Phylogeny and Synonymy of Gyrodinium heterostriatum comb. nov. (Dinophyceae), a Common Unarmored Dinoflagellate in the World Oceans

• Authors: Fernando Gómez , Luis Felipe Artigas , Rebecca J. Gast

Abstracts

EN

The North Sea and the English Channel are regions with a long tradition of plankton studies, where the colony-forming haptophyte Phaeocystis globosa dominates the spring phytoplankton blooms. Among its predators, we investigated an abundant unarmored dinoflagellate (~3000 cells per liter) in the North Sea in May 2019. It has been reported in the literature as Gymnodinium heterostriatum or G. striatissimum, and often identified as Gyrodinium spirale. Phylogenetic analyses using the small-, large subunit- and Internal Transcriber Spacers of the ribosomal RNA (SSU-, LSU-, ITS rRNA) gene sequences indicate that our isolates clustered within the Gyrodinium clade. The new sequences formed a sister group with sequences of the freshwater taxon Gyrodinium helveticum, being one of the infrequent marine-freshwater transitions in the microbial world. This isolate is the first characterized member of a clade of numerous environmental sequences widely distributed from cold to tropical seas. This common and abundant taxon has received several names due to its morphological plasticity (changes of size and shape, often deformed after engulfing prey) and the difficulty in discerning surface striation. We conclude that the priority is for the species name Gymnodinium heterostriatum Kofoid & Swezy 1921, a new name that was proposed for Gymnodinium spirale var. obtusum sensu Dogiel 1906. The species Gyrodinium striatissimum (Hulburt 1957) Gert Hansen & Moestrup 2000 and Gymnodinium lucidum D. Ballantine in Parke & Dixon 1964 (=G. hyalinum M. Lebour 1925) are posterior synonyms. We propose Gyrodinium heterostriatum comb. nov. for Gymnodinium heterostriatum.

Keywords

EN

Dinophyta; Gymnodinium; new combination; taxonomy; molecular phylogenetics; North Atlantic

• Publisher: Uniwersytet Jagielloński. Wydawnictwo Uniwersytetu Jagiellońskiego
• Journal: Acta Protozoologica
• Year: 2020
• Volume: 59
• Issue: 2
• Pages: 77-98

Dates

published

2020

Contributors

author

Fernando Gómez

• Carmen Campos Panisse 3, Puerto de Santa María, Spain
• Université du Littoral Côte d’Opale, Université de Lille, CNRS UMR 8187 LOG, Laboratoire d’Océanologie et de Géosciences, Wimereux, France

author

Luis Felipe Artigas

• Université du Littoral Côte d’Opale, Université de Lille, CNRS UMR 8187 LOG, Laboratoire d’Océanologie et de Géosciences, Wimereux, France

author

Rebecca J. Gast

• Woods Hole Oceanographic Institution, Woods Hole, USA

References

• Annenkova N. V., Belykh O. I., Denikina N. N., Belikov S. I. (2009) Identification of dinoflagellates from the Lake Baikal on the basis of molecular genetic data. Dokl. Biol. Sci. 426: 253–256
• Annenkova N. V. (2018) Identification of Lake Baikal plankton dinoflagellates from the genera Gyrodinium and Gymnodinium using single-cell PCR. Russ. J. Genet. 54: 1302–1313
• Christaki U., Genitsaris S., Monchy S., Li L. L., Rachik S., Breton E., Sime-Ngando T. (2017) Parasitic eukaryotes in a mesoeutrophic coastal system with marked Phaeocystis globose blooms. Front. Mar. Sci. 4: 416
• Elbrächter M. (1975) Taxonomical notes on North Sea dinoflagellates I. Kiel. Meeresforsch. 31: 58–64
• Elbrächter M. (1979) On the taxonomy of unarmoured dinophytes (Dinophyta) from the Northwest African upwelling region. “Meteor” Forsch.-Ergebnisse Reihe D 30: 1–22
• Elbrächter M. (1994) Redescription of Gymnodinium heterostriatum Kofoid and Swezy 1921 (Dinophyceae). Helgoländer Meeresunters. 48: 359–364
• Elbrächter M., Hoppenrath M. (2009) Dinoflagellates. In: Marine phytoplankton: selected microphytoplankton species from the North Sea around Helgoland and Sylt, (Eds. M. Hoppenrath, M. Elbrächter, G. Drebes), Kleine Senckenberg-Reihe. Schweizerbartsche Verlagsbuchhandlung, Stuttgart, 113–206
• Daugbjerg N., Hansen G., Larsen J. Moestrup Ø. (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates.  Phycologia 39: 302–317
• Dodge J. D. (1982) Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, London
• Dogiel V. (1906) Beiträge zur Kenntnis der Peridineen. Mitt. Zool. Sta. Neapel 18: 1–45
• Drebes G. (1974) Marines Phytoplankton: eine Auswahl der Helgoländer Planktonalgen (Diatomeen, Perideneen). Georg Thieme, Stuttgart
• Gast R. J., Fuerst P. A., Byers T. J. (1994) Discovery of group I introns in the nuclear small subunit ribosomal RNA genes of Acanthamoeba. Nucleic Acids Res. 22: 592–596
• Gómez F., Souissi S. (2008) The impact of the 2003 summer heat wave and the 2005 late cold wave on the phytoplankton in the north-eastern English Channel. C. R. Biol. 331: 678–685
• Grattepanche J. D., Breton E., Brylinski J. M., Lecuyer E., Christaki U. (2011) Succession of primary producers and micrograzers in a coastal ecosystem dominated by Phaeocystis globosa blooms. J. Plankton Res. 33: 37–50
• Hulburt E. M. (1957) The taxonomy of unarmoured Dinophyceae of shallow embayments on Cape Cod, Massachusetts. Biol. Bull. 112: 196–219
• Kofoid C. A., Swezy O. (1921) The free-living unarmored Dinoflagellata. Mem. Univ. Calif. 5: 1–538
• Kofoid C. A. (1931) Report of the biological survey of Mutsu Bay. 18. Protozoan fauna of Mutsu Bay. Subclass Dinoflagellata; Tribe Gymnodinoidae. Sci. Rep. Tohoku Imp. Univ. 4th ser., Biol. 6: 1–43
• Kumar S., Stecher G., Tamura K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870–1874
• Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A., Lopez R., Thompson J. D., Gibson T. J., Higgins D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948
• Lebour M. V. (1917) The Peridiniales of Plymouth Sound from the region beyond the breakwater. J. Mar. Biol. Ass. U.K. 11: 183–200
• Lebour M. V. (1925) The dinoflagellates of northern seas. Marine Biological Association of the United Kingdom, Plymouth Logares R., Bråte J., Bertilsson S., Clasen J. L., Shalchian-Tabrizi K., Rengefors K. (2009) Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol. 17: 414–422
• Medlin L., Elwood H. J., Stickel S., Sogin M. L. (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491–499
• Parke M., Dixon P. S. (1964) A revised check-list of British marine algae. J. Mar. Biol. Ass. U.K. 44: 499–542
• Penard E. (1891) Les Péridiniacées du Léman. Bull. Trav. Soc. Bot. Genève 6: 1–63
• Paulmier G. (1992) Catalogue illustré des microphytes planctoniques et benthiques des côtes normandes. DRV-92.007-RH/Le Robert. IFREMER, Issy-les-Moulineaux.
• Schütt, F. (1895) Die Peridineen der Plankton-Expedition. Ergebnisse der Plankton-Expedition der Humboldt-Stiftung 6: 1–170
• Stelfox-Widdicombe C. E., Archer S. D., Burkill P. H., Stefels J. (2004) Microzooplankton grazing in Phaeocystis and diatomdominated waters in the southern North Sea in spring. J. Sea Res. 51: 37–51
• Takano Y., Horiguchi T. (2004) Surface ultrastructure and molecular phylogenetics of four unarmored heterotrophic dinoflagellates, including the type species of the genus Gyrodinium (Dinophyceae). Phycol. Res. 54: 107–116
• Takayama H. (1998) Morphological and taxonomical studies of the free-living unarmored dinoflagellates occurring in the Seto Inland Sea and adjacent waters. Dissertation. The University of Tokyo, Tokyo
• Terrado R., Vincent W. F., Lovejoy C. (2009) Mesopelagic protists: diversity and succession in a coastal Arctic ecosystem. Aquat. Microb. Ecol. 56: 25–40
• Tillmann U., Hesse K. J. (1998) On the quantitative importance of heterotrophic microplankton in the northern German Wadden Sea. Estuaries 21: 585–596
• Wailes G. H. (1939) Canadian Pacific fauna. 1. Protozoa, 1e. Mastigophora. Technical report, University of Toronto Press for the Fisheries Research Board of Canada
• Weekers P. H. H., Gast R. J., Fuerst P. A., Byers T. J. (1994) Sequence variations in small subunit ribosomal RNAs of Hartmannella vermiformis and their phylogenetic implications. Mol. Biol. Evol. 11: 684–690

Identifiers

DOI

10.4467/16890027AP.20.007.12675

Biblioteka Nauki

52062719