Skip to main content
Log in

On the extrusomes of Oxyrrhis marina (Dinophyceae)

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42

    Google Scholar 

  • Boakes DE, Codling EA, Thorn GJ, Steinke M (2011) Analysis and modelling of swimming behaviour in Oxyrrhis marina. J Plankton Res 33:641–649

    Article  Google Scholar 

  • Bouck GB, Sweeney BM (1966) The fine structure and ontogeny of trichocysts in marine dinoflagellates. Protoplasma 61:205–223

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Clarke KJ, Pennick NC (1976) The occurrence of body scales in Oxyrrhis marina Dujardin. Br Phycol J 11:345–348

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Dodge JD, Crawford RM (1971a) Fine structure of the dinoflagellate Oxyrrhis marina. I. The general structure of the cell. Protistologica 7:295–303

    Google Scholar 

  • Dodge JD, Crawford RM (1971b) Fine structure of the dinoflagellate Oxyrrhis marina. II. The flagellar system. Protistologica 7:399–409

    Google Scholar 

  • Dodge JD, Crawford RM (1974) Fine structure of the dinoflagellate Oxyrrhis marina. III. Phagotrophy. Protistologica 10:239–244

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hansen G, Moestrup Ø (1998) Light and electron microscopical observations on Peridiniella catenata (Dinophyceae). Eur J Phycol 33:293–305

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Höhfeld I, Melkonian M (1998) Lifting the curtain? The microtubular cytoskeleton of Oxyrrhis marina (Dinophyceae) and its rearrangement during phagocytosis. Protist 149:75–78

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoppenrath M, Leander BS (2007) Morphology and phylogeny of the pseudocolonial dinoflagellate Polykrikos lebourae and Polykrikos herdmanae n. sp. Protist 158:209–227

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Livolant F (1982a) Dinoflagellate trichocyst ultrastructure. I—The shaft. Biol Cell 43:201–210

    Google Scholar 

  • Livolant F (1982b) Dinoflagellate trichocyst ultrastructure. II—Existance of a sheath. Biol Cell 43:211–216

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Messer G, Ben-Shaul Y (1971) Fine structure of trichocyst fibrils of the dinoflagellate Peridinium westii. J Ultrastruct Res 37:94–104

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rhiel E, Westermann M, Steiniger F, Kirchhoff C (2013) Isolation and characterization of the ejectisomes of the prasinophyte Pyramimonas grossii. Protoplasma 250:1351–1361

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Erhard Rhiel.

Ethics declarations

Conflict of interest

The author declares that he has no conflict of interest.

Additional information

Handling Editor: Reimer Stick

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rhiel, E. On the extrusomes of Oxyrrhis marina (Dinophyceae). Protoplasma 254, 901–909 (2017). https://doi.org/10.1007/s00709-016-0999-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-016-0999-2

Keywords

Navigation