Ultrastructural features of the basal dinoflagellate Ellobiopsis chattoni (Ellobiopsidae, Alveolata), parasite of copepods.
DOI:
https://doi.org/10.37543/oceanides.v29i2.135Keywords:
Apicomplexa, Dinophyceae, perkinsids, Perkinsozoa, Syndiniales, syndinianAbstract
Ellobiopsis chattoni is the type species of the ellobiopsids, an enigmatic lineage of parasitic alveolates that branched between the syndinean dinoflagellates and the perkinsids. We have investigated the ultrastructure of four trophonts from three calanoid copepod hosts collected from the port of Valencia, northwestern Mediterranean Sea. The cell wall showed a thick and homogenous layer and flask-shaped mucocysts that excreted an electron-dense substance that forms the outer layer. The cell wall in the attachment peduncle of Ellobiopsis was thicker and with numerous invaginations. The inner section showed numerous longitudinal channels here interpreted as conduits for the transport of host fluids. Trophomere and gonomere were separated by a thin septum with a central pore. Before the mature gonomere detached from the trophomere, the area of junction became undulated. Deficiencies in the fixation of the membrane organelle preclude discussing on
other ultrastructural features. To date the ultrastructure of three ellobiopsid genera have been examined. The trophonts of Ellobiopsis and Thalassomyces showed a high similarity in the cell wall, with characteristic flaskshaped mucocysts. The lack of flask-shaped mucocysts in Ellobiocystis and other morphological and ecological differences argue against the monophyly of the ellobiopsids.
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References
Albaina, A. & X. Irigoien. 2006. Fecundity limitation of Calanus helgolandicus by the parasite Ellobiopsis sp. J. Plankton Res., 28:413-418. https://doi.org/10.1093/plankt/fbi129
Appleton, P.L. & K. Vickerman. 1998. In vitro cultivation and developmental cycle in culture of a parasitic dinoflagellate (Hematodinium sp.) associated with mortality of the Norway lobster (Nephrops norvegicus) in British waters. Parasitol., 116: 115-130. https://doi.org/10.1017/S0031182097002096
Bradbury, P.C. 1994. Parasitic protozoa of mollusks and crustaceans. 139-264. In: J.P. Kreier (Ed.). Parasitic Protozoa. Academic Press, New York. https://doi.org/10.1016/B978-0-08-092414-4.50008-9
Cachon, J. 1964. Contribution à l'étude des Péridiniens parasites. Cytologie, cycles évolutifs. Ann. Sci. nat. Zool., 6 (12e): 1-158.
Cachon, J. & M. Cachon. 1971. Ultrastructures du genre Oodinium Chatton. Différenciations cellulaires en rapport avec la vie parasitaire. Protistologica, 7: 153-169.
Cachon, J. & M. Cachon. 1974. Le système stomatopharyngien de Kofoidinium Pavillard. Comparaisons avec celui divers Péridiniens fibres et parasites. Protistologica, 10: 217-222.
Cachon, J. & M. Cachon. 1977. Observations on the mitosis and on the chromosome evolution during the life cycle of Oodinium, a parasitic dinoflagellate. Chromosoma, 60:237-251. https://doi.org/10.1007/BF00329773
Caullery, M. 1910. Ellobiopsis chattoni, n. g., n. sp., parasite de Calanus helgolandicus Claus, appartenant probablement aux Péridiniens. Bull. biol. Fr. Bel., 44: 201-214.
Cavalier-Smith, T. 1991. Cell diversification in heterotrophic flagellates. 113-131. In: D.J. Patterson & J. Larsen (Eds.). The Biology of Free-Living Heterotrophic Flagellates. Syst. Assoc. Special Vol. 45. Clarendon Press, Oxford.
Corliss, J.O. 1975. Nuclear characteristics and phylogeny in the protistan phylum Ciliophora. Biosystems, 7: 338-349. https://doi.org/10.1016/0303-2647(75)90012-X
Dick, M.W. 2001. Straminipilous Fungi: Systematics of the Peronosporomycetes, including accounts of the marine straminipilous protists, the plasmodiophorids, and similar organisms. Kluwer, Dordrecht.
Dodge, J.D. & R.M. Crawford. 1971. Fine structure of the dinoflagellate Oxyrrhis marina. Part 1: The general structure of the cell. Protistologica, 7: 295-304.
