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New record of bioluminescence in Odontosyllis cf. australiensis (Annelida: Syllidae: Eusyllinae) in Japan

Published online by Cambridge University Press:  07 January 2022

Genki Kobayashi Open the ORCID record for Genki Kobayashi [Opens in a new window]  and
Tatsuya Sakamoto Open the ORCID record for Tatsuya Sakamoto [Opens in a new window]
Genki Kobayashi*
Affiliation:
Seto Marine Biological Laboratory, Field Science Education and Research Center, Kyoto University, 459 Shirahama, Nishimuro, Wakayama649-2211, Japan
Tatsuya Sakamoto
Affiliation:
Fisheries Resources Institute, Japan Fisheries Research and Education Agency, 1551-8, Tairamachi, Nagasaki, Nagasaki 851-2213, Japan
*
Author for correspondence: Genki Kobayashi, E-mail: genkikobayashi5884@gmail.com
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Abstract

Bioluminescence is widespread in the marine environment. The bioluminescence of some species of the fireworm Odontosyllis (Annelida: Syllidae: Eusyllinae) has been well studied, although the presence or absence of bioluminescence in most species of this genus is yet to be revealed. The bioluminescent worms were observed after sunset around the new moon day in July and October 2020 and in July to October 2021 in Nagasaki Prefecture, Japan. Molecular phylogenetic analysis based on two mitochondrial and one nuclear gene sequence showed that the worms were closely related to Odontosyllis australiensis, but the partial 16S rRNA gene sequences differed by 2% between those of the Japanese and Australian material. Because only epitokes, i.e. morphologically modified sexually mature worms, were collected, further studies on morphological characters of atokes would be required in the future. We therefore tentatively refer to them as Odontosyllis cf. australiensis. Molecular phylogenetic analysis also showed that known bioluminescent Odontosyllis species belong to various lineages.

Keywords

Annelidsfirewormmolecular phylogenypolychaetes
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 6 , September 2021 , pp. 919 - 925
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Aguado, MT, Nygren, A and Siddall, ME (2007) Phylogeny of syllidae (Polychaeta) based on combined molecular analysis of nuclear and mitochondrial genes. Cladistics 23, 552–564.Google ScholarPubMed
Aguado, MT, San Martín, G and Siddall, ME (2012) Systematics and evolution of syllids (Annelida, Syllidae). Cladistics 28, 234–250.CrossRefGoogle Scholar
Aguado, MT, Capa, M, Lago-Barcia, D, Gil, J, Pleijel, F and Nygren, A (2019) Species delimitation in Amblyosyllis (Annelida, Syllidae). PLoS ONE 14, e0214211.CrossRefGoogle Scholar
Álvarez-Campos, P, Giribet, G and Riesgo, A (2017) The Syllis gracilis species complex: a molecular approach to a difficult taxonomic problem (Annelida, Syllidae). Molecular Phylogenetics and Evolution 109, 138–150.CrossRefGoogle Scholar
Audino, JA, Serb, JM and Marian, JEAR (2020) Hard to get, easy to lose: evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia). Evolution 74, 2105–2120.CrossRefGoogle Scholar
Bassot, J (1979) Sites actifs et facilitation dans trois systèmes bioluminescents. Archives de zoologie expérimentale et générale 120, 5–24.Google Scholar
Berkeley, E (1935) Swarming of Odontosyllis phosphorea, Moore, and of other polychæta near Nanaimo, BC. Nature 136, 1029.CrossRefGoogle Scholar
Brugler, MR, Aguado, MT, Tessler, M and Siddall, ME (2018) The transcriptome of the Bermuda fireworm Odontosyllis enopla (Annelida: Syllidae): a unique luciferase gene family and putative epitoky-related genes. PLoS ONE 13, e0200944.CrossRefGoogle ScholarPubMed
Capa, M and Hutchings, P (2021) Annelid diversity: historical overview and future perspectives. Diversity 13, 129.CrossRefGoogle Scholar
