallefet Proximal to distal gradient of luminescence in the arm of Amphiura filiformis Echinodermata-Ophiuroidea 2010 CRC Press
Y. Dewael J. Mallefet Luminescence in ophiuroids (Echinodermata) does not share a common nervous control in all species J. Exp. Biol. 2002 205 799 806 1:STN:280:DC%2BD387ot1WjsQ%3D%3D 10.1242/jeb.205.6.799 11914388
J. Delroisse et al. Fine structure of the luminous spines and luciferase detection in the brittle star Amphiura filiformis Zool. Anz. 2017 269 1 12 10.1016/j.jcz.2017.05.001
L.-O. Loo P. Jonsson M. Sköld Ö. Karlsson Passive suspension feeding in Amphiura filiformis (Echinodermata: Ophiuroidea): feeding behaviour in flume flow and potential feeding rate of field populations Mar. Ecol. Prog. Ser. 1996 139 143 155 1996MEPS.139.143L 10.3354/meps139143
L.-O. Loo R. Rosenberg Production and energy budget in marine suspension feeding populations: Mytilus edulis, Cerastoderma edule, Mya arenaria and Amphiura filiformis J. Sea Res. 1996 35 199 207 1996JSR..35.199L 10.1016/S1385-1101(96)90747-9
O. Lindahl L. Hernroth Phyto-Zooplankton community in coastal waters of western Sweden -An ecosystem off balance? Mar. Ecol. Prog. Ser. 1983 10 119 126 1983MEPS..10.119L 10.3354/meps010119
S. Dupont M.C. Thorndyke Growth or differentiation? Adaptive regeneration in the brittlestar Amphiura filiformis J. Exp. Biol. 2006 209 3873 3881 10.1242/jeb.02445 16985203
H.F. Dietrich A.R. Fontaine A decalcification method for ultrastructure of echinoderm tissues Stain Technol. 1975 50 351 354 1:STN:280:DyaE287gsFCjtw%3D%3D 10.3109/10520297509117086 813335
K.C. Richardson L. Jarett E.H. Finke Embedding in epoxy resins for ultrathin sectioning in electron microscopy Stain Technol. 1960 35 313 323 1:STN:280:DyaF3c%2FmtV2rsA%3D%3D 10.3109/10520296009114754 13741297
O. Shimomura Presence of coelenterazine in non-bioluminescent marine organisms Comp. Biochem. Physiol. B 1987 86 361 363 10.1016/0305-0491(87)90306-3
O. Shimomura S. Inoue F.H. Johnson Y. Haneda Widespread occurrence of coelenterazine in marine bioluminescence Comp. Biochem. Physiol. B 1980 65 435 437 10.1016/0305-0491(80)90044-9
M. Bessho-Uehara et al. Evidence for de novo biosynthesis of the luminous substrate coelenterazine in ctenophores Iscience 2020 23 101859 2020iSci..23j1859B 1:CAS:528:DC%2BB3MXhtV2lurnJ 10.1016/j.isci.2020.101859 33376974 7756133
Y. Oba S. Kato M. Ojika S. Inouye Biosynthesis of coelenterazine in the deep-sea copepod Metridia pacifica Biochem. Biophys. Res. Commun. 2009 390 684 688 1:CAS:528:DC%2BD1MXhsVKgtbvE 10.1016/j.bbrc.2009.10.028 19833098
M. Maar et al. Trophodynamic function of copepods, appendicularians and protozooplankton in the late summer zooplankton community in the Skagerrak Mar. Biol. 2004 144 917 933 10.1007/s00227-003-1263-9
C. Vargas et al. Importance of copepods versus appendicularians in vertical carbon fluxes in a Swedish fjord Mar. Ecol. Prog. Ser. 2002 241 125 138 2002MEPS.241.125V 10.3354/meps241125
M. Kuse H. Kiyota Marine bioluminescence with dehydrocoelenterazine, an imidazopyrazinone compound Marine natural Products 2021 Topics in heterocyclic chemistry Springer 85 103
S. Inouye M. Nakamura T. Hosoya Enzymatic conversion of dehydrocoelenterazine to coelenterazine using FMN-bound flavin reductase of NAD (P) H: FMN oxidoreductase Biochem. Biophys. Res. Commun. 2022 587 24 28 1:CAS:528:DC%2BB3MXis1KmsbzE 10.1016/j.bbrc.2021.11.089 34864391
G. Tzertzinis et al. Coelenterazine sulfotransferase from Renilla muelleri PLoS ONE 2022 17 e0276315 1:CAS:528:DC%2BB38XislSjt7rO 10.1371/journal.pone.0276315 36251663 9576082
C. Coubris L. Duchatelet S. Dupont J. Mallefet A brittle star is born: Ontogeny of luminous capabilities in Amphiura filiformis PLoS ONE 2024 19 e0298185 1:CAS:528:DC%2BB2cXmvVSgt7c%3D 10.1371/journal.pone.0298185 38466680 10927081
D. Deheyn J. Mallefet M. Jangoux Evidence of seasonal variation in bioluminescence of Amphipholis squamata (Ophiuroidea, Echinodermata): effects of environmental factors J. Exp. Mar. Biol. Ecol. 2000 245 245 264 1:STN:280:DC%2BC2sbhsFarug%3D%3D 10.1016/S0022-0981(99)00166-5 10699213
B. Czeczuga Comparative studies of carotenoids in the fauna of the Gullmar Fjord (Bohuslan, Sweden) III Echinodermata. Hydrobiologia 1977 53 271 275 1:CAS:528:DyaE2sXkvVWmsro%3D 10.1007/BF00818549
G. Britton G. Britton S. Liaaen-Jensen H. Pfander Functions of intact carotenoids Carotenoids Natural functions 2008 Springer 189 212
C. Calestani G.M. Wessel M. Kloc J. Kubiak These colors don’t run: regulation of pigment—biosynthesis in Echinoderms Marine Organisms as Model Systems in Biology and Medicine 2018 Results and problems in cell differentiation Springer 515 525 10.1007/978-3-319-92486-1_22
L. Duchatelet J.M. Claes J. Delroisse P. Flammang J. Mallefet Glow on sharks: state of the art on bioluminescence research Oceans 2021 2 4 822 842 10.3390/oceans2040047
P.J. Herring The comparative morphology of hepatic photophores in decapod Crustacea J. Mar. Biol. Assoc. U.K. 1981 61 723 737 10.1017/S0025315400048165
P.J. Herring N.A. Locket The luminescence and photophores of euphausiid crustaceans J. Zool. 1978 186 431 462 10.1111/j.1469-7998.1978.tb03932.x