Original PaperGertia stigmatica gen. et sp. nov. (Kareniaceae, Dinophyceae), a New Marine Unarmored Dinoflagellate Possessing the Peridinin-type Chloroplast with an Eyespot
Introduction
The family Kareniaceae is mainly comprised of three unarmored dinoflagellate genera, Karenia, Karlodinium and Takayama (Bergholtz et al., 2005, Daugbjerg et al., 2000, de Salas et al., 2008). One of characteristic features of this family is the shape of the furrow-like apical structure complex (ASC, = apical groove). Daugbjerg et al. (2000) described two genera with the straight ASC, Karenia and Karlodinium, the latter having a ventral pore and plug-like structure. De Salas et al. (2003) subsequently established the genus Takayama with a sigmoid ASC, showing a close relationship to Karlodinium. Recently, the affinity of Asterodinium gracile Sournia and Brachidinium capitatum F. J. R. Taylor to the Kareniaceae was demonstrated by molecular phylogeny, justifying the previous morphological observation of these species having a straight ASC (Benico et al. 2019; Gómez et al. 2005; Gómez 2006; Henrichs et al. 2011). Gómez et al. (2016) provided SSU rDNA sequence of Ptychodiscus noctiluca Stein, which similarly possesses a straight ASC, but its phylogenetic relationship to the Kareniaceae was not fully resolved. Members of the Kareniaceae, especially the three major genera, are recognized as fish-killing dinoflagellates (e.g., Dai et al., 2014, Leong et al., 2015, Lim et al., 2014, Onoue et al., 1985, Takayama, 1981, Takayama, 1985, Takayama and Matsuoka, 1991, Takayama et al., 1998, Yang et al., 2000), and more than 30 species have so far been described (e.g., Bergholtz et al., 2005, Daugbjerg et al., 2000, de Salas et al., 2003, de Salas et al., 2004, de Salas et al., 2005, de Salas et al., 2008, Gu et al., 2013, Haywood et al., 2004, Luo et al., 2018, Nézan et al., 2014, Yang et al., 2000, Yang et al., 2001).
Another diagnostic feature of the Kareniaceae is the possession of chloroplasts (i.e., photosynthetic plastids) containing fucoxanthin and 19′-acyloxyfucoxanthins (i.e., 19′-hexanoyloxyfucoxanthin and 19′-butanoyloxyfucoxanthin; 19′-AF-type) and lacking peridinin (e.g., Bergholtz et al., 2005, Bjørnland and Tangen, 1979, Chang and Gall, 2013, de Salas et al., 2003, de Salas et al., 2004, de Salas et al., 2005, Hansen et al., 2000, Tangen and Bjørnland, 1981), which is different from the peridinin-type chloroplast typical in dinoflagellates. Phylogeny of plastid-encoded DNAs showed the kareniacean chloroplast to be of haptophyte origin (e.g., Gabrielsen et al., 2011, Ishida and Green, 2002, Takishita et al., 1999, Takishita et al., 2000, Takishita et al., 2004, Takishita et al., 2005, Tengs et al., 2000, Waller and Koreny, 2017).
A naked dinoflagellate recently reported from the Ross Sea, Antarctic Ocean, does not have the typical chloroplast, even though it is closely related to the Kareniaceae in molecular analysis (Gast et al. 2006). According to Gast et al. (2007), this dinoflagellate possesses temporary chloroplasts (kleptochloroplasts) captured from the haptophyte Phaeocystis sp.; however, the phylogenetic position of this kleptochloroplast is not closely related to the permanent chloroplasts of Karenia and Karlodinium in the haptophyte clade. Similar isolates related to the Ross Sea dinoflagellate were also reported from the French coast (as Kareniaceae sp. in Nézan et al. 2014). These isolates are referred to as ‘kleptoplastic sp.’ in this article.
An interesting novel kareniacean species was isolated from the Japanese coast. This small marine dinoflagellate has the straight ASC of the Kareniaceae, but differs in having the peridinin-type chloroplast with an eyespot. In the present study, Gertia stigmatica gen. et sp. nov. is proposed for this isolate, with the description of its ultrastructure and pigment composition, and discussion of the evolutionary status on the basis of molecular phylogeny inferred from nucleus- and chloroplast-encoded DNAs.
Section snippets
Gertia K. Takahashi et Iwataki gen. nov.
Unarmored dinoflagellates with chloroplast containing peridinin as a major pigment. Straight furrowed apical structure complex present.
Type species: Gertia stigmatica (described below).
Etymology: Named after Dr. Gert Hansen who proposed the genus Karenia Hansen et Moestrup ex Daugbjerg et al. (2000).
Gertia stigmatica K. Takahashi et Iwataki sp. nov.
Marine unarmored dinoflagellate. Cells ellipsoid, 5.9–9.5 μm long and 4.9–7.8 μm wide, with the epicone smaller than the hypocone. Cingulum anterior, displaced about one and a half cingulum width.
Taxonomy
Gertia stigmatica possesses the straight ASC, the character shared with Karenia and Karlodinium, and its position in the Kareniaceae was supported by nucleus-encoded rDNA phylogenies. On the other hand, the chloroplast found in G. stigmatica was of peridinin-type, which is distinct from 19′-AF-type reported in other kareniacean species (Benico et al., 2019, Daugbjerg et al., 2000, de Salas et al., 2003). This pigment composition does not correspond with the diagnosis of the family Kareniaceae
Methods
Culture: A strain of Gertia stigmatica gen. et sp. nov. (mdd472-kt strain) originated from a surface seawater off the coast of Manazuru, Sagami Bay, Japan (35°09′N, 139°10′E) in October 2016. Heterocapsa circularisquama and Karenia mikimotoi cultures used in pigment analyses were collected from Mikawa Bay, Japan in 2018, and from Manila Bay, Philippines in 2018, respectively. 500 mL of surface water obtained was prescreened by using a 20 μm mesh, and gently concentrated by gravity filtration
Acknowledgements
We appreciate Dr. Shinji Shimode of Yokohama National University and Ms. Shiori Otake of University of Tokyo for their sampling assistance. Dr. Kazutaka Takahashi of University of Tokyo provided experimental tools including maintenance of culture strain, molecular analysis and EM preparation. Dr. Fumiko Ishizuna of University of Tokyo provided assistance on TEM. Dr. Tomoyo Katayama and Mr. Shota Takino of University of Tokyo and Dr. Takashi Yoshikawa of Tokai University provided assistance on
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2022, Harmful AlgaeCitation Excerpt :Also, we assessed the HAB extent and dynamics by using satellite-derived imagery, because the unique pigment composition of Karenia can be recognized in satellite imagery data (Soto et al., 2015). Karenia cells contain fucoxanthin as an accessory carotenoid and lack peridinin, a major diagnostic pigment for many dinoflagellates (Daugbjerg et al., 2000; Hansen et al., 2000; Örnólfsdóttir et al., 2003; Steidinger et al., 2008; Takahashi et al., 2019). Satellite imagery provides a potential solution for addressing various HAB-associated issues such as species recognition of blooming algae, intensity assessment and bloom stage prediction, HAB diagnostics and zoning (Shen et al., 2012; Blondeau-Patissier et al., 2014; Palmer et al., 2015; Ogashawara, 2019; Zohdi and Abbaspour, 2019; Hill et al., 2020; Wolny et al., 2020).
First record of a Takayama bloom in Haizhou Bay in response to dissolved organic nitrogen and phosphorus
2022, Marine Pollution BulletinCitation Excerpt :The family originally consisted of three genera: Karenia, Karlodinium, and Takayama (Bergholtz et al., 2005; Daugbjerg et al., 2000; de Salas et al., 2008). Some studies have suggested the addition of four genera to the Kareniaceae family: Asterodinium, Brachidinium, Gertia, and Shimiella (Benico et al., 2019; Ok et al., 2021; Takahashi et al., 2019). The species in the three most common genera, Karenia, Karlodinium, and Takayama, have been reported as HAB-causative species because they produce toxins and harmful substances that not only kill fish, marine mammals, and other animals, but also cause neurotoxic shellfish poisoning and respiratory distress in humans.
Morphological variation and phylogeny of Karenia selliformis (Gymnodiniales, Dinophyceae) in an intensive cold-water algal bloom in eastern Hokkaido, Japan
2022, Harmful AlgaeCitation Excerpt :The unarmored dinoflagellates in the Kareniaceae are responsible for mass mortalities of fish and other organisms in coastal marine environments (Lundholm et al., 2009 onwards). Among the seven genera in this family, Asterodinium Sournia, Brachidinium Sournia, Gertia K.Takahashi et Iwataki, Karenia G.Hansen et Moestrup, Karlodinium Larsen, Shimiella Ok, Jeong, Lee et Noh, and Takayama de Salas, Bolch et Hallegraeff, species in Karenia, Karlodinium and Takayama have caused harmful algal blooms (HABs) (Daugbjerg et al., 2000; de Salas et al., 2003; Benico et al., 2019; Takahashi et al., 2019; Ok et al., 2021). In the Northwest Pacific, fisheries damage has been reported with kareniacean blooms of Karenia mikimotoi (Miyake et Kominami ex Oda) G.Hansen et Moestrup, Karenia longicanalis Yang, Hodgkiss et G.Hansen, Karenia papilionacea Haywood et Steidinger, Karlodinium digitatum (Yang, Takayama, Matsuoka et Hodgkiss) Gu, Chan et Lu, Karlodinium australe de Salas, Bolch et Hallegraeff, Karlodinium veneficum (Ballantine) Larsen, and Takayama acrotrocha Larsen (Yang et al., 2000, 2001; Tang et al., 2012; Lim et al., 2014; Yamaguchi et al., 2016; Li et al., 2019; Benico et al., 2020).
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