Daly, JM (1975) Reversible epitoky in the life history of the polychaete Odontosyllis polycera (Schmarda 1861). Journal of the Marine Biological Association of the United Kingdom 55, 327–344.CrossRefGoogle Scholar
Deheyn, DD and Latz, MI (2009) Internal and secreted bioluminescence of the marine polychaete Odontosyllis phosphorea (Syllidae). Invertebrate Biology 128, 31–45.CrossRefGoogle Scholar
Deheyn, D, Mallefet, J and Jangoux, M (2000) Expression of bioluminescence in Amphipholis squamata (Ophiuroidea: Echinodermata) in presence of various organisms: a laboratory study. Journal of the Marine Biological Association of the United Kingdom 80, 179–180.CrossRefGoogle Scholar
Erdman, DS (1965) Lunar periodicity in the swarming of luminescent worms, Odontosyllis octodentata Treadwell (Annelida) off La Parguera, PR. Caribbean Journal of Science 5, 103–107.Google Scholar
Fischer, A and Fischer, U (1995) On the life-style and life-cycle of the luminescent polychaete Odontosyllis enopla (Annelida: Polychaeta). Invertebrate Biology 114, 236–247.CrossRefGoogle Scholar
Folmer, O, Black, M, Hoeh, W, Lutz, R and Vrijenhoek, R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google ScholarPubMed
Fraser, CM (1915) The swarming of Odontosyllis. Proceedings and Transactions of the Royal Society of Canada, Ser 3, 43–49.Google Scholar
Galloway, TW and Welch, PS (1911) Studies on a phosphorescent Bermudan annelid, Odontosyllis enopla Verrill. Transactions of the American Microscopical Society 30, 13–39.CrossRefGoogle Scholar
Gaston, GR and Hall, J (2000) Lunar periodicity and bioluminescence of swarming Odontosyllis luminosa (Polychaeta: Syllidae) in Belize. Gulf and Caribbean Research 12, 47–51.CrossRefGoogle Scholar
Haddock, SHD, Moline, MA and Case, JF (2010) Bioluminescence in the sea. Annual Review of Marine Science 2, 443–493.CrossRefGoogle Scholar
Haneda, Y (1971) Luminous swimming Polychaeta from the Banda Islands. Science Report of the Yokosuka City Museum 18, 1–2.Google Scholar
Hartmann-Schröder, G (1981) Die polychaeten der tropisch-subtropischen westküste australiens (zwischen Exmouth im Norden und Cervantes im Süden). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 78, 19–96.Google Scholar
Horii, N (1982) Observation on luminous polychaeta, Odontosyllis undecimdonta from Toyama Bay, Japan Sea. Science Report of the Yokosuka City Museum 29, 1–3.Google Scholar
Huntsman, AG (1948) Odontosyllis at Bermuda and lunar periodicity. Journal of the Fisheries Research Board of Canada 7b, 363–369.CrossRefGoogle Scholar
Imajima, M (1996) Polychaeta. Tokyo: Seibutsu Kenkyusha.Google Scholar
Inoue, S, Okada, K, Tanino, H, Kakoi, H and Horii, N (1990) 6-Propionyllumazines from the marine polychaete, Odontosyllis undecimdonta. Chemistry Letters 19, 367–368.CrossRefGoogle Scholar
Inoue, S, Okada, K, Tanino, H, Kakoi, H, Ohnishi, Y and Horii, N (1991) New lumazines from the marine polychaete, Odontosyllis undecimdonta. Chemistry Letters 20, 563–564.CrossRefGoogle Scholar
Inoue, S, Okada, K, Tanino, H and Kakoi, H (1993) A new hexagonal cyclic enol phosphate of 6-β-Hydroxypropionyllumazines from the marine swimming polychaete, Odontosyllis undecimdonta. Heterocycles 35, 147–150.CrossRefGoogle Scholar
Jones, BW and Nishiguchi, MK (2004) Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Marine Biology 144, 1151–1155.CrossRefGoogle Scholar
Kakoi, H, Tanino, H, Okada, K and Inoue, S (1995) 6-Acyllumazines from the Marine polychaete, Odontosyllis undecimdonta. Heterocycles 41, 789–797.CrossRefGoogle Scholar
Katoh, K, Rozewicki, J and Yamada, KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20, 1160–1166.CrossRefGoogle Scholar
