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Morphology, Molecular Phylogeny, and Pigment Characterization of a Novel Phenotype of the Dinoflagellate Genuspelagodinium from Korean Waters

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Morphology, Molecular Phylogeny, and Pigment Characterization of a Novel Phenotype of the Dinoflagellate Genuspelagodinium from Korean Waters Research Article Algae 2015, 30(3): 183-195 http://dx.doi.org/10.4490/algae.2015.30.3.183 Open Access Morphology, molecular phylogeny, and pigment characterization of a novel phenotype of the dinoflagellate genus Pelagodinium from Korean waters Éric Potvin1,*, Hae Jin Jeong2, Nam Seon Kang2, Jae Hoon Noh3 and Eun Jin Yang1 1Division of Polar Ocean Environment, Korea Polar Research Institute, Incheon 406-840, Korea 2School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, Seoul 151-747, Korea 3Marine Resources Research Department, KIOST, Ansan 425-600, Korea The dinoflagellate genusPelagodinium is genetically classified in distinct sub-clades and subgroups. However, it is dif- ficult to determine whether this genetic diversity represents intra- or interspecific divergence within the genus since only the morphology of the type strain of the genus Pelagodinium, Pelagodinium bei, is available. An isolate associated with the genus Pelagodinium from Shiwha Bay, Korea, was recently cultured. This isolate formed a subgroup with 3 to 4 strains from the Atlantic Ocean, Mediterranean Sea, and Indian Ocean. This subgroup was distinct from the subgroup contain- ing P. bei. The morphology of the isolate was analyzed using optical and scanning electron microscopy and was almost identical to that of P. bei except that this isolate had two series of amphiesmal vesicles (AVs) in the cingulum, unlike P. bei that has one series. When the pigment compositions of the isolate and P. bei were analyzed using high-performance liquid chromatography, these two strains had peridinin as a major accessory pigment and their pigment compositions were almost identical. In addition, the swimming behaviors of these two strains were very similar. The re-examination of the type culture of P. bei revealed two series in the cingulum as for the isolate. The new findings on the number of series of AVs in the cingulum, the pigment composition, and the swimming behaviors suggest that P. bei and the isolate may be conspecific despite their association to genetically different subgroups. This study provides a basis to further understand the molecular classification withinPelagodinium combining genetic, morphological, pigment, and behavioral data. Key Words: foraminifera; Gymnodinium bei; pelagic symbiont; Suessiaceae; Suessiales INTRODUCTION Marine dinoflagellates are ubiquitous and play diverse trichocysts, and swimming behavior were recognized, roles in marine ecosystems (Jeong et al. 2010, 2012, 2015). detailed observations of the arrangement of the amphies- The dinoflagellate Gymnodinium bei Spero is a sym- mal vesicles (AVs) was lacking (Spero 1987). Thereafter, biont of the foraminifer Orbulina universa D’Orbigny various dinoflagellate symbionts of planktonic foramin- (Spero 1987). While basic features such as the shape, di- ifera sampled worldwide were characterized genetically mensions, presence of an hypoconal flange and stalked and referred as “G. bei” (Gast and Caron 1996, Shaked and pyrenoids penetrated by thylakoid lamellae, absence of De Vargas 2006). However, these results suggested that This is an Open Access article distributed under the Received May 13, 2015, Accepted July 27, 2015 terms of the Creative Commons Attribution Non-Com- Corresponding Author mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which * permits unrestricted non-commercial use, distribution, and reproduction E-mail: [email protected] in any medium, provided the original work is properly cited. Tel: +82-32-760-5345, Fax: +82-32-760-5399 Copyright © 2015 The Korean Society of Phycology 183 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860 Algae 2015, 30(3): 183-195 “G. bei” was more closely related to the order Suessiales. group P1a, sister of subgroup P1b as defined by Shaked Subsequently, a culture of a dinoflagellate isolated from and De Vargas (2006) based on LSU rDNA (Siano et al. Orbulina universa, collected off the coast of Puerto Rico 2010). There is an important genetic diversity between in the Caribbean Sea, was established (Siano et al. 2010). and within clades P1 and P2 (Shaked and De Vargas 2006). Similar features to G. bei were observed on the collected As stated by Siano et al. (2010), only sequences identical isolate, suggesting that the cultured dinoflagellate wasG. to the type sequence should be attributed to P. bei. All bei (Spero 1987). The morphological characterization of other sequences should be designated as Pelagodinium the dinoflagellate revealed various features. It had a single sp. awaiting further characterization to verify their actual elongated apical vesicle (EAV) with a row of small knobs, a taxonomic status. feature not present in the genus Gymnodinium. The pres- The increase of studies assessing the diversity and dis- ence of a type E extraplastidial eyespot, the arrangement tribution in the field using molecular tools makes the de- of the AVs in series, and