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Description of a New Freshwater Bloom-Forming Dinoflagellate with a Diatom Endosymbiont, Peridiniopsis Minima Sp

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Description of a New Freshwater Bloom-Forming Dinoflagellate with a Diatom Endosymbiont, Peridiniopsis Minima Sp Algological Studies 145/146 (2014), p. 119–133 Article Published online May 2014 Description of a new freshwater bloom-forming dinoflagellate with a diatom endosymbiont, Peridiniopsis minima sp. nov. (Peridiniales, Dinophyceae) from China Qi Zhang, Guoxiang Liu* & Zhengyu Hu State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydro- biology, Chinese Academy of Sciences, Wuhan 430072, P.R. China With 4 figures and 2 tables Abstract: A new freshwater dinoflagellate, Peridiniopsis minima Zhang, Liu et Hu sp. nov. (Peridiniales, Dinophyceae), from the Jiulongjiang River, Fujian Province, China, is described. The dinoflagellate can form serious brown freshwater blooms in the river. The cell is very small and the plate formula is: Po, x, 3', 1a, 6'', 5c, 4s (?), 5''', 2''''. The dinoflagellate is characterized by the presence of a eukaryotic endosymbiotic alga. The dinoflagellate cell possesses two dif- ferent types of nuclei: a dinokaryon and a eukaryotic nucleus from the diatom endosymbiont. Our molecular analyses based on SSU, LSU and ITS rDNA sequences revealed that these fresh- water diatom-harbouring Peridiniopsis species forms a strongly supported subclade, very dis- tant from Peridiniopsis borgei, which is the type species of Peridiniopsis, and distinctively separated from marine diatom-harbouring dinoflagellates. The phylogenetic analyses based on endosymbiont SSU rDNA sequences indicate that the diatom endosymbionts of Peridiniopsis species are closely related to centric diatoms, such as Discostella and Cyclotella. Keywords: Peridiniopsis, Peridiniopsis minima, Dinoflagellate, Phylogeny, Diatom endosym- biont Introduction The cosmopolitan genus Peridiniop sis was established by Lemmermann (1904, p. 134), wi th P. borgei Lemmermann as t he type species. Peridiniopsis is the second largest genus of thecate, freshwater dinoflagellate (ca. 20 species) (Popovský & Pfie- ster 1990). According to the revision by Bourrelly (1968 ), this genus differs from Peridinium in the number of the anterior intercalary plates (0a or 1a in Peridiniopsis, *Corresponding author: [email protected] © E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart, Germany www.schweizerbart.de DOI: 10.1127/1864-1318/2014/0159 1864-1318/0159 $ 3.75 120 Qi Zhang, Guoxiang Liu & Zhengyu Hu whereas 2a or 3a in Peridinium). Species of Peridiniopsis have the plate tabulation 3-5', 0-1a, 6-8'', 5''', 2'''' (Bourrelly 1968). However, this taxonomic criterion seems to be an oversimplification. Based on morphological and molecular evidence, some Peridiniopsis species have been transferred to new genera in recent years (e.g. Bol- tovskoy 1999, Calado et al. 2009). Several dinoflagellates are known to possess two different types of nuclei: a di- nokaryon and an ordinary eukaryotic nucleus from an endosymbiont (reviewed by Schnepf & Elbrächter 1999). Endosymbionts have been observed in Durinskia baltica (Levander) Carty et Cox [= Peridinium balti cum (Levander ) Lemmermann] by Tomas & Cox (1973), in Durinskia capensis Pienaar, Sakai et Horiguchi by Pienaar et al. (2007), in Kryptoperidinium foliaceum (Stein) Lindeman [= Peridinium foliaceum (Stein) Biecheler] by Dodge (1983), Jeffrey & Vesk (1976) and Kempton et al. (2002), in Peridinium quinquecorne Abé by Horiguchi & Pienaar (1991), in D inothrix para- doxa Pascher by Horiguchi & Chihara (1993), for Gymnodinium quadrilobatum Horiguchi et Pienaar by Horiguchi & Pienaar (1994) and in Galeidinium rugatum Tamura et Horiguchi by Tamura et al. (2005). Some Peridiniopsis species a lso pos- sess an endosymbiotic diatom or diatom-like alga. Takan o et al. (2008) revealed t hat Peridiniopsis kevei Grigorszky et Vasas and P. penardii (Lemmermann) Bourrelly are two diatom-ha rboring dinoflagellates. Zhang et al. (2011) r ecently described a new variety of a freshwater bloom-forming dinoflagellate, Peridiniopsis penardii (Lem- mermann) Bourrelly var. robusta Q. Zhang, G.X. Liu et Z.Y. Hu, from China with a similar type of endosymbiont. In the summer of 2011, an extensive algal bloom was observed in Jonglongjiang River, Fujian Province, China. We investigated the causative organism and found that the dense bloom caused by a small unidentified peridinioid dinoflagellate. After examining its morphological characteristics and thecal plate arrangement, we con- sidered it to represent a new species. Based on the morphological and molecular evi- dence, we demonstrated the phylogenetic affinities of this new dinoflagellate with a similar type of endosymbiont. Material and methods Collection and preservation Plankton samples were collected from Jiulongjiang River, Fujian