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Molecular Phylogeny of Dinophysoid Dinoflagellates: the Systematic Position of Oxyphysis Oxytoxoides and the Dinophysis Hastata Group (Dinophysales, Dinophyceae)1

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Molecular Phylogeny of Dinophysoid Dinoflagellates: the Systematic Position of Oxyphysis Oxytoxoides and the Dinophysis Hastata Group (Dinophysales, Dinophyceae)1 J. Phycol. 47, 393–406 (2011) Ó 2011 Phycological Society of America DOI: 10.1111/j.1529-8817.2011.00964.x MOLECULAR PHYLOGENY OF DINOPHYSOID DINOFLAGELLATES: THE SYSTEMATIC POSITION OF OXYPHYSIS OXYTOXOIDES AND THE DINOPHYSIS HASTATA GROUP (DINOPHYSALES, DINOPHYCEAE)1 Fernando Go´mez2 Universite´ Lille Nord de France, Laboratoire d¢Oce´anologie et Ge´osciences, CNRS UMR 8187, Station Marine de Wimereux, 28 Av. Foch, 62930 Wimereux, France Purificacio´nLo´pez-Garcı´a and David Moreira Unite´ d’Ecologie, Syste´matique et Evolution, CNRS UMR 8079, Universite´ Paris-Sud, Baˆtiment 360, 91405 Orsay Cedex, France The dinophysoid dinoflagellates are currently Abbreviations: bp, base pairs; BV, bootstrap value; divided into three families: Amphisoleniaceae, Dino- s.s., sensu stricto physaceae (mainly Dinophysis Ehrenb. and Phalacro- ma F. Stein), and Oxyphysaceae, the latter including only one member, Oxyphysis oxytoxoides Kof. Phalac- The dinophysoids (see Appendix S1 in the sup- roma has been recently reinstated separately from plementary material for a note on the spelling of Dinophysis, and its amended description is currently the supergeneric names derived from Dinophysis restricted to cells whose epithecae were large but authored by P. C. Silva) are a well-defined order of <1 ⁄ 4 of the cell length. With the aim of improving marine dinoflagellates with 280 recognized species the phylogeny of Dinophysales, we obtained 54 new classified in three families: Amphisoleniaceae, Dino- SSU rRNA gene sequences of 28 species. Taxon-rich physaceae, and Oxyphysaceae (Fensome et al. 1993, SSU rDNA phylogenetic analysis showed that Dino- Steidinger and Tangen 1997, Go´mez 2005). The physales split into two major clades, one containing cells are laterally compressed with a reduced epit- the Amphisoleniaceae (Amphisolenia F. Stein–Tripo- heca and a larger hypotheca consisting of two large solenia Kof.) and the other containing the Dinophys- plates united by a sagittal serrate suture with a zig- aceae. The latter are divided into two well- zag course (Kofoid and Skogsberg 1928, Tai and supported sister groups, the Dinophysaceae sensu Skogsberg 1934, Abe´ 1967a,b,c, Balech 1967). stricto (s.s.) (Dinophysis, Ornithocercus F. Stein, Histi- According to Balech (1980), the dinophysoids are oneis F. Stein) and, tentatively, a separate family for also unusual among the thecate dinoflagellates in the clade of the type and most of the Phalacroma that, despite their extreme morphological specializa- species. Based on combined phylogenies of new tion, their plate arrangement and number are more SSU rDNA and available LSU rDNA data, O. oxytoxo- or less similar in all species and genera, except for ides (elongated epitheca, >1 ⁄ 4 of the cell length) the genera Amphisolenia F. Stein and Citharistes F. branched with a strong support with the type of Stein. Phalacroma. We therefore propose Phalacroma oxy- The dinophysoid genus Phalacroma F. Stein was toxoides comb. nov. for O. oxytoxoides. Our SSU morphologically separated from Dinophysis Ehrenb. rDNA phylogeny also suggests that the assumed high based mainly on differences in epithecal elevation intraspecific variability of Dinophysis hastata F. Stein (Stein 1883, Kofoid and Skogsberg 1928). Dinophysis hides a number of cryptic species. According to species have a reduced epitheca, and their anterior their distinct phylogenetic placement, the forms cingular list forms a funnel-shaped fan, whereas D. hastata f. phalacromides Jørg. and D. hastata Phalacroma species have a visible epitheca above an f. uracanthides Jørg. should be erected at the species anterior cingular list that is typically narrow and level. We propose for them the names Dinophysis directed horizontally. However, detailed tabulation phalacromoides comb. nov. and Dinophysis uracan- studies, especially at the sulcus level, did not show thoides comb. nov. any significant difference between Dinophysis and Key index words: Amphisolenia; cryptic species; Phalacroma. For this reason and because of their Dinophysiaceae; Dinophysiales; dinophysioid intergrading morphology, Abe´ (1967b) and Balech dinoflagellate; Histioneis; Ornithocercus; Oxyphysi- (1967) transferred Phalacroma species into Dinophy- aceae; Phalacroma; SSU and LSU rDNA phylogeny sis. More recently, and based on molecular data, Handy et al. (2009) and Hastrup Jensen and Daugb- jerg (2009) observed a deep separation between spe- 1Received 21 March 2010. Accepted 6 October 2010. cies of the Phalacroma and Dinophysis lineages. 