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.)

K. Lindberg, Ø. Moestrup and N. Daugbjerg. 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: 416–440. Sediment samples were collected from a small pond in southern Sweden. Several cysts from the samples germinated into clonal cultures, identified as Woloszynskia coronata (Wolosz.) R.H. Thompson 1951. They were compared with other species of Woloszynskia established in culture, using scanning electron microscopy, transmission electron microscopy, partial large subunit ribosomal DNA (LSU rDNA) and morphology of the resting cysts. Significant differences were found, and we conclude that the genus Woloszynskia as presently circumscribed is artificial, and comprises at least four genera. In this first paper we transfer W. coronata to a new genus; Tovellia gen. nov., type species: Tovellia coronata (Wolosz.) comb. nov. Previous studies on ultrastructure and DNA sequencing referring to Woloszynskia coronata are based on W. coronata var. glabra, which is raised to species level as Tovellia glabra sp. nov. Other species included in the new genus are Tovellia apiculata (basionym Woloszynskia apiculata Stosch) and Tovellia stoschii (basionym Woloszynskia stoschii R. Shyam & Sarma). Two identical cultures presently identified as Woloszynskia limnetica Bursa (from University of Washington Culture Collection, Seattle) and W. pseudopalustris (J. Schiller) Kiselev [from Culture Collection of Algae at the University of Cologne, Cologne] differ from Tovellia in LSU rDNA sequences and in cyst type and are transferred to Jadwigia gen. nov., as J. applanata sp. nov. The most striking feature of Tovellia and Jadwigia is the anatomy of the eyespot, which is extraplastidial, and composed of nonmembrane bound lipid globules. This type of eyespot is also present in Katodinium campylops (T.M. Harris) A.R. Loebl., a species undoubtedly related to Tovellia, and in ‘Glenodinium sp.’ sensu Kreimer 1999, and together they form a distinct family, Tovelliaceae fam. nov.

[1]  Ø. Moestrup,et al.  On the freshwater dinoflagellates presently included in the genus Amphidinium, with a description of Prosoaulax gen. nov. , 2005 .

[2]  G. Flaim,et al.  Reinterpretation of the dinoflagellate ‘Glenodinium sanguineum’ in the reddening of Lake Tovel, Italian Alps , 2004 .

[3]  S. Murray,et al.  A new genus of athecate interstitial dinoflagellates, Togula gen. nov., previously encompassed within Amphidinium sensu lato: Inferred from light and electron microscopy and phylogenetic analyses of partial large subunit ribosomal DNA sequences , 2004 .

[4]  Shauna A. Murray,et al.  AMPHIDINIUM REVISITED. I. REDEFINITION OF AMPHIDINIUM (DINOPHYCEAE) BASED ON CLADISTIC AND MOLECULAR PHYLOGENETIC ANALYSES 1 , 2004 .

[5]  G. Hansen,et al.  Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains , 2003 .

[6]  A. Rochon,et al.  Morphological and LSU rDNA sequence variation within the Gonyaulax spinifera-Spiniferites group (Dinophyceae) and proposal of G. elongata comb. nov. and G. membranacea comb. nov. , 2003 .

[7]  C. Lovejoy,et al.  Bipolar distribution of the cyst-forming dinoflagellate Polarella glacialis , 2003, Polar Biology.

[8]  Ø. Moestrup,et al.  Ultrastructural study of the type species of Peridiniopsis, Peridiniopsis borgei (Dinophyceae), with special reference to the peduncle and flagellar apparatus , 2002 .

[9]  Hanne Kaas,et al.  Effects of nutrient-limitation and irradiance on marine phytoplankton pigments , 2002 .

[10]  Ø. Moestrup,et al.  Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates , 2000 .

[11]  G. Kreimer.  Reflective properties of different eyespot types in dinoflagellates. , 1999, Protist.

[12]  G. Procaccini,et al.  POLARELLA GLACIALIS, GEN. NOV., SP. NOV. (DINOPHYCEAE): SUESSIACEAE ARE STILL ALIVE! , 1999 .

[13]  Ø. Moestrup,et al.  TAXONOMY AND ULTRASTRUCTURE OF A FRESHWATER, HETEROTROPHIC AMPHIDINIUM (DINOPHYCEAE) THAT FEEDS ON UNICELLULAR PROTISTS , 1998 .

[14]  C. Bolch.  The use of sodium polytungstate for the separation and concentration of living dinoflagellate cysts from marine sediments , 1997 .

[15]  D. Caron,et al.  Molecular phylogeny of symbiotic dinoflagellates from planktonic foraminifera and radiolaria. , 1996, Molecular biology and evolution.

[16]  K. Roberts,et al.  GENERAL ULTRASTRUCTURE AND FLAGELLAR APPARATUS ARCHITECTURE OF WOLOSZYNSKIA LIMNETICA (DINOPHYCEAE) , 1995 .

[17]  K. Roberts,et al.  Flagellar apparatus transformation and development in Prorocentrum micans and P. minimum (Dinophyceae) , 1995 .

[18]  L. Thinh,et al.  Gymnodinium linucheae sp. nov.: The dinoflagellate symbiont of the jellyfish Linuche unguiculata , 1995 .

[19]  D. Anderson,et al.  IDENTIFICATION OF GROUP‐ AND STRAIN‐SPECIFIC GENETIC MARKERS FOR GLOBALLY DISTRIBUTED ALEXANDRIUM (DINOPHYCEAE). II. SEQUENCE ANALYSIS OF A FRAGMENT OF THE LSU rRNA GENE 1 , 1994 .

[20]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[21]  L. Wilcox.  MULTILAYERED STRUCTURES (MLSs) IN TWO DINOFLAGELLATES, KATODINIUM CAMPYLOPS AND WOLOSZYNSKIA PASCHERI 1 , 1989 .

[22]  G. Lenaers,et al.  Dinoflagellates in evolution. A molecular phylogenetic analysis of large subunit ribosomal RNA , 1989, Journal of Molecular Evolution.

[23]  K. Roberts,et al.  COMPARATIVE ANALYSES OF THE DINOFLAGELLATE FLAGELLAR APPARATUS. I. WOLOSZYNSKIA SP. 1 , 1989 .

[24]  J. Skvarla,et al.  Occurrence, Growth, and SEM Portrait of Woloszynskia reticulata Thompson (Dinophyceae) , 1980 .

[25]  J. Sherley,et al.  Observations on the theca of the motile phase of free-living and symbiotic isolates of Zooxanthella microadriatica (Freudenthal) comb.nov. , 1979, Journal of the Marine Biological Association of the United Kingdom.

[26]  Y. Sarma,et al.  Woloszynskia stoschii andGymnodinium indicum, two new freshwater dinoflagellates from India: Morphology, reproduction and cytology , 1975, Plant Systematics and Evolution.

[27]  H. Stosch.  Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates, Gymondinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. , 1973 .

[28]  J. Dodge,et al.  The encystment of a freshwater dinoflagellate: A light and electron-microscopical study , 1972 .

[29]  R. Crawford,et al.  A fine‐structural survey of dinoflagellate pyrenoids and food‐reserves , 1971 .

[30]  A. R. Loeblich.  Index to the genera, subgenera, and sections of the Pyrrhophyta , 1970 .

[31]  M. Montgomery,et al.  A NEW FRESHWATER DINOFLAGELLATE , 1966 .

[32]  A. Bursa.  The Freshwater Dinoflagellate Woloszynskia limnetica n. sp. Membrane and Protoplasmic Structures , 1958 .

[33]  23. Otto Suchlandt: Dinoflagellaten als Erreger von rotem Schnee , 1916, Berichte der Deutschen Botanischen Gesellschaft.

[34]  G. Lenaers,et al.  A molecular phylogeny of dinoflagellate protists (Pyrrhophyta) inferred from the sequence of 24S rRNA divergent domains D1 and D8 , 2005, Journal of Molecular Evolution.

[35]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[36]  Yves Van de Peer,et al.  The European Large Subunit Ribosomal RNA database , 2000, Nucleic Acids Res..

[37]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[38]  H. Ettl,et al.  Süsswasserflora von Mitteleuropa , 1985 .

[39]  H. Netzel,et al.  3 – Dinoflagellate Cell Cortex , 1984 .

[40]  J. Dodge.  The functional and phylogenetic significance of dinoflagellate eyespots. , 1983, Bio Systems.

[41]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .

[42]  G. Dürr.  Elektronenmikroskopische Untersuchungen am Panzer von dinoflagellaten: I. Gonyaulax polyedra , 1979 .

[43]  G. Dürr.  Elektronenmikroskopische untersuchungen am panzer von dinoflagellaten: II. Peridinium cinctum , 1979 .

[44]  D. Hibberd,et al.  Observations on the Cytology and Ultrastructure of the New Algal Class, Eustigmatophyceae , 1972 .

[45]  R. Crawford,et al.  A survey of thecal fine structure in the Dinophyceae , 1970 .

[46]  B. Párducz,et al.  Ciliary movement and coordination in ciliates. , 1967, International review of cytology.

[47]  A. J. Schilling.  Die Süsswasser-Peridineen , 1891 .

[48]  F. Stein.  Der Organismus der Infusionsthiere , 1859 .

[49]  C. G. Ehrenberg.  Beiträge zur Kenntniss der Organisation der Infusorien und ihrer geographischen Verbreitung, besonders in Sibirien. , 1830 .