the absence of trichocyst con- tailed characterization of strains associated to the various firmed its affiliation with other symbiotic dinoflagellates phylotypes and their comparison with the type species and certain genetically related non-symbiotic genera particularly relevant. However, details of the sulcal area, from Suessiales. The arrangement of the series of vesicles the internal transcribed spacers and 5.8S ribosomal RNA of the analyzed strain was unique within the Suessiales, gene (referred to as ITS rDNA), and the pigment compo- and the pyrenoid ultrastructure was different from other sition of the type species P. bei were not assessed, which symbiotic dinoflagellates. Furthermore, phylogenetic impaired the comparison between strains of various phy- analysis based on the large subunit ribosomal RNA gene lotypes. (referred to as LSU rDNA) established that G. bei clusters We recently established a clonal culture of a small di- in an independent, well-supported clade within Sues- noflagellate able to grow photosynthetically from Shiwha siales with other sequences of symbiotic dinoflagellates Bay, Korea, that was related to the genus Pelagodinium. extracted from planktonic foraminifera (Shaked and De The phylotype of this strain was unreported. In this study, Vargas 2006, Siano et al. 2010). This led to the reclassi- we describe the morphological and genetic features, and fication of G. bei and its combination within the newly the swimming behavior of this isolate using optical and erected genus Pelagodinium Siano, Montresor, Probert et scanning electron microscopy (SEM), and phylogenetic De Vargas as Pelagodinium bei (Spero) Siano, Montresor, analyses based on ITS and LSU rDNA. We also deter- Probert et De Vargas. mined the pigment composition using high-performance Extraction from pooled symbionts, combined host and liquid chromatography (HPLC). To clearly determine the symbionts, culture of symbionts established after micro- identity of the new phylotype, we also reinvestigated the dissection, and bulk microplanktonic communities, fol- type culture of P. bei to complement the data previously lowed by amplification or cloning, and sequencing have available (Siano et al. 2010). This study provides a basis increased our knowledge on the distribution of symbi- to further understand the molecular classification within onts associated with foraminifera around the world (Gast the genus Pelagodinium. and Caron 1996, Shaked and De Vargas 2006, Decelle et al. 2012, Kok et al. 2014, De Vargas et al. 2015). The distribu- tion of Pelagodinium is mainly based on molecular data. MATERIALS AND METHODS It has been reported in various areas of the Atlantic Ocean (Shaked and De Vargas 2006, De Vargas et al. 2015), Indian Isolation Ocean (Shaked and De Vargas 2006, De Vargas et al. 2015), western North Pacific Ocean (Fujiki et al. 2014, Kok et al. The culture of the isolate from Korea was established 2014), South Pacific Ocean (Shaked and De Vargas 2006, from surface sediment samples collected on September De Vargas et al. 2015), and Mediterranean Sea (Shaked 30, 2010 (depth, 11.5 m; surface temperature, 19.6°C; sa- and De Vargas 2006, Decelle et al. 2012, De Vargas et al. linity, 11.7) from Shiwha Bay, Korea (37°18′ N, 126°36′ E). 2015). The surface sediment was collected from an Eckman grab In the phylogenetic analyses, the phylotypes associated (WILDCO; Wildlife Supply Company, Buffalo, NY, USA) with the genus Pelagodinium were clustered into various and stored in the dark at 4°C until further analyses. To sub-clades, which were then subdivided into subgroups concentrate potentially viable cells, between 1 and 2 mL (Shaked and De Vargas 2006). The type sequence of P. of sediment were sieved through 100-µm and 15-µm Ny- bei clustered in clade P1, sister of clade P2, and the sub- tex meshes with filtered seawater. The 15-100 µm fraction http://dx.doi.org/10.4490/algae.2015.30.3.183 184 Potvin et al. Pelagodinium bei from Korea was then transferred to a 100-mL beaker with filtered sea- USA). The sample was subsequently centrifuged (WiseS- water. A manual vortex was applied and the suspended pin CF-10 Microcentrifuge; DAIHAN Scientific Co., Ltd., fraction was recovered to concentrate cells. The remnant Namyangju, Korea) at 7,500 ×g for 5 min at room temper- fraction was incubated in F/2-Si culture medium (Guil- ature. The cells were immediately subjected to total DNA lard and Ryther 1962) with a salinity of 32 at 20°C under a extraction using the AccuPrep Genomic DNA extraction light-dark cycle 14 : 10 at a photon flux of 20 µmol -2m s-1. kit (Bioneer Corp., Daejeon, Korea) according to the man- A cell swimming in the medium was isolated by micro- ufacturer’s instructions. manipulation and a monoclonal culture was established Amplicons of the ITS and LSU rDNA were obtained. after two serial single-cell isolations. The polymerase chain reaction (PCR) final mix concen- trations were as follows: 1× PCR f-Taq buffer (fTaq DNA Type culture of Pelagodinium bei polymerase; SolGent Co., Ltd., Daejeon, Korea), 0.2 mM of dNTP (fTaq DNA Polymerase; SolGent Co., Ltd.), 0.4 The culture that was used to establish the holotype of µM of each primer, 0.025 U µL-1 of f-Taq DNA polymerase the type species P.
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