Province, China (117°15 '14''E, 25° 12'35'' N) by Sen Li n, on 16 Augus t 201 1 at the time of bloom formation. Samples were preserved in 10 % formalin and 90 % ethanol. Ethanol-fixed samples were frozen at –20°C until analysis. Morphospecies identification For observation of the thecal plates, formalin-fixed cells were sterilized with 0.1 % Fluorescent Brightener 28 (Sigma, UK) (Fritz & Triemer 1985) and observed using Description of a new dinoflagellate with a diatom endosymbiont 121 epifluorescence microscopy (EFM) (Leica DM5000B, Germany). Ethidium bromide (EB)-stained cells were prepared by a common method for observation of nuclei (Liu et al. 2008). We also observed cells for differential interference contrast (DIC) and phase contrast (PC) microscopy using a Leica DM5000B microscope. Micrographs were taken with a Leica DFC 320 digital camera. Cells isolation and DNA extraction About 20 cells were isolated from ethanol-fixed samples under an inverted micro- scope for each PCR reaction (Olympus CKX41, Japan). Individual dinoflagellate cells were then placed in a 200 μL PCR tube. The DNA extraction wa s performed by treating the cells with Proteinase K (pK) which is commonly used in molecular biol- ogy to digest protein and remove contaminations from preparations of nucleic acids. Proteinase K (1 μL 200 μg/ml) was then added, and the tubes were maintained at 55°C for 50 minutes. Samples were then incubated at 95°C for a further 10 minutes to inac- tivate the proteinase K and facilitate DNA denaturation. The tubes were then cooled at 4°C in preparation for PCR amplification (Ki et al. 2005). Finally, the elution volume of DNA used in the PCR was about 5 μL. Single-cell PCR and sequencing The sequences of nuclear-encoded rDNA (SSU, LSU and ITS[ITS1/5.8S/IT S2]) and plastid-encoded 23S rDNA from the dinoflagellate and SSU rDNA from the endo- symbiont nucleus were determined usi ng the sing-cell PCR method. The details of this method are described by Zhang et al. (2011). Polymerase chain reaction condi- tions for partial 23S rDNA amplifications using primers have been described previ- ously (Zhang et al. 2000). The methods of PCR amplifications of nuclear-encoded rDNA and endosymbiontic SSU rDNA were the same as described by Zhang et al. (2011) . All amplicons were sequenced from both s ides using PCR primers. The PCR products were analyzed on an ABI 3700 sequencer (Applied Biosystems, USA). The sequences were deposited in GenBank under the Accession numbers: JQ639752, JQ639767, JQ639770, JX027617, and JX141779. Phylogenetic analyses The SSU, LSU, ITS and endosymbiont SSU sequences w ere downloaded from Gen- Bank. Perkins us marinus was used as an outgroup in the SSU, LSU and ITS phylo- genies. Bolidomonas mediterranea was used as an outgroup in the endosymbiont SSU phylogeny. The SSU, LSU, ITS and endosymbiont SSU consisted of 49 sequences with 1599 characters, 51 sequences with 529 characters, and 38 sequences with 506 characters, 40 sequences with 1304 characters, respectively. After the elimination of identical and apparently erroneous sequences, we created four sets of alignments us- ing Clustal X (v1.8) (Thompson et al. 1997) and Bioedit (v7.0.9.1) (Hall 1999). We 122 Qi Zhang, Guoxiang Liu & Zhengyu Hu analyzed conversion/transversion and genetic distances using MEGA (v4.0.0.4103) (Tamura et al. 2007). The phylogenies were estimated using Maximum Likelihood(ML) and Bayesian Inference (BI) as implemented in Paup 4.0* (v4.0b10) (Swofford 2002) and MrBayes (v3.1.2) (Huelsenbeck & Ronquist 2001). The program Modeltest (v3.07) (Posada & Crandall 1998) was used to explore the model of sequence evolution that best fits the data set by the hierarchical likelihood ratio test (hLRT) (Huelsenbeck & Cran- dall 1997). In ML analyses, a heuristic search option with r andom addition of se- quences (100 replicates) and the nearest neighbor interchange branch-swapping algo- rithm (NNI) were used for tree searching. All Bayesian Markov Chain Monte Carlo (MCMC) analyses were run with seven Markov chains (six heated chains, one cold) for 1,000,000 generations. Trees were sampled every 100 generations. We obtained posterior probability (PP) values for the branching patterns in BI trees as well as bootstrap (BP) values in ML trees. The evolutionary model used in ML and BI analy- ses for the SSU, ITS, endosymbiont SSU phylogenies was TrN+I+G. The GTR+G model was selected for LSU phylogeny. Bootstrap values and posterior probabilities for some clades obtained across the phylogenies were presented on the nodes. Results Taxonomic descriptions Peridiniopsis minima Zhang, Liu et Hu sp. nov. Figs. 1–3 Diagnosis: Unicellular, freshwater thecate dinoflagellate. Cells measure 8–15 μm in length , 6–12 μm in width. The plate tabulat ion is Po, x, 3', 1a, 6'', 5c, 4s (?), 5''', 2''''. Cells are compressed dorsoventrally, oval or spherical in ventral view and subcircular in
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