Fritz, L. & M. Nass. 1992. Development of the endoparasitic dinoflagellate Amoebophrya ceratii within host dinoflagellate species. J. Phycol., 28: 312-320. https://doi.org/10.1111/j.0022-3646.1992.00312.x
Gajadhar A.A., W.C. Marquardt, R. Hall, J. Gunderson, E.V. Aritzia-Carmona & M.L. Sogin. 1991. Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates and ciliates. Mol. Biochem. Parasitol., 45: 147-154. https://doi.org/10.1016/0166-6851(91)90036-6
Galt, J.H. & H.C. Whisler. 1970. Differentiation of flagellated spores in Thalassomyces ellobiopsid parasite of marine Crustaceae. Arch. Mikrobiol., 71: 295-303. https://doi.org/10.1007/BF00417127
Goggin, C.L. & S.C. Barker. 1993. Phylogenetic position of the genus Perkinsus (Protista, Apicomplexa) based on small subunit ribosomal RNA. Mol. Biochem. Parasitol., 60: 65-70. https://doi.org/10.1016/0166-6851(93)90029-W
Gómez, F. 2012. A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Syst. Biodivers., 10: 267-275. https://doi.org/10.1080/14772000.2012.721021
Gómez, F., P. López-García, A. Nowaczyk & D. Moreira. 2009. The crustacean parasites Ellobiopsis Caullery, 1910 and Thalassomyces Niezabitowski, 1913 form a monophyletic divergent clade within the Alveolata. Syst. Parasitol., 74: 65-74. https://doi.org/10.1007/s11230-009-9199-1
Gómez, F., D. Moreira & P. López-García. 2010. Molecular phylogeny of noctilucoid dinoflagellates (Noctilucales, Dinophyta). Protist, 161: 466-478. https://doi.org/10.1016/j.protis.2009.12.005
Gómez-Gutiérrez, J., C.J. Robinson, S. Kawaguchi & S. Nicol. 2010. Parasite diversity of Nyctiphanes simplex and Nematoscelis difficilis (Crustacea: Euphausiacea) along the northwestern coast of México. Dis. Aquat. Org., 88: 249-266. https://doi.org/10.3354/dao02155
Harada, A., S. Ohtsuka & T. Horiguchi. 2007. Species of the parasitic genus Duboscquella are members of the enigmatic Marine Alveolate Group I. Protist, 158: 337-347. https://doi.org/10.1016/j.protis.2007.03.005
Hovasse, R. 1935. Deux péridiniens parasites convergents: Oodinium poucheti (Lemm.), Protoodinium chattoni gen. nov. sp. nov. Bull. biol. Fr. Bel., 69: 59-86.
Hovasse, R. 1952. Ellobiopsis fagei Hovasse, Ellobiopsidé parasite, en Méditerranée, de Clausocalanus arcuicornis Dana. Bull. Inst. Oceanogr., 1016: 1-12.
Höhfeld, I. & M. Melkonian. 1988. Amphiesmal ultrastructure in Noctiluca miliaris Suriray (Dinophyceae). Helgol. Meeresunt., 42: 601-612. https://doi.org/10.1007/BF02365630
Horiguchi, T. & S. Ohtsuka. 2001. Oodinium inlandicum sp. nov. (Blastodiniales, Dinophyta), a new ectoparasitic dinoflagellate infecting a chaetognath, Sagitta crassa. Plankton Biol. Ecol., 48: 85-95.
Lee, J.J., S.H. Hutner & E.C. Bovee (Eds.). 1985. An Illustrated Guide to the Protozoa. Society of Protozoologists. Allen, Lawrence, Kansas.
McLean, N. & C. Nielsen. 1989. Oodinium jordani n. sp., a dinoflagellate (Dinoflagellata: Oodinida) ectoparasitic on Sagitta elegans (Chaetognatha). Dis. Aquat. Org., 7: 61-66. https://doi.org/10.3354/dao007061
Miller, J.J., C.F. Delwiche & D.W. Coats. 2012. Ultrastructure of Amoebophrya sp. and its changes during the course of infection. Protist, 163: 720-745. https://doi.org/10.1016/j.protis.2011.11.007
Netzel, H. & G. Dürr. 1984. Dinoflagellates cell cortex. 43-105. In: D.L. Spector (Ed.). Dinoflagellates. Academic Press, New York. https://doi.org/10.1016/B978-0-12-656520-1.50007-9
Norén, F., O. Moestrup & A.-S. Rehnstam -Holm. 1999. Parvilucifera infectans Norén et Moestrup sp. nov. (Perkinsozoa phylum nov.): A parasitic flagellate capable of killing toxic microalgae. Eur. J. Protistol., 35:233-254. https://doi.org/10.1016/S0932-4739(99)80001-7
Oborník, M., D. Modrý, M. Lukeš, E. Cernotíková-Stříbrná, J. Cihlář, M. Tesařová, E. Kotabová, M. Vancová, O. Prášil & J. Lukeš. 2012. Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist, 163:306-323. https://doi.org/10.1016/j.protis.2011.09.001
Ohtsuka, S., T. Horiguchi, Y. Hanamura, K. Nagasawa & T. Suzaki. 2003. Intersex in the mysid Siriella japonica izuensis Li: the possibility it is caused by infestation with parasites. Plankton Biol. Ecol., 50: 65-70.
