Ultrastructure and LSU rDNA-based phylogeny of Esoptrodinium gemma (Dinophyceae), with notes on feeding behavior and the description of the flagellar base area of a planozygote

Journal of Phycology

Volumn 42, Issue 2, 2006, Pages 434-452

  Calado, António J ^a   Craveiro, Sandra C ^a   Daugbjerg, Niels ^b   Moestrup, Øjvind ^b  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Bernardinium bernardinense; Dinophyceae; Esoptrodinium gemma; Eyespot; Flagellar apparatus; LSU rDNA; Phagotrophy; Phylogeny; Planozygote; Ultrastructure

Indexed keywords

DINOFLAGELLATE; FEEDING BEHAVIOR; PHYLOGENY; ULTRASTRUCTURE;

BERNARDINIUM; CHLOROPHYTA; CILIOPHORA; DINOPHYCEAE; MASTIGOPHORA (FLAGELLATES); PSEUDOPODA;

EID: 33645515005     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2006.00195.x     Document Type: Article

References (66)

1. Bergholtz T. Daugbjerg N. Moestrup Ø. Fernández-Tejedor M. (in press). On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov., based on light and electron microscopy, nuclear-encoded LSU rDNA and pigment composition. J. Phycol. 42 170 93.
2. Calado A. J. Craveiro S. C. Moestrup Ø. 1998. Taxonomy and ultrastructure of a freshwater, heterotrophic Amphidinium (Dinophyceae) that feeds on unicellular protists. J. Phycol. 34 536 54.
3. Calado A. J. Hansen G. Moestrup Ø. 1999. Architecture of the flagellar apparatus and related structures in the type species of Peridinium, P. cinctum (Dinophyceae). Eur. J. Phycol. 34 179 91.
4. Calado A. J. Moestrup Ø. 1997. Feeding in Peridiniopsis berolinensis (Dinophyceae) new observations on tube feeding by an omnivorous, heterotrophic dinoflagellate. Phycologia 36 47 59.
5. Calado A. J. Moestrup Ø. 2002. Ultrastructural study of the type species of Peridiniopsis, Peridiniopsis borgei (Dinophyceae), with special reference to the peduncle and flagellar apparatus. Phycologia 41 567 84.
6. Calado A. J. Moestrup Ø. 2005. On the freshwater dinoflagellates presently included in the genus Amphidinium, with a description of Prosoaulax gen. nov. Phycologia 44 112 9.
7. Chodat R. ("avec la collaboration de M. J. Zender") 1924. Algues de la région du Grand Saint-Bernard. III. Bull. Soc. Bot. Genève Ser. 2 15 33 48.
8. Coats D. W. Tyler M. A. Anderson D. M. 1984. Sexual processes in the life cycle of Gyrodinium uncatenum (Dinophyceae) a morphogenetic overview. J. Phycol. 20 351 61.
9. Conrad W. 1926. Recherches sur les flagellates de nos eaux saumâtres. 1e partie dinoflagellates. Arch. Protistenk. 55 63 100 pls 1, 2.
10. Conrad W. 1939. Notes protistologiques. IX. Sur trois Dinoflagellates de l'eau saumâtre. Bull. Mus. R. Hist. Nat. Belg. 15 1 10.
11. Crawford R. M. Dodge J. D. 1971. The dinoflagellate genus Woloszynskia. II. The fine structure of W. coronata. Nova Hedwigia 22 699 719.
12. Dangeard P.-A. 1892. La nutrition animale des Péridiniens. Botaniste 3 7 27 pls 1, 2..
13. de Rijk P. Wuyts J. van der Peer Y. Winkelmans T. de Wachter R. 2000. The European large subunit ribosomal RNA database. Nucleic Acids Res. 28 117 8.
14. Dodge J. D. 1984. The functional and phylogenetic significance of dinoflagellate eyespots. BioSystems 16 259 67.
15. Dodge J. D. Crawford R. M. 1969. The fine structure of Gymnodinium fuscum. New Phytol. 68 613 8.
16. Gao X. Dodge J. D. 1991. The taxonomy and ultrastructure of a marine dinoflagellate, Scrippsiella minima sp. Nov.. Br. Phycol. J. 26 21 31.
17. Gao X. Dodge J. D. Lewis J. 1989. An ultrastructural study of planozygotes and encystment of a marine dinoflagellate, Scrippsiella sp.. Br. Phycol. J. 24 153 65.
18. Hansen P. J. Calado A. J. 1999. Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J. Eukaryot. Microbiol. 46 382 9.
19. Hansen G. Daugbjerg N. 2004. Ultrastructure of Gyrodinium spirale, the type species of Gyrodinium (Dinophyceae), including a phylogeny of G. dominans, G. rubrum and G. spirale deduced from partial LSU rDNA sequences. Protist 155 271 94.
20. Hansen G. Daugbjerg N. Franco J. M. 2003. Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae 2 317 35.
