Abstract
The nucleotide sequence analysis of the PCR products corresponding to the variable large-subunit rRNA domains D1, D2, D9, and D10 from ten representative dinoflagellate species is reported. Species were selected among the main laboratory-grown dinoflagellate groups: Prorocentrales, Gymnodiniales, and Peridiniales which comprise a variety of morphological and ecological characteristics. The sequence alignments comprising up to 1,000 nucleotides from all ten species were employed to analyze the phylogenetic relationships among these dinoflagellates. Maximum parsimony and neighbor joining trees were inferred from the data generated and subsequently tested by bootstrapping. Both the D1/D2 and the D9/D10 regions led to coherent trees in which the main class of dinoflagellates, Dinophyceae, is divided in three groups: prorocentroid, gymnodinioid, and peridinioid. An interesting outcome from the molecular phylogeny obtained was the uncertain emergence of Prorocentrum lima. The molecular results reported agreed with morphological classifications within Peridiniales but not with those of Prorocentrales and Gymnodiniales. Additionally, the sequence comparison analysis provided strong evidence to suggest that Alexandrium minutum and Alexandrium lusitanicum were synonymous species given the identical sequence they shared. Moreover, clone Gg1V, which was determined Gymnodinium catenatum based on morphological criteria, would correspond to a new species of the genus Gymnodinium as its sequence clearly differed from that obtained in G. catenatum. The sequence of the amplified fragments was demonstrated to be a valuable tool for phylogenetic and taxonomical analysis among these highly diversified species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anderson DM (1990) Toxin variability in Alexandrium species. In: Graneli E, Sundstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, New York, pp 41–51
Balech E (1985) The genus Alexandrium or Gonyaulax of the tamarensis group. In: Anderson DM, White AW, Baden DG (eds) Toxic marine dinoflagellates. Elsevier, New York, pp 33–38
Balech E (1989) Redescription of Alexandrium minutum Halim (Dinophyceae) type species of the genus Alexandrium. Phycologia 28(2):206–211
Baroin A, Perasso R, Qu LH, Brugerolle G, Bachellerie JP, Adoutte A (1988) Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S ribosomal RNA. Proc Natl Acad Sci USA 85:3474–3478
Bujak J, Williams G (1981) The evolution of dinoflagellates. Can J Bot 59:2077–2087
Costas E, López-Rodas V (1994) Identification of marine dinoflagellates using fluorescent lectins. J Phycol 30:987–990
Deveraux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387–395
Dodge JD (1965) Chromosome structure in the dinoflagellates and the problem of the mesokaryotic cell. Excerpta Med Int Congr Ser 91:339–341
Dodge JD (1982) Marine dinoflagellates on the Britain Isles. Her Majesty's Stationery Office, London, pp 1–303
Dodge JD (1984) Dinoflagellate taxonomy. In: Spector DL (ed) Dinoflagellates. Academic Press, New York, pp 17–42
Engberg J, Nielsen H, Lenaers G, Murayama O, Fujitani H, Higashinakawa T (1990) Comparison of primary and secondary 26S rRNA structures in two structural constraint in expansion segments. J Mol Evol 30:514–521
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nature 111:223–257
Fraga S, Bravo I, Delgado M, Franco JM, Zapata M (1994) Differences between two chain forming, athecate, red-tide dinoflagellates: Gymnodinium catenatum Graham and Gymnodinium sp. In: Lassus P (ed) Toxic marine phytoplankton. Doc and Lavoissier, Paris (in press)
Greenwood SJ, Sogin ML, Lynn DH (1991) Phylogenetic relationships within the class oligohymenophorea, phylum Ciliophora, inferred from the complete small subunit rRNA gene sequences of Colpidium campylum, Glaucoma chattoni, and Opisthonecta henneguyi. J Mol Evol 33:163–174
Halim Y (1960) Alexandrium minutum nov. g. nov. sp. dinoflagellé provocant des “eaux rouges”. Vie Milieu 11(1):102–105
Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–561
