Abstract
Oxyrrhis marina was subjected to conventional transmission electron microscopy, with emphasis being laid on its extrusomes. Mainly regular trichocysts were obvious in ultrathin sections. They were highly abundant, approximately 2 μm in length and 200 nm in width, and composed of the characteristic features, i.e., an anterior tip and the posterior crystalline body. The tip measures approximately 440 nm in length and is built by an outer less electron-dense concentric layer followed by an inner electron-dense core with a translucent center in the middle. The less electron-dense layer most likely ends up in a bundle of filaments which are concentrically placed around the electron-dense core in the transition zone between the tip and body. Trichocyst bodies which are sectioned along the longitudinal axis are approximately 1.5 μm in length and show a regular striation of electron-dense and electron-translucent lines with a spacing of 9 nm. Cross-sectioned bodies are square-shaped and show a crystalline lattice composed of particles which are 8–9 nm in size. Discharge of regular trichocysts results in long rigid rods. They are square-shaped, 54 nm broad, and with a regular striation of approximately 54 nm along their longitudinal axes. Besides regular trichocysts, an additional type of extrusome was registered. It is not as abundant as regular trichocysts, membrane-enclosed, 2 μm in length and 180 nm in width, and resembles two bullets adjacent to each other with the tips facing in opposite directions. The two parts are slightly of different lengths (anterior part, 740 nm; posterior part, 590 nm) and widths (anterior part, 126 nm; posterior part, 117 nm) and separated from each other by a gap of 30 nm. The anterior part is more electron-dense than the posterior one. A faint electron-dense sheet-like structure was registered between the envelope membrane and these two inner structures. In extrusomes which had been arrested in the process of discharge, the anterior part gives rise to an oozing, amorphous, fibrous blob, while the posterior part consists of twisted filaments which most likely function as the charge of a gun for the release of the anterior part.
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References
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42
Boakes DE, Codling EA, Thorn GJ, Steinke M (2011) Analysis and modelling of swimming behaviour in Oxyrrhis marina. J Plankton Res 33:641–649
Bouck GB, Sweeney BM (1966) The fine structure and ontogeny of trichocysts in marine dinoflagellates. Protoplasma 61:205–223
Breckels MN, Roberts EC, Archer SD, Malin G, Steinke M (2011) The role of dissolved infochemicals in mediating predator–prey interactions in the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 33:629–639
Cachon M, Cosson J, Cosson M-P, Huitorel P, Cachon J (1988) Ultrastructure of the flagellar apparatus of Oxyrrhis marina. Biol Cell 63:159–168
Clarke KJ, Pennick NC (1976) The occurrence of body scales in Oxyrrhis marina Dujardin. Br Phycol J 11:345–348
Davidson K, Sayegh F, Montagnes DJS (2011) Oxyrrhis marina-based models as a tool to interpret protozoan population dynamics. J Plankton Res 33:651–663
Dodge JD, Crawford RM (1971a) Fine structure of the dinoflagellate Oxyrrhis marina. I. The general structure of the cell. Protistologica 7:295–303
Dodge JD, Crawford RM (1971b) Fine structure of the dinoflagellate Oxyrrhis marina. II. The flagellar system. Protistologica 7:399–409
Dodge JD, Crawford RM (1974) Fine structure of the dinoflagellate Oxyrrhis marina. III. Phagotrophy. Protistologica 10:239–244
Gavelis GS (2015) Evolution of complex organelles in dinoflagellates. Dissertation, The University of British Columbia, Vancouver
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervaceae (Cleve) Gran. Can J Microbiol 8:229–239
Hansen G, Moestrup Ø (1998) Light and electron microscopical observations on Peridiniella catenata (Dinophyceae). Eur J Phycol 33:293–305
Hausmann K (1973) Cytologische studien an trichocysten. VI. Feinstruktur und Funktionsmodus der Trichocysten der Flagellaten Oxyrrhis marina und des Ciliaten Pleuronema marinum. Helgoländer Meeresun 25:39–62