21. Hansen G. Moestrup Ø. 1998a. Fine-structural characterization of Alexandrium catenella (Dinophyceae) with special emphasis on the flagellar apparatus. Eur. J. Phycol. 33 281 91.
22. Hansen G. Moestrup Ø. 1998b. Light and electron microscopical observations on Peridiniella catenata (Dinophyceae). Eur. J. Phycol. 33 293 305.
23. Hansen G. Moestrup Ø. Roberts K. M. 2000. Light and electron microscopical observations on the type species of Gymnodinium, G. fuscum (Dinophyceae). Phycologia 39 365 76.
24. Heimann K. Roberts K. R. Wetherbee R. 1995. Flagellar apparatus transformation and development in Prorocentrum micans and P. minimum (Dinophyceae). Phycologia 34 323 35.
25. Huber-Pestalozzi G. 1950. Cryptophyceen, Chloromonadinen, Peridineen. In Thienemann A. [Ed.] Die Binnengewässer. Vol. 16. E. Schweizerbart'sche Verlagsbuchhandlung Stuttgart 310 pp.
26. Javornický P. 1962. Two scarcely known genera of the class Dinophyceae Bernardinium Chodat and Crypthecodinium Biecheler. Preslia 34 98 113.
27. Javornický P. 1997. Bernardinium Chodat (Dinophyceae), an athecate dinoflagellate with reverse, right-handed course of the cingulum and transverse flagellum, and Esoptrodinium genus novum, its mirror-symmetrical pendant. Arch. Hydrobiol. Suppl. 122 Algol. Stud. 87 29 42.
28. Kawai H. Kreimer G. 2000. Sensory mechanisms. Phototaxes and light perception in algae. In Leadbeater B. S. C. Green J. C. [Eds.] The Flagellates. Unity, Diversity and Evolution. Taylor & Francis New York pp. 124 46 (Systematics Association Special Volume No. 59.) pp. 124-146.
29. Kremp A. Elbrächter M. Schweikert M. Wolny J. L. Gottschling M. 2005. Woloszynskia halophila (Biecheler) comb. nov. a bloom-forming cold-water dinoflagellate co-occurring with Scrippsiella hangoei (Dinophyceae) in the Baltic Sea. J. Phycol. 41 629 42.
30. Leaché A. D. Reeder T. W. 2002. Molecular systematics of the eastern fence lizard (Sceloporus undulatus) a comparison of parsimony, likelihood, and Bayesian approaches. Syst. Biol. 51 44 68.
31. Leadbeater B. S. C. Dodge J. D. 1967a. An electron microscope study of nuclear and cell division in a dinoflagellate. Arch. Mikrobiol. 57 239 54.
32. Leadbeater B. S. C. Dodge J. D. 1967b. An electron microscope study of dinoflagellate flagella. J. Gen. Microbiol. 46 305 14 pls. 1-4.
33. Lenaers G. Maroteaux L. Michot B. Herzog M. 1989. Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA. J. Mol. Evol. 29 40 51.
34. Lindberg K. Moestrup Ø. Daugbjerg N. 2005. Studies on woloszynskioid dinoflagellates I Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 44 416 40.
35. Maddison D. R. Maddison W. P. 2003. MacClade 4. Sinauer Associates Inc. Sunderland, MAs, USA.
36. Matvienko O. M. Litvinenko R. M. 1977. Pirofitovi vodorosti. In Hollerbach M. M. Kondrat'eva N. V. [Eds.] Viznachnyk Prisnovodnykh Vodorostej Ukrains'koj RSR. Vol. 3(2). Naukova Dumka Kiev 386 pp.
37. Moestrup Ø. 2000. The flagellate cytoskeleton. Introduction of a general terminology for microtubular flagellar roots in protists. In Leadbeater B. S. C. Green J. C. [Eds.] The Flagellates. Unity, Diversity and Evolution (Systematics Association Special Volume No. 59). Taylor & Francis New York pp. 69 94.
38. Moestrup Ø. Hansen G. Daugbjerg N. Flaim G. D'Andrea M. Studies on woloszynskioid dinoflagellates II on Tovellia sanguinea sp. nov., the dinoflagellate species responsible for the reddening of Lake Tovel, N. Italy. Eur. J. Phycol. (submitted).
39. Nichols H. W. 1973. Growth media - freshwater. In Stein J. R. [Ed.] Handbook of Phycological Methods. Culture Methods and Growth Measurements. Cambridge University Press Cambridge pp. 7 24.
40. Patterson D. J. 1999. Diversity of eukaryotes. Am. Nat. 154 S96 S124.
41. Pfiester L. A. 1984. Sexual reproduction. In Spector D. L. [Ed.] Dinoflagellates. Academic Press Orlando pp. 181 99.
42. Popovský J. 1990. New knowledge on freshwater dinoflagellates of Central Europe; with description of a new species. Arch. Hydrobiol. Suppl. 87 Algol. Stud. 60 1 18.
43. Popovský J. Pfiester L. A. 1990. Dinophyceae (Dinoflagellida). In Ettl H. Gerloff J. Heynig H. Mollenhauer D. [Eds.] Süßwasserflora von Mitteleuropa. Vol. 6. Gustav Fischer Jena 272 pp.
44. Posada D. Crandall K. A. 1998. MODELTEST testing the model of DNA substitution. Bioinformatics 14 817 8.
45. Roberts K. R. Hansen G. Taylor F. J. R. 1995. General ultrastructure and flagellar apparatus architecture of Woloszynskia limnetica (Dinophyceae). J. Phycol. 31 948 57.
46. Roberts K. R. Timpano P. 1989. Comparative analyses of the dinoflagellate flagellar apparatus. I. Woloszynskia sp. J. Phycol. 25 26 36.
47. Ronquist F. Huelsenbeck J. P. 2003. Mr. Bayes 3 Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 4.
48. Schiller J. 1935. Dinoflagellatae (Peridineae) in monographischer Behandlung. In Kolkwitz R. [Ed.] Rabenhorst's Kryptogamen-flora von Deutschland, Österreich und der Schweiz. 2nd ed. Vol. 10, 3 part 2. Akademische Verlagsgesellschaft Leipzig pp. 589 [The volume was finished in 1937 but the relevant pages were published in March 1935].
49. Scholin C. A. Herzog M. Sogin M. Anderson D. M. 1994. Identification of group-and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the LSU rRNA gene. J. Phycol. 30 999 1011.
50. Spero H. J. 1982. Phagotrophy in Gymnodinium fungiforme (Pyrrhophyta) the peduncle as an organelle of ingestion. J. Phycol. 18 356 60.
51. Spero H. J. 1985. Chemosensory capabilities in the phagotrophic dinoflagellate Gymnodinium fungiforme. J. Phycol. 21 181 4.
52. Starmach K. 1974. Cryptophyceae, Dinophyceae, Raphidophyceae. In Starmach K. Sieminska J. [Eds.] Flora Słodkowodna Polski. Vol. 4. Państwowe Wydawnictwo Naukowe Warszawa 520 pp.
53. Stein F. 1878. Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfolge bearbeitet. III. Abtheilung. Die Naturgeschichte der Flagellaten oder Geisselinfusorien. I. Hälfte. Den noch nicht Abgeschlossenen allgemeinen Theil nebst Erklärung der sämmtlichen Abbildungen enthaltend. Wilhelm Engelmann Leipzig 154 pp., 24 pls.
54. Stein F. 1883. Der Organismus der Infusionsthiere... III. Abtheilung. II. Hälfte. Die Naturgeschichte der arthrodelen Flagellaten. Einleitung und Erklärung der Abbildungen. Wilhelm Engelmann Leipzig 30 pp., 25 pls.
55. von Stosch H. A. 1964. Zum Problem der sexuellen Fortpflanzung in der Peridineengattung Ceratium. Helgol. Wiss. Meeresunters. 10 140 52.
56. von Stosch H. A. 1965. Sexualität bei Ceratium cornutum (Dinophyta). Naturwissenschaften 52 112 3.
57. von Stosch H. A. 1973. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates, Gymnodinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. Br. Phycol. J. 8 105 34.
58. * Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates Sunderland, MA.
59. Tamura K. Nei N. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10 512 26.
60. Thompson R. H. 1951. A new genus and new records of fresh-water Pyrrophyta in the Desmokontae and Dinophyceae. Lloydia 13 277 99.
61. Van de Peer Y. Van der Auwera G. de Wachter R. 1996. The evolution of stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal RNA. J. Mol. Evol. 42 201 10.
62. Wawrik F. 1983. Sommerliche Planktonaspekte 1981 seltene und neue Algen aus Teichen des Waldviertels in Niederösterreich. Nova Hedwigia 36 775 94.
63. Wedemayer G. J. Wilcox L. W. 1984. The ultrastructure of the freshwater colorless dinoflagellate Peridiniopsis berolinense (Lemm.) Bourrelly. J. Protozool. 31 444 53.
64. Wilcox L. W. 1989. Multilayered structures (MLSs) in two dinoflagellates, Katodinium campylops and Woloszynskia pascheri. J. Phycol. 25 785 9.
65. Wołoszyńska J. 1917. Nowe gatunki Peridineów, tudziez spostrzezenia nad budowa okrywy u Gymnodiniów i Glenodiniów. - Neue Peridineen-Arten, nebst Bemerkungen über den Bau der Hülle bei Gymno- und Glenodinium. Bull. Int. Acad. Sci. Cracovie, Cl. Sci. Math. Nat., Ser. B 1917 114 22 pls. 11-13.
66. Yang Z. Rannala B. 1997. Bayesian phylogenetic inference using DNA sequences a Markov chain Monte Carlo method. Mol. Biol. Evol. 14 717 24.