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(Dinophyceae), with Descriptions of Ceratocorys Malayensis Sp Phycologia ISSN: 0031-8884 (Print) 2330-2968 (Online) Journal homepage: https://www.tandfonline.com/loi/uphy20 Attributing Ceratocorys, Pentaplacodinium and Protoceratium to Protoceratiaceae (Dinophyceae), with descriptions of Ceratocorys malayensis sp. nov. and Pentaplacodinium usupianum sp. nov. Zhaohe Luo, Zhen Fei Lim, Kenneth Neil Mertens, Bernd Krock, Sing Tung Teng, Toh Hii Tan, Chui Pin Leaw, Po Teen Lim & Haifeng Gu To cite this article: Zhaohe Luo, Zhen Fei Lim, Kenneth Neil Mertens, Bernd Krock, Sing Tung Teng, Toh Hii Tan, Chui Pin Leaw, Po Teen Lim & Haifeng Gu (2020) Attributing Ceratocorys, Pentaplacodinium and Protoceratium to Protoceratiaceae (Dinophyceae), with descriptions of Ceratocorysmalayensissp.nov. and Pentaplacodiniumusupianumsp.nov., Phycologia, 59:1, 6-23, DOI: 10.1080/00318884.2019.1663693 To link to this article: https://doi.org/10.1080/00318884.2019.1663693 View supplementary material Published online: 16 Oct 2019. Submit your article to this journal Article views: 51 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=uphy20 PHYCOLOGIA 2020, VOL. 59, NO. 1, 6–23 https://doi.org/10.1080/00318884.2019.1663693 Attributing Ceratocorys, Pentaplacodinium and Protoceratium to Protoceratiaceae (Dinophyceae), with descriptions of Ceratocorys malayensis sp. nov. and Pentaplacodinium usupianum sp. nov. 1 2 3 4 5 2 2 2 ZHAOHE LUO ,ZHEN FEI LIM ,KENNETH NEIL MERTENS ,BERND KROCK ,SING TUNG TENG ,TOH HII TAN ,CHUI PIN LEAW ,PO TEEN LIM , 1 AND HAIFENG GU 1Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China 2Bachok Marine Research Station, Institute of Ocean and Earth Sciences, University of Malaya, Bachok 16310, Malaysia 3Ifremer, LER BO, Station de Biologie Marine, Place de la Croix, BP40537, Concarneau CEDEX F-29185, France 4Alfred Wegener Institute for Polar and Marine Research, Ecological Chemistry, Am Handelshafen 12, Bremerhaven D-27570, Germany 5Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, Kota Samarahan 94300, Malaysia ABSTRACT ARTICLE HISTORY The gonyaulacean family Protoceratiaceae is characterised by five precingular plates. It currently Received 22 May 2019 encompasses the type genus Ceratocorys and the fossil genus Atopodinium. Fourteen strains of Accepted 02 September 2019 Ceratocorys, Pentaplacodinium, and Protoceratium were established from Malaysian and Hawaiian waters, Published online 16 October and their morphologies were examined using light and scanning electron microscopy. Two new species, 2019 Ceratocorys malayensis sp. nov. and Pentaplacodinium usupianum sp. nov., were described from Malaysian KEYWORDS waters. They share a Kofoidean plate formula of Po, Pt, 3ʹ, 1a, 6ʹʹ, 6C, 6S, 5ʹʹʹ, 1p, 1ʹʹʹʹ. Ceratocorys Ceratocoryaceae; malayensis has a short first apical plate (1ʹ) with no direct contact with the anterior sulcal plate (Sa) Gonyaulacaceae; Molecular whereas Pentaplacodinium usupianum had a parallelogram-shaped 1ʹ plate which often contacted the Sa phylogeny; Protoceratium plate. The genera Ceratocorys and Pentaplacodinium were emended accordingly to incorporate species reticulatum; Yessotoxin bearing five or six precingular plates. The Protoceratium strain from Hawaii was morphologically similar to P. reticulatum, but differed in the lack of a ventral pore in plate 1′ and slight or lack of contact between plates 1′ and Sa, and is here designated as P. cf. reticulatum. The maximum-likelihood and Bayesian inference analyses based on SSU, LSU and ITS ribosomal DNA sequences revealed that these three genera are monophyletic and form a well-resolved group. Our results support Protoceratium and Pentaplacodinium as members of the family Protoceratiaceae, characterised by the presence of one anterior intercalary plate. Seven strains of Protoceratium cf. reticulatum, Ceratocorys malayensis and Pentaplacodinium usupianum were examined for yessotoxin production by LC-MS/MS but none pro- duced a detectable amount of toxin. INTRODUCTION sometimes inconsistent (Helenes 2000) or gradational in nature, and, in some instances, tentative (Fensome et al. 1993). The Gonyaulacales is a major order of dinophytes that is subdi- Currently, the Ceratocorythaceae include only the extant vided into five suborders based only on morpho-anatomy genus Ceratocorys F.Stein and the fossil genus Atopodinium (Fensome et al. 1993). One of these, Gonyaulacineae, encompasses Drugg (Fensome et al. 1993). Ceratocorys is characterised by two extant families, Gonyaulacaceae and Ceratocorythaceae, and three apical plates, one small anterior intercalary plate and one fossil family, Areoligeraceae. Ceratocorythaceae have five five precingular plates (3′, 1a, 5′′). The third Kofoidean pre- precingular plates, L-type ventral organisation and strong dextral cingular plate in Ceratocorys is considered homologous to torsion, whereas Gonyaulacaeae have six precingular plates, L- to both the third and fourth precingular plates in other gonyau- S-type ventral organisation and sinistral to dextral torsion lacoid dinoflagellate genera (Mertens et al. 2018b). (Fensome et al. 1993). Thus, the key difference between Additionally, cells of Ceratocorys are often characterised by Gonyaulacaceae and Ceratocorythaceae is the number of precin- an angular body, shorter epitheca relative to hypotheca, small gular plates (six versus five). The Gonyaulacaceae was subdivided to large spines on the hypotheca, and heavily ornamented further into three subfamilies by Fensome et al.(1993): theca (Carbonell-Moore 1996). Twelve Ceratocorys species Cribroperidinioideae (with L-type ventral organisation and dextral have been described, e.g. Ceratocorys anacantha M.C. torsion), Leptodinioideae (with L-type ventral organisation and Carbonell-Moore, C. armata (Schütt) Kofoid, C. bipes sinistral or neutral torsion), and Gonyaulacoideae (with S-type (Cleve) Kofoid, C. horrida Stein; all are exclusively marine ventral organisation and neutral torsion). The criteria used to and found only in tropical and subtropical waters (Carbonell- distinguish subfamilies of Gonyaulacaceae, however, were CONTACT Haifeng Gu [email protected] Colour versions of one or more of the figures in the article can be found online at www.tandfonline.com/uphy. Supplemental data for this article can be accessed on the publisher’s website. © 2019 International Phycological Society Luo et al.: Attributing Ceratocorys, Pentaplacodinium and Protoceratium to Protoceratiaceae (Dinophyceae) 7 Moore 1996; Graham 1942). However, sequences of MATERIAL AND METHODS Ceratocorys are available for only three species: Ceratocorys Sample collection and treatment armata, C. horrida, and C. gourretii, which share high nucleo- tide similarity for the SSU (100%) and LSU ribosomal gene Surface sand samples (upper 5 cm) were collected by SCUBA markers (> 99%; Mertens et al. 2018b). divers using plastic bottles from Semariang and Talang–Talang Pentaplacodinium Mertens, Carbonell-Moore, Pospelova & Island (Sarawak), Rawa Island (Terengganu), Malaysia, from Head was established for strains formerly identified as 2010 to 2016 (Table 1). The samples were rinsed with filtered Protoceratium reticulatum (Claparède & Lