Molecular phylogeny of the parasitic dinoflagellate Syltodinium listii (Gymnodiniales, Dinophyceae) and generic transfer of Syltodinium undulans comb. nov. (= Gyrodinium undulans)

Highlights

• The parasite Syltodinium listii is first reported since the original description.

• Syltodinium undulans comb. nov. is proposed for Gyrodinium undulans.

• Syltodinium SSU rRNA gene sequence clusters with Chytriodinium and Dissodinium.

• Chytriodiniaceae contain free-living taxa (G. aureolum, G. corollarium, G. plasticum).

Abstract

The parasitic dinoflagellate Syltodinium listii was investigated from the open waters of the English Channel, southern North Sea and the NW Mediterranean Sea. Syltodinium listii has been unreported since its original description in the North Sea. Cells of S. listii were able to infect copepod eggs of different species, and even nauplii, and after each infection formed up to 32 cells embedded in a mucous envelope. Infection of the same host by more than one dinoflagellate was frequent; although overall, the progeny were reduced in number. Molecular phylogeny based on the small subunit ribosomal RNA (SSU rRNA) gene revealed that S. listii clusters with a group of environmental sequences from the cold North Atlantic region as a sister group of Gymnodinium aureolum. The large subunit ribosomal RNA (LSU rRNA) gene sequences of S. listii from the English Channel and cf. Gyrodinium undulans from the Mediterranean Sea were identical. Thus, we propose Syltodinium undulans comb. nov. for Gyrodinium undulans. The first internal transcribed spacer (ITS) and complete SSU rRNA gene sequences of Dissodinium pseudolunula are provided. The parasitic species of Chytriodinium, Dissodinium and Syltodinium cluster together within the family Chytriodiniaceae, including the free-living species Gymnodinium aureolum, G. corollarium and G. plasticum.

Introduction

Copepods are the most abundant animal group in the ocean. The lipid-rich copepod eggs are the target of parasitic species of the dinoflagellate genera Chytriodinium, Schizochytriodinium and Dissodinium, whose dinospores infest the eggs, absorb the host contents and form successive sporangia that release gymnodinioid infective spores (Apstein 1906; Cachon and Cachon 1968; Dogiel 1906; Drebes 1969, 1978, 1981; Elbrächter 1988; Gómez and Artigas 2013; Gönnert 1936; Lebour 1925; Pouchet 1885). Molecular phylogenies reveal that Chytriodinium spp. and Dissodinium pseudolunula cluster within the Gymnodinium clade (Gómez et al. 2009; Gómez and Skovgaard 2015; Kim et al. 2008).

According to Drebes (1988), the parasitic dinoflagellate Syltodinium listii appeared by chance as a contaminant in a culture of Dissodinium fed with copepod eggs, and once recognized, it was identified from the summer plankton of the North Sea. Cells of S. listii developed a peduncle that sucked out the contents of copepod and rotifer eggs. After food uptake, the trophont detached and began successive binary divisions to form up to 16 or 32 gymnodinioid cells inside of a mucous envelope (Drebes 1988). In a clonal culture of the diatom Odontella aurita, Drebes and Schnepf (1998) detected the contamination of a dinoflagellate that fed on the diatom, and was able to feed on copepod eggs. Drebes and Schnepf (1998) identified it as Gyrodinium undulans that was described as a free-living species from the North American coasts at Great Pond, Woods Hole (Hulburt 1957). The morphology and life cycle was similar to Syltodinium listii, and Drebes and Schnepf (1998) suggested that G. undulans and S. listii may be the winter and summer forms, respectively, of the same species.

The smooth cell surface of Gyrodinium undulans does not fit with the current circumscription of the genus Gyrodinium that is restricted, among other characters, to cell coverings with longitudinal striae (Hansen and Daugbjerg 2004; Takano and Horiguchi 2004). Gyrodinium undulans and Syltodinium listii are characterized by a distinctive sigmoid anterior extension of the sulcus (Drebes 1988; Hulburt 1957). A sigmoid apical groove is a diagnostic character of the genus Takayama (de Salas et al. 2003). All the known species of Takayama, and other closely related genera (Brachidinium, Karenia, Karlodinium) are photosynthetic species with fucoxanthin as an accessory pigment, while G. undulans and S. listii are heterotrophic species. From the NW Mediterranean Sea, Reñé et al. (2015) reported a micrograph of a cell identified as cf. G. undulans with the distinctive sigmoid anterior sulcus. The partial LSU rRNA gene sequence (GenBank accession number KP790206) clustered within the Gymnodinium clade with sequences of Gymnodinium aureolum as the closer relative. Reñé et al. (2015, p. 256) concluded “Since a close phylogenetic relationship between G. undulans and S. listii can be expected (if not representing the same species), G. undulans can be rejected as a member of the Gyrodinium genus because it is included within the Gymnodiniales s.s. clade. However, since our specimen could not be precisely identified, any systematic change would be premature”.

In this study, we investigate the molecular phylogeny, life cycle and host specificity of Syltodinium listii from the English Channel. We provide the first molecular data of the genus Syltodinium (SSU-, LSU rRNA and ITS gene sequences), and the first ITS and complete SSU rRNA gene sequences of Dissodinium pseudolunula.