Hausmann K (1978) Extrusive organelles in protists. Int Rev Cytol 52:197–276
Höhfeld I, Melkonian M (1998) Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (Dinophyceae) and its rearrangement during phagocytosis. Protist 149:75–78
Honsell G, Bonifacio A, De Bortoli M, Penna A, Battocchi C, Ciminiello P, Dell’Aversano C, Fattorusso E, Sosa S, Yasumoto T, Tubaro A (2013) New insights on cytological and metabolic features of Ostreopsis cf. ovata Fukuyo (Dinophyceae): a multidisciplinary approach. PLoS ONE 8(2):e57291. doi:10.1371/journal.pone.0057291
Hoppenrath M, Leander BS (2007) Morphology and phylogeny of the pseudocolonial dinoflagellate Polykrikos lebourae and Polykrikos herdmanae n. sp. Protist 158:209–227
Hoppenrath M, Yubuki N, Bachvaroff TR, Leander BS (2010) Re-classification of Phaeopolykrikos hartmannii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes. Eur J Protistol 46:29–37
Hoppenrath M, Chomérat N, Horiguchi T, Schweikert M, Nagahama Y, Murray S (2013) Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae)—A proposal and review. Harmful Algae 27:1–28
Hwang JS, Nagai S, Hayakawa S, Takaku Y, Gojobori T (2008) The search for the origin of cnidarian nematocysts in dinoflagellates. In: Pontarotti P (ed) Evolutionary biology from concept to application. Springer, Berlin, pp 135–152
Lee MJ, Jeong HJ, Lee KH, Jang SH, Kim JH, Kim KY (2015) Mixotrophy in the nematocyst-taeniocyst complex-bearing phototrophic dinoflagellate Polykrikos hartmannii. Harmful Algae 49:124–134
Livolant F (1982a) Dinoflagellate trichocyst ultrastructure. I—The shaft. Biol Cell 43:201–210
Livolant F (1982b) Dinoflagellate trichocyst ultrastructure. II—Existance of a sheath. Biol Cell 43:211–216
Lowe CD, Keeling PJ, Martin LE, Slamovits CH, Watts PC, Montagnes DJS (2011) Who is Oxyrrhis marina? Morphological and phylogenetic studies on an unusual dinoflagellate. J Plankton Res 33:555–567
Messer G, Ben-Shaul Y (1971) Fine structure of trichocyst fibrils of the dinoflagellate Peridinium westii. J Ultrastruct Res 37:94–104
Montagnes DJS, Lowe CD, Martin L, Watts PC, Downes-Tettmar N, Yang Z, Roberts EC, Davidson K (2011) Oxyrrhis marina growth, sex and reproduction. J Plankton Res 33:615–627
Öpik H, Flynn KJ (1989) The digestive process of the dinoflagellate, Oxyrrhis marina Dujardin, feeding on the chlorophyte, Dunaliella primolecta Butcher: a combined study of ultrastructure and free amino acids. New Phytol 113:143–151
Rhiel E, Westermann M, Steiniger F, Kirchhoff C (2013) Isolation and characterization of the ejectisomes of the prasinophyte Pyramimonas grossii. Protoplasma 250:1351–1361
Roberts EC, Wootton EC, Davidson K, Jeong HJ, Lowe CD, Montagnes DJS (2011) Feeding in the dinoflagellate Oxyrrhis marina: linking behavior with mechanisms. J Plankton Res 33:603–614
Slamovits CH, Keeling PJ (2011) Contributions of Oxyrrhis marina to molecular biology, genomics and organelle evolution of dinoflagellates. J Plankton Res 33:591–602
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Vesk M, Lucas IAN (1986) The rhabdosome: a new type of organelle in the dinoflagellate Dinophysis. Protoplasma 134:62–64
Westfall J, Bradbury PC, Townsend JW (1983) Ultrastructure of the dinoflagellate Polykrikos. I. Development of the nematocyst-taeniocyst complex and morphology of the site for extrusion. J Cell Sci 63:245–261
Yamada N, Terada R, Tanaka A, Horiguchi T (2013) Bispinodinium angelaceum gen. et sp. nov. (Dinophyceae), a new sand-dwelling dinoflagellate from the seafloor off Mageshima Island, Japan. J Phycol 49:555–569
Acknowledgments
The author expresses his gratitude to Ms. Silke Ammermann for excellent technical assistance, to Mr. Frank Steiniger (EMZ, University of Jena, Germany) for his help in lattice analysis, and to Mr. F. Rhiel for his help in the schematic drawings of Fig. 7.
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Rhiel, E. On the extrusomes of Oxyrrhis marina (Dinophyceae). Protoplasma 254, 901–909 (2017). https://doi.org/10.1007/s00709-016-0999-2
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DOI: https://doi.org/10.1007/s00709-016-0999-2