Okamoto, N., A. Horák & P.J. Keeling. 2012. Description of two species of early branching dinoflagellates, Psammosa pacifica n. g., n. sp. and P. atlantica n. sp. PLoS ONE 7 (6): art. no. e34900. https://doi.org/10.1371/journal.pone.0034900
Perkins F.O., J.R. Barta, R.E. Clopton, M.A. Pierce & S.J. Upton. 2000. Phylum Apicomplexa. 190-304. In: J.J. Lee, G.F. Leedale & P. Bradbury (Eds.). The Illustrated Guide to the Protozoa. Allen Press, Lawrence, Kansas.
Ris H. & D.F. Kubai. 1974. An unusual mitotic mechanism in the parasitic protozoan Syndinium sp. J. Cell Biol., 60: 702-720. https://doi.org/10.1083/jcb.60.3.702
Saldarriaga, J.F., M.L. McEwan, N.M. Fast, F.J.R. Taylor & P.J. Keeling. 2003. Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int. J. Syst. Evol. Microbiol., 53: 355-365. https://doi.org/10.1099/ijs.0.02328-0
Sam-Yellowe, T.Y. 1996. Rhoptry organelles of the apicomplexa: Their role in host cell invasion and intracellular survival. Parasitol. Today, 12: 308-316. https://doi.org/10.1016/0169-4758(96)10030-2
Schweikert, M. & M. Elbrächter. 2006. First ultrastructural investigations on Ellobiopsis spec. (incertae sedis) a parasite of copepods. Endocytobiosis Cell Res., 17: 73.
Scott, T. 1897. The marine fishes and invertebrates of Loch Fyne. 15th Annual Reports of Fisheries Board, Scottish Science Investigations, 107-174. https://doi.org/10.5962/bhl.title.53611
Shields, J.D. 1994. The parasitic dinoflagellates of marine crustaceans. Annual Rev. Fish Diseases, 4: 241-271. https://doi.org/10.1016/0959-8030(94)90031-0
Siano, R., M. Montresor, I. Probert, F. Not & C. de Vargas. 2010. Pelagodinium gen. nov. and P. béii comb. nov., a dinoflagellate symbiont of planktonic foraminifera. Protist, 161: 385-399. https://doi.org/10.1016/j.protis.2010.01.002
Silberman J.D., A.G. Collins, L.A., Gershwin, P.J. Johnson & A.J. Roger. 2004. Ellobiopsids of the genus Thalassomyces are alveolates. J. Eukaryot. Microbiol., 52: 246-252. https://doi.org/10.1111/j.1550-7408.2004.tb00555.x
Skovgaard, A., R. Massana, V. Balagué & E. Saiz. 2005. Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist, 156: 413-423. https://doi.org/10.1016/j.protis.2005.08.002
Small, H.J., J.D. Shields, K.S. Reece, K. Bateman & G.D. Stentiford. 2012. Morphological and molecular characterization of Hematodinium perezi (Dinophyceae: Syndiniales), a dinoflagellate parasite of the harbour crab, Liocarcinus depurator. J. Eukaryot. Microbiol., 59: 54-66. https://doi.org/10.1111/j.1550-7408.2011.00592.x
Soyer, M.O. 1972. Les ultrastructures nucléaires de la Noctiluque (Dinoflagellé libre) au cours de la sporogenése. Chromosoma, 39: 419-441. https://doi.org/10.1007/BF00326176
Soyer, M.O. 1974. Étude ultrastructurale de Syndinium sp. Chatton parasite coelomique de copépodes Pélagiques. Vie Milieu, 24: 191-212.
Taylor, F.J.R. (Ed.) 1987. The Biology of Dinoflagellates. Botanical Monographs 21, Blackwell, Oxford.
Triemer, R.E. 1982. A unique mitotic variation in the marine dinoflagellate Oxyrrhis marina (Pyrrhophyta). J. Phycol., 18: 399-411. https://doi.org/10.1111/j.1529-8817.1982.tb03202.x
Whisler, H.C. 1990. Incertae Sedis Ellobiopsida. 715-719. In: L. Margulis, J.O. Corliss, M. Melkonian & D.J. Chapman (Eds.). Handbook of Protoctista. Jones & Bartlett, Boston.
Wolters, J. 1991. The troublesome parasites - molecular and morphological evidence that Apicomplexa belong to the dinoflagellateciliate clade. BioSystems, 25: 75-83. https://doi.org/10.1016/0303-2647(91)90014-C
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