Kobayashi, G, Goto, R, Takano, T and Kojima, S (2018) Molecular phylogeny of Maldanidae (Annelida): multiple losses of tube-capping plates and evolutionary shifts in habitat depth. Molecular Phylogenetics and Evolution 127, 332–344.CrossRefGoogle ScholarPubMed
Kobayashi, G, Itoh, H, Fukuda, H and Kojima, S (2021) The complete mitochondrial genome of the sand bubbler crab Scopimera globosa and its phylogenetic position. Genomics 113, 831–839.CrossRefGoogle ScholarPubMed
Kotlobay, AA, Dubinnyi, MA, Purtov, KV, Guglya, EB, Rodionova, NS, Petushkov, VN, Bolt, YV, Kublitski, VS, Kaskova, ZM, Ziganshin, RH, Nelyubina, YV, Dorovatovskii, PV, Eliseev, IE, Branchini, BR, Bourenkov, G, Ivanov, IA, Oba, Y, Yampolsky, IV and Tsarkova, AS (2019) Bioluminescence chemistry of fireworm Odontosyllis. Proceedings of the National Academy of Sciences USA 116, 18911–18916.CrossRefGoogle ScholarPubMed
Lanfear, R, Frandsen, PB, Wright, AM, Senfeld, T and Calcott, B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.Google ScholarPubMed
Latz, MI (1995) Physiological mechanisms in the control of bioluminescent countershading in a midwater shrimp. Marine and Freshwater Behaviour and Physiology 26, 207–218.CrossRefGoogle Scholar
Lau, ES and Oakley, TH (2021) Multi-level convergence of complex traits and the evolution of bioluminescence. Biological Review 96, 673–691.CrossRefGoogle ScholarPubMed
Lewis, SM and Cratsley, CK (2007) Flash signal evolution, mate choice, and predation in fireflies. Annual Review of Entomology 53, 293–321.CrossRefGoogle Scholar
Markert, RE, Markert, BJ and Vertrees, NJ (1961) Lunar periodicity in spawning and luminescence in Odontosyllis enopla. Ecology 42, 414–415.CrossRefGoogle Scholar
Martin, D, Aguado, MT, Fernández Álamo, MA, Britayev, TA, Böggemann, M, Capa, M, Faulwetter, S, Fukuda, MV, Helm, C, Petti, MA, Ravara, A and Teixeira, MAL (2021) On the diversity of Phyllodocida (Annelida: Errantia), with a focus on Glyceridae, Goniadidae, Nephtyidae, Polynoidae, Sphaerodoridae, Syllidae, and the holoplanktonic families. Diversity 13, 131.CrossRefGoogle Scholar
McCloskey, M, Schell, J, Sandland, GJ and Gerrish, GA (2017) Luminescent syllid (Odontosyllis spp.) courtship display densities vary across marine habitats around South Water Caye, Belize. Gulf and Caribbean Research 28, 40–45.CrossRefGoogle Scholar
Morin, JG and Bermingham, EL (1980) Bioluminescent patterns in a tropical ostracod. American Zoologist 20, 851.Google Scholar
Morin, JG and Cohen, AC (2010) It's all about sex: bioluminescent courtship displays, morphological variation and sexual selection in two New Genera of Caribbean ostracodes. Journal of Crustacean Biology 30, 56–67.CrossRefGoogle Scholar
Nakamura, K, Kano, Y, Suzuki, N, Namatame, T and Kosaku, A (2007) 18S rRNA phylogeny of sea spiders with emphasis on the position of Rhynchothoracidae. Marine Biology 153, 213–223.CrossRefGoogle Scholar
Nguyen, LT, Schmidt, HA, von Haeseler, A and Minh, BQ (2014) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.CrossRefGoogle ScholarPubMed
Palumbi, SR (1996) Nucleic acids II: the polymerase chain reaction. In Hillis, DM, Moritz, C and Mable, BK (eds), Molecular Systematics. Sunderland, MA: Sinauer Associates, pp. 205–247.Google Scholar
Potts, FA (1913) The swarming of Odontosyllis. Proceedings of the Cambridge Philosophical Society, Mathematical and Physical Sciences 17, 193–200.Google Scholar
Prentiss, NK (2020) Nocturnally swarming Caribbean polychaetes of St. John, U.S. Virgin Islands, USA. Zoosymposia 19, 91–102.CrossRefGoogle Scholar
Ramesh, CH, Mohanraju, R, Karthick, P and Murthy, KN (2017) Distribution of bioluminescent polychaete larvae of Odontosyllis sp. in South Andaman. Indian Journal of Geo-Marine Sciences 46, 735–737.Google Scholar
Rivers, TJ and Morin, JG (2008) Complex sexual courtship displays by luminescent male marine ostracods. Journal of Experimental Biology 211, 2252–2262.CrossRefGoogle ScholarPubMed
