PROTISTOLOGY European Journal of Protistology 41 (2005) 287–298

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PROTISTOLOGY European Journal of Protistology 41 (2005) 287–298 ARTICLE IN PRESS European Journal of PROTISTOLOGY European Journal of Protistology 41 (2005) 287–298 www.elsevier.de/ejop Phylogenetic analyses of the polycystine Radiolaria based on the 18s rDNA sequences of the Spumellarida and the Nassellarida Tomoko Yuasaa,Ã, Osamu Takahashib, Daisuke Hondac, Shigeki Mayamad aDivision of Mathematics and Natural Science Education, United Graduate School of Education, Tokyo Gakugei University, Koganei, Tokyo 184-8501, Japan bDepartment of Astronomy and Earth Sciences, Tokyo Gakugei University, Koganei, Tokyo 184-8501, Japan cDepartment of Biology, Faculty of Science and Engineering, Konan University, Okamoto, Kobe 658-8501, Japan dDepartment of Biology, Tokyo Gakugei University, Koganei, Tokyo 184-8501, Japan Received 5 May 2004; received in revised form 10 May 2005; accepted 16 June 2005 Abstract Acantharea, Polycystinea, and Phaeodarea have members that are widely distributed in the marine plankton. Many biologists use the conventional term ‘‘Radiolaria’’ to include these three classes. However, on the basis of an 18S rDNA study, Polet et al. (2004, Protist 155, 53–63) recently suggested that the Phaeodarea should be moved into the Phylum Cercozoa. In the present paper, the phylogenetic relationships of the Acantharea and the Polycystinea, especially the phylogenetic positions of Nassellarida and Spumellarida, were inferred from 18S rDNA sequences including those we have determined from the Family Spongodiscidae (Class Polycystinea, Order Spumellarida) and the Family Pterocorythidae (Class Polycystinea, Order Nassellarida). Among major eukaryotic lineages, the Polycystinea were shown to constitute a paraphyletic group: in the phylogenetic trees for the relationships among polycystines, the collosphaerid, sphaerozoid, and thalassicollid spumellarians and the pterocorycid nassellarians constantly formed a monophyletic group, from which the spongodiscid spumellarians were excluded. This conclusion is not consistent with the current taxonomy of the ‘‘Radiolaria,’’ and leads us to consider that the collosphaerid, sphaerozoid, and thalassicollid spumellarians and the pterocorycid nassellarians may have evolved from an ancestor with triradiate branched spicules. r 2005 Elsevier GmbH. All rights reserved. Keywords: Radiolaria; Polycystinea; Acantharea; Spumellarida; Nassellarida; 18s rDNA Introduction endoskeleton that facilitate a floating existence (e.g. Anderson 1983). Currently, many researchers use the Members of Acantharea, Polycystinea, and Phaeo- term ‘‘Radiolaria’’ as a conventional name that com- darea are planktonic protists that are widely distributed prehensively includes all Acantharea, Polycystinea, and in tropical, subtropical, and even polar marine environ- Phaeodarea. ments. They have roughly spherical–subspherical cells Mu¨ ller (1858) first assigned the term ‘‘Rhizopoda and thread-like pseudopodia extending radially over the radiolaria’’ to all planktonic organisms with a central capsule and a radiating skeleton. He included the ÃCorresponding author. Fax: +81 42 329 7538. polycystine and acantharian species in this group. E-mail address: [email protected] (T. Yuasa). Thereafter, Haeckel (1887) used the term ‘‘Radiolaria’’ 0932-4739/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.ejop.2005.06.001 ARTICLE IN PRESS 288 T. Yuasa et al. / European Journal of Protistology 41 (2005) 287–298 to designate the following four taxa: Acantharia, Recently, Polet et al. (2004) and Nikolaev et al. Spumellaria, Nassellaria, and Phaeodaria. This use of (2004) reported 18S rDNA and actin sequence data for the term was partially attributed to similarities in the radiolarians. In their phylogenetic trees, the cytoplasmic morphology, including a perforated capsu- acantharian and polycystine clade constantly included lar wall with fusules and their radial skeletons. However, Sticholonche zanclea Hertwig (taxopodid Heliozoa), and in a modern taxonomic system, Levine et al. (1980) did interestingly the Phaeodarea appeared in the Phylum not recognize the ‘‘Radiolaria’’ as a taxonomic group, Cercozoa. They therefore insisted upon the polyphyly of apparently on the basis of the substantial differences ‘‘Radiolaria’’ and supported the close relationships among the species in the classes, and they excluded the among the Radiolaria, the Foraminifera, and the term ‘‘Radiolaria’’ from their system. This was princi- Cercozoa in the group ‘‘Rhizaria’’ (Cavalier-Smith pally because within the Actinopoda the chemical 2002). composition of the skeletons differs, being of strontium We have already reported 18S rDNA sequences of sulfate (SrSO4) in the Class Acantharea, opaline silica three solitary shell-bearing species of the spongodiscid (SiO2) in the Class Polycystinea, and opaline silica with spumellarian polycystines (Takahashi et al. 2004). In organic matter in the Class Phaeodarea. As with other our report, we also referred to the possibility that the organisms, radiolarian classification systems mainly Polycystinea and the Acantharea form a monophyletic based on morphological studies may have problems group among eukaryotes. In that study, however, there due to convergent or parallel evolution in similar were insufficient taxa to resolve the detailed taxonomic environments. affiliations of the Acantharea and especially the Poly- Over several decades, much research based on cystinea. On the basis of 18S rDNA sequences of three molecular analyses, which is independent of morphol- further species of the Family Spongodiscidae (spumel- ogy, has shown that DNA sequences are useful markers larian Polycystinea) and two species of the Family of evolutionary relationships (e.g. Sogin et al. 1989), and Pterocorythidae (nassellarian Polycystinea) that we have the effectiveness of analyses combining the methods of determined, we here attempt to obtain a better under- morphology and molecular biology has been shown for standing of the phylogenetic relationship between the many taxonomic groups (e.g. Ku¨ hn et al. 2000). In Polycystinea and the Acantharea and also to determine particular, the comparison of ribosomal DNA (rDNA) the phylogenetic position of the Nassellarida among sequences has been shown to be a useful tool for them. clarifying the molecular evolution of both eukaryotes and prokaryotes (e.g. Van de Peer et al. 2000). Amaral Zettler et al. (1997) first examined 18S rDNA sequences of two acantharian and four polycystine Materials and methods species (including three colonial forms and one solitary skeletonless form) in order to explore the diversity of the Sample collection Superclass Actinopoda. They suggested that among the so-called ‘‘crown’’ (Knoll 1992) eukaryotes, the colonial Polycystine samples were collected from surface and solitary skeletonless Polycystinea had emerged seawater in spring 2002 using a plankton net (60 cm before the Acantharea, and they concluded that the diameter opening with 37 mm mesh net) at Site 990528 Polycystinea and the Acantharea do not form a (261370N, 1271470E), located approximately 5 km north- monophyletic group (Amaral Zettler et al. 1997). On west of Okinawa Island, Japan. The collected samples the other hand, Lo´ pez-Garcı´ a et al. (2002) examined the were stored at about 5 1C and immediately brought to 18S rDNA sequences of polycystine- and acantharian- the laboratory at the Tropical Biosphere Research related genomic fragments from Antarctic deep waters Center, University of the Ryukyus. In the laboratory, and revealed a diversity of pico-size protists in the deep polycystine species were transferred from the samples to Antarctic Ocean. They showed that the Polycystinea six-well culturing dishes containing filtered seawater and and the Acantharea formed a monophyletic group at the stored until 18S rDNA region amplifications were apical region of the ‘‘crown’’ group in their phylogenetic processed. trees. Their data indicated a close relationship between The spumellarian polycystines that were subjected to the Polycystinea and the Acantharea that was different molecular analysis are Euchitonia elegans (Ehrenberg) from the result of Amaral Zettler et al. (1997). Lo´ pez- (Fig. 1a), Dicranastrum furcatum Haeckel (Fig. 1b), Garcı´ a et al. (2002) referred to long-branch attraction and Triastrum aurivillii Cleve (Fig. 1c), all from the (LBA) artifacts (Felsenstein 1978) to explain the Family Spongodiscidae. The nassellarian polycystines differences in the topologies, because all known poly- that were examined were two species belonging to cystine branches at that time (e.g. Siphonosphaera Family Pterocorythidae: Eucyrtidium hexagonatum cyathina) were recognized to be fast-evolving lineages Haeckel (Fig. 1d) and Pterocorys zancleus (Mu¨ ller) (Amaral Zettler et al. 1999). (Fig. 1e). ARTICLE IN PRESS T. Yuasa et al. / European Journal of Protistology 41 (2005) 287–298 289 Fig. 1. Light micrographs (LM) of the Polycystinea used in this study. Scale bars indicate 100 mm. (a) Euchitonia elegans (Ehrenberg). (b) Dicranastrum furcatum Haeckel. (c) Triastrum aurivillii Cleve. (d) Eucyrtidium hexagonatum Haeckel. (e) Pterocorys zancleus (Mu¨ ller). DNA extraction and amplification The central capsule was rinsed twice more in distilled water, and then incubated for 30 min at 37 1C in 0.2 mg/ A single cell of each polycystine was rinsed twice in ml Proteinase K solution. This sample was used as a filtered seawater, and the central capsule was physically template for the amplification of 18S rDNA regions. separated with a sterilized razor blade from
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