2 Author for correspondence: e-mail fernando.gomez@fitoplancton. Accordingly, Hastrup Jensen and Daugbjerg (2009) com. 393 394 FERNANDO GO´ MEZ ET AL. reinstated the genus Phalacroma and amended its chambers at ·100 magnification with an inverted microscope description, which is currently restricted to cells (Nikon Eclipse TE200, Nikon Inc., Tokyo, Japan) and was whose epithecae are large but having <1 ⁄ 4 of the photographed at ·200 or ·400 magnification with a digital camera (Nikon Coolpix E995). Sampling continued from cell length. This definition excluded some Phalacro- October 2008 to August 2009 in the surface waters of the port ma species with a prominent epitheca (Phalacroma (depth of 2 m) of Banyuls sur Mer, France (42°28¢50¢¢ N, apicatum Kof. et Skogsb. and Phalacroma cf. argus F. 3°08¢09¢¢ E), and from September 2009 to February 2010 in the Stein) that branched within the other Dinophysa- Bay of Villefranche sur Mer, Ligurian Sea. For the latter ceae clade (Dinophysis, Ornithocercus, Histioneis, location, sampling was performed at a long-term monitoring Citharistes). Hastrup Jensen and Daugbjerg (2009) site called Point B (43°41¢10¢¢ N, 7°19¢00¢¢ E; water column divided the Dinophysales into three major clades: depth 80 m) and sporadically at Point C (43°40¢ N, 7°19¢00¢¢ E; water column depth 600 m). Sampling in double one basal clade for Amphisolenia; another clade for oblique angle was performed with a custom-made conical species with the classical Phalacroma outline, includ- phytoplankton net (53 lm mesh size, 54 cm diameter and ing the type species of Phalacroma; and a third clade 280 cm length). The samples were prepared with the same with a variety of subclades (Ornithocercus and Cithar- procedure described above. The specimens were observed with istes, Histioneis, some Phalacroma species, and several an inverted microscope (Olympus IX51; Olympus Inc., Tokyo, Dinophysis clusters). These authors reported that Japan) and photographed with an Olympus DP71 digital camera. The specimen of O. oxytoxoides was collected by using Dinophysis was polyphyletic, as it formed four sepa- a strainer with netting of 20 lm aperture from the surface rate clades. This indicated that besides Dinophysis waters of the E´tang de Thau at Se`te (43°24¢48¢¢ N, 3°41¢11¢¢ E) s.s., Dinophysis should be divided into at least three and analyzed following the procedure described above. E´tang additional new genera. de Thau is a large semienclosed coastal lagoon on the French These molecular phylogenetic studies still sup- Mediterranean coast (75 km2, mean depth 4.5 m) under the ported the division of the Dinophysales into three influence of freshwater inputs. In addition, open-water samples were collected from the BOUM (Biogeochemistry from the families: Amphisoleniaceae, Dinophysaceae, and Oligotrophic to the Ultra-oligotrophic Mediterranean) cruise Oxyphysaceae (Hastrup Jensen and Daugbjerg in the Mediterranean Sea between the Gulf of Lions and 2009). The latter is restricted to the monotypic Cyprus. Ten liters was collected from the surface with a bucket genus Oxyphysis Kof., which has a peridinioid and filtered by using a strainer of 20 lm netting aperture. The appearance, suggesting a possible link between din- retained material was fixed with absolute ethanol to a final ophysoids and peridinioids (Kofoid 1926). Nonethe- concentration of 50% concentrate seawater sample and 50% less, based on morphological traits, Abe´ (1967a) ethanol. At the laboratory, the ethanol sample was examined following the procedure described above. In all cases, each suggested that Oxyphysis might have a common specimen was micropipetted individually with a fine capillary ancestor with the Amphisolenia-Triposolenia line, leav- into a clean chamber and washed several times in serial drops ing its phylogenetic relationship unresolved. of 0.2 lm filtered and sterilized seawater (live specimens from With the aim of improving the phylogeny of coastal waters) or ethanol (ethanol prefixed specimens from Dinophysales, we obtained 54 new SSU rRNA gene open waters). Finally, the specimen was deposited into a sequences of 28 dinophysoid species from several 0.2 mL tubes (ABgene; Thermo Fisher Scientific Inc., Cour- taboeuf, France) filled with several drops of absolute ethanol. dinophysoid genera, including Amphisolenia, Tripo- The sample was kept at room temperature and in darkness solenia, and Oxyphysis as well as the type of Phalacro- until the molecular analysis could be performed. ma. Their phylogenetic analysis together with that of PCR amplification of SSU rRNA genes and sequencing. The combined available LSU rDNAs showed that specimens fixed in ethanol were centrifuged (Eppendorf, Dinophysales split into two major clades, the Amph- Hamburg, Germany) gently for 5 min at 504g. Ethanol was isoleniaceae (Amphisolenia-Triposolenia) and the then evaporated in a vacuum desiccator and single cells were resuspended directly in 25 lL of Ex TaKaRa buffer (TaKaRa, Dinophysaceae, the latter including two well-sup- distributed by Lonza
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