Rivers, TJ and Morin, JG (2009) Plasticity of male mating behaviour in a marine bioluminescent ostracod in both time and space. Animal Behaviour 78, 723–734.CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England) 19, 1572–1574.CrossRefGoogle ScholarPubMed
San Martín, G (1990) Eusyllinae (Syllidae, Polychaeta) from Cuba and Gulf of Mexico. Bulletin of Marine Science 46, 590–619.Google Scholar
San Martín, G and Hutchings, P (2006) Eusyllinae (Polychaeta: Syllidae) from Australia with the description of a new genus and fifteen new species. Records of the Australian Museum 58, 257–370.CrossRefGoogle Scholar
Schultz, DT, Kotlobay, AA, Ziganshin, R, Bannikov, A, Markina, NM, Chepurnyh, TV, Shakhova, ES, Palkina, K, Haddock, SHD, Yampolsky, IV and Oba, Y (2018) Luciferase of the Japanese syllid polychaete Odontosyllis umdecimdonta. Biochemical and Biophysical Research Communications 502, 318–323.CrossRefGoogle Scholar
Shimomura, O, Johnson, FH and Saiga, Y (1963) Partial purification and properties of the Odontosyllis luminescence system. Journal of Cellular and Comparative Physiology 61, 275–292.CrossRefGoogle Scholar
Steiner, G and Dreyer, H (2003) Molecular phylogeny of Scaphopoda (Mollusca) inferred from 18S rDNA sequences: support for a Scaphopoda-Cephalopoda clade. Zoologica Scripta 32, 343–356.CrossRefGoogle Scholar
Tanino, H, Takakura, H, Kakoi, H, Okada, K and Inoue, S (1994) (S)-6-(1-Hydroxypropyl)lumazine derivatives from the marine polychaete, Odontosyllis undecimdonta. Heterocycles 38, 971–974.CrossRefGoogle Scholar
Tanino, H, Takakura, H, Kakoi, H, Okada, K and Inoue, S (1996) (S)-2-Methyl-1,5-bis(1,3-dimethyl-6-lumazinyl)-1,5-pentanedione from the marine polychaete, Odontosyllis undecimdonta. Heterocycles 42, 125–128.Google Scholar
Tsuji, FI and Hill, E (1983) Repetitive cycles of bioluminescence and spawning in the polychaete, Odontosyllis phosphorea. Biological Bulletin 165, 444–449.CrossRefGoogle ScholarPubMed
Van Lummel, L (1932) Over lichtende wormpjes in de baai van bataria. De Tropische Natuur 21, 85–87.Google Scholar
Verdes, A and Gruber, DF (2017) Glowing worms: biological, chemical, and functional diversity of bioluminescent annelids. Integrative and Comparative Biology 57, 18–32.CrossRefGoogle ScholarPubMed
Verdes, A, Alvarez-Campos, P, Nygren, A, Martin, GS, Rouse, G, Deheyn, DD, Gruber, DF and Holford, M (2018) Molecular phylogeny of Odontosyllis (Annelida, Syllidae): a recent and rapid radiation of marine bioluminescent worms. BioRxiv, 241570. https://www.biorxiv.org/content/10.1101/241570v1.Google Scholar
von der Heyden, S, Lipinski, MR and Matthee, CA (2010) Remarkably low mtDNA control region diversity in an abundant demersal fish. Molecular Phylogenetics and Evolution 55, 1183–1188.CrossRefGoogle Scholar
White, TJ, Bruns, T, Lee, S and Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols: A Guide to Methods and Applications. Cambridge, MA: Academic Press, pp. 315–322.Google Scholar
Widder, EA (2001) Marine bioluminescence: why do so many animals in the open ocean make light? Bioscience Explain 1, 1–9.Google Scholar
Wilkens, LA and Wolken, JJ (1981) Electroretinograms from Odontosyllis enopla (Polychaeta; Syllidae): initial observations on the visual system of the bioluminescent fireworm of Bermuda. Marine Behaviour and Physiology 8, 55–66.CrossRefGoogle Scholar
Wolken, JJ and Florida, RG (1984) The eye structure of the bioluminescent fireworm of Bermuda, Odontosyllis enopla. Biological Bulletin 166, 260–268.CrossRefGoogle Scholar
Zörner, SA and Fischer, A (2007) The spatial pattern of bioluminescent flashes in the polychaete Eusyllis blomstrandi (Annelida). Helgoland Marine Research 61, 55–66.CrossRefGoogle Scholar

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