Herzog M, von Boletsky S, Soyer MO (1984) Ultrastructural and biochemical nuclear aspects of the dinoflagellates as a sister group of the actual eukaryotes? Orig Life 13:205–215
Ishida Y, Chang-Hoon K, Yoshihiko S, Nobuyasu H, Aritsume U (1993) PSP toxin production is chromosome dependent in Alexandrium spp. In: Smayda TJ, Shimizu Y (eds) Toxic marine phytoplankton. Elsevier, New York, pp 881–887
Kodama M (1990) Possible links between bacteria and toxin production in algal blooms. In: Graneli E, Sandstrom B, Edler L, Anderson DM (eds) Toxic marine phytoplankton. Elsevier, Amsterdam, pp 52–61
Lapeyre B, Feliu J (1993) Nucleotide sequence of LsuRNA from Schizosaccharomyces pombe directly submitted to GenBank with accession number z19578 (Unpublished)
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(1):40–51
Lenaers G, Scholin C, Bhaud Y, Saint-Hilaire D, Herzog M (1991) A molecular phylogeny of dinoflagellate protists (Pyrrophyta) inferred from the sequence of 24S rRNA divergent domains D1 and D8. J Mol Evol 32:53–63
Loeblich AR (1976) Dinoflagellate evolution: speculation and evidence. J Protozool 23:13–28
Loeblich AR (1984) Dinoflagellate evolution. In: Spector DL (ed) Dinoflagellates. Academic Press, New York, pp 481–522
Mendoza H, López-Rodas V, González-Gil S, Aguilera A, Costas E (1995) Use of polyclonal antisera and blocking of the antibodies in the identification of marine dinoflagellates: species-specific and clone-specific antisera against Gymnodinium and Alexandrium. J Exp Mar Biol Ecol (in press)
Michot B, Hassouna N, Bachelleire JP (1984) Secondary structure of mouse 28S rRNA and general models for the folding of the large RNA in eukaryotes. Nucleic Acids Res 12:4259–4279
Perasso R, Baroin A, Qu LH, Bachelleire JP, Adoutte A (1989) Origin of the algae. Nature 339:142–144
Preparata RM, Meyer EB, Preparata FP, Simon EM, Vossbrinck CR, Nanney DL (1989) Ciliate evolution: the ribosomal phylogenies of the tetrahymenine ciliates. J Mol Evol 28:427–441
Preparata RM, Beam CA, Himes M, Nanney DL, Meyer EB, Simon EM (1992) Crypthecodinium and Tetrahymena: an exercise in comparative evolution. J Mol Evol 34:209–18
Saitou N, Nei N (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Salim M, Maden BE (1981) Nucleotide sequence of Xenopus laevis ribosomal RNA inferred from gene sequence. Nature 291:205–208
Sanger F, Nicklen FS, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Scholin CA, Anderson DM (1993) Population analysis of toxic and nontoxic Alexandrium species using ribosomal RNA signature sequences. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, New York, pp 95–102
Scholin CA, Anderson DM (1994) Identification of groups and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). RFLP analysis of short subunit rRNA genes. J Phycol 30:744–754
Silva ES (1982) Relationship between dinoflagellates and intracellular bacteria. In: Tevring T, Hoppe H (eds) Marine algae in pharmaceutical science. W de Gruyter & Co, New York, Vol 2, pp 269–288
Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383–1387
Taylor F (1980) On dinoflagellate evolution. Biosystems 13:65–108
Taylor FIR (1993) The species problem and its impact on harmful phytoplankton studies. In: Smayda TJ, Shimizu Y (eds) Toxic marine dinoflagellates. Elsevier, New York, pp 81–86
Williams GL (1978) Dinoflagellates acritarchs and tasmanids. In: Haq BH, Boersme A (eds) Introduction to marine micropaleontology. Elsevier North-Holland, New York, pp 293–326
Wolters J (1991) The troublesome parasites—molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems 25:75–83
Wood AM, Leathan T (1992) The species concept in phytoplankton ecology. J Phycol 28:723–729
Author information
Authors and Affiliations
Additional information
Correspondence to: J. M. Bautista
Rights and permissions
About this article
Cite this article
Zardoya, R., Costas, E., López-Rodas, V. et al. Revised dinoflagellate phylogeny inferred from molecular analysis of large-subunit ribosomal RNA gene sequences. J Mol Evol 41, 637–645 (1995). https://doi.org/10.1007/BF00175822
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00175822