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Dinophyceae), with Notes on Feeding Behavior and the Description of the Flagellar Base Area of a Planozygote1

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Dinophyceae), with Notes on Feeding Behavior and the Description of the Flagellar Base Area of a Planozygote1 J. Phycol. 42, 434–452 (2006) r 2006 Phycological Society of America DOI: 10.1111/j.1529-8817.2006.00195.x 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 PLANOZYGOTE1 Anto´nio J. Calado,2 Sandra C. Craveiro Departamento de Biologia, Universidade de Aveiro, P-3810-193 Aveiro, Portugal Niels Daugbjerg and Øjvind Moestrup Department of Phycology, Biological Institute, University of Copenhagen, Øster Farimagsgade 2D, DK-1353 Copenhagen K, Denmark A small, freshwater dinoflagellate with an incom- Markov chains; MP, maximum parsimony; NJ, plete cingulum, identified as Esoptrodinium gemma neighbor-joining; PP, posterior probabilities; PSC, Javornicky´ (5Bernardinium bernardinense sensu au- peduncular striated collar; SRC, striated root con- ctt. non sensu Chodat), was maintained in mixed nective (TSR to LMR); TB, transverse basal body; culture and examined using light and serial section TMR, transverse microtubular root; TMRE, TMR TEM. Vegetative flagellate cells, large cells with two extension; TSR, transverse striated root; TSRM, longitudinal flagella (planozygotes), and cysts were transverse striated root microtubule; VR, ventral examined. The cells displayed a red eyespot near ridge the base of the longitudinal flagellum, made of two or three layers of pigment globules not bounded by a membrane. Yellow-green, band-shaped chloro- plasts, bounded by three membranes and contain- The organism used in this study is a naked dino- ing lamella with three thylakoids, were present in flagellate that would be readily identified as Bern- both flagellate cells and cysts. Most cells had food ardinium bernardinense Chodat by recent dinoflagellate vacuoles, containing phagotrophically ingested floras (Starmach 1974, Matvienko and Litvinenko chlamydomonads or chlorelloid green algae; inges- 1977, Popovsky´ and Pfiester 1990). In his original de- tion occurred through the ventral area, involving a scription of B. bernardinense, Chodat (1924, pp. 40–41) thin pseudopod apparently driven by the peduncle. mentioned the incomplete cingulum, which disap- The pusule was tubular, with numerous diverticula peared on the dorsal side, and the absence of chloro- in its distal portion, and opened into the longitudi- plasts and of a distinct sulcus. The new genus nal flagellar canal. Three roots were associated with Bernardinium was compared with Hemidinium F. Stein, each pair of flagellar bases, both in vegetative cells from which it was distinguished mainly by the well-de- and in a planozygote. The longitudinal microtubu- fined sulcus in the two Hemidinium species previously lar root bifurcated around the longitudinal basal described. Although Hemidinium was originally de- body. The planozygote contained a single peduncle scribed as unarmored (Stein 1878, pp. 91 and 97, and associated structures, and a single transverse 1883, pl. 2, Figs. 23–26), the type species is currently flagellar canal with the two converging transverse regarded as a thecate form with thin plates (Popovsky´ flagella. Using two ciliates as outgroup species, and Pfiester 1990). The smaller of the two cell portions phylogenetic analyses based on maximum parsimo- delimited by the incomplete cingulum was placed on ny, neighbor-joining and posterior probability (Bay- top in Chodat’s (1924) original drawings; his descrip- esian analysis) supported a clade comprising tion shows he regarded this as the epicone (‘‘parte di- Esoptrodinium, Tovellia, and Jadwigia. midia superiore’’). Schiller (1935) reinterpreted the orientation of the cell and reproduced Chodat’s draw- Key index words: Bernardinium bernardinense; ings with the longitudinal flagellum emerging down- Dinophyceae; Esoptrodinium gemma; eyespot; flag- ward, pointing out that, with this orientation, the ellar apparatus; LSU rDNA; phagotrophy; phylo- cingulum is directed toward the right side of the geny; planozygote; ultrastructure body. Huber-Pestalozzi (1950, p. 164) regarded Abbreviations: BA, Bayesian analysis; BB, basal the species as imperfectly described and transferred body; LB, longitudinal basal body; LMR, longitu- it to Hemidinium. dinal microtubular root; MCMC, Monte Carlo The second report of an organism identified as B. bernardinense is that of Thompson (1951); the cells de- scribed resembled Chodat’s (1924) in both size and 1Received 31 August 2005. Accepted 22 December 2005. general morphology, but displayed the orientation of 2Author for correspondence: e-mail [email protected]. cingulum and transverse flagellum that is common in 434 ESOPTRODINIUM ULTRASTRUCTURE AND PHYLOGENY 435 dinoflagellates, i.e. to the cell’s left. A third and more Light microscopy. The morphology and swimming mode of detailed description of an organism under this name cells were recorded with a Sony Video Cassette Recorder comes from Javornicky´ (1962), whose specimens show SLV-825 (Sony Corporation, Tokyo, Japan). Micrographs the same orientation as those of Thompson (1951). were taken with a Leica DMLB light microscope (Leica Mi- crosystems, Wetzlar, Germany) with differential interference Javornicky´ (1962) considered the orientation shown in contrast. Observations of the feeding process were made in Chodat’s (1924) drawings to be an error, and Conrad’s microchambers prepared by attaching a rectangular Plasti- (1939) comment that Bernardinium is an inverse Hemi- cine support onto a 24 mm 32 mm coverslip, placing a dinium to be therefore unjustified. Wawrik (1983) re- drop of the culture in the midÂdle of the coverslip, inverting ported the species, with the name H. bernardinense, it over a slide, and pressing along the edges. from a pond in Lower Austria (Wawrik 1983, Fig. 1g); Electron microscopy. Cultured material was fixed in a mix- ture of 1% glutaraldehyde and 0.25% osmium tetroxide (final a single cell is depicted with the cingulum extending to concentrations) in 0.1 M phosphate buffer, pH 7.2, for 15 min the viewer’s left, although the orientation of the cell at room temperature. After centrifugation, the pellet was was not mentioned and a transverse flagellum was not rinsed in the same buffer, embedded in 1.5% agar, and post- seen. Popovsky´ (1990) reported B. bernardinense with a fixed for approximately 1 h in 1% buffered osmium tetroxide left hand orientation of the cingulum from ponds in at room temperature. Rinsing in buffer and water, and de- Czechoslovakia, although his drawings show cells with hydration through a graded ethanol series up to 70%, was performed at 41 C. After the final dehydration steps in a different general morphology and a well-marked ethanol and propylene oxide, at room temperature, the ma- sulcus, making the identification somewhat doubtful. terial was embedded in Epon. Single cells of E. gemma, which Javornicky´ (1997) reported a flagellate with the gen- were greatly outnumbered by green flagellates and other eral features ascribed to B. bernardinense from a little prey organisms, were singled out in the blocks with the light freshwater pond in Ru¨gen Island, North-East Germa- microscope and sectioned with a diamond knife on a Reichert ny and both the cingulum and the transverse flagellum Ultracut E (Leica Microsystems, Wetzlar, Germany). The sec- oriented toward the cell’s right; upon comparison with tions were picked up with slot grids, placed on Formvar film, contrasted with uranyl acetate and lead citrate, and exam- Chodat’s (1924) drawings, Javornicky´ (1997) conclud- ined with a JEOL JEM 1010 electron microscope (JEOL Ltd., ed that this German population represented B. bernar- Tokyo, Japan). Serial sections from two vegetative cells, a dinense in the original sense of Chodat. Considering the planozygote and a cyst were examined. nearly mirror-symmetrical populations studied by PCR amplification. Using a capillary pipette three cells of both Thompson (1951) and Javornicky´ (1962) to rep- E. gemma from a culture grown on a species of Chlamydomonas resent not only a different species, but a different ge- were transferred through three rinses in double-distilled wa- ter and placed in the same 0.5 mL PCR tube containing 8 mL nus, Javornicky´ (1997) described the new genus of double-distilled water. Amplification of partial LSU rDNA Esoptrodinium, with the type species Esoptrodinium gem- using the forward primer ‘‘D1F’’ (Scholin et al. 1994) and the ma based on the population described by Javornicky´ reverse dinoflagellate specific primer ‘‘Dino-ND’’ (Hansen (1962) under the name B. bernardinense. The organism and Daugbjerg 2004) resulted in a PCR product of approx- studied herein has a left-oriented cingulum and trans- imately 1800 bp in length. The temperature profile used for verse flagellum and is therefore identifiable as E. gem- PCR amplification and subsequent determination of the nu- ´ clear-encoded LSU rDNA sequence (GenBank DQ289020) ma Javornicky. was established as described previously (Hansen et al. 2003, The organization of the flagellar base area has been Hansen and Daugbjerg 2004). studied in detail for over 20 species of dinoflagellates Sequence alignment. The LSU rDNA sequence of Eso- (Calado and Moestrup 2002, Hansen and Daugbjerg ptrodinium was determined in both directions and added to 2004). Although swimming dinoflagellate cells result- the same data matrix recently compiled by Moestrup et al. ing from the fusion of gametes are known to have two (2006) to elucidate the phylogeny of woloszynskioid dino- longitudinal flagella and the parallel arrangement of flagellates. The data matrix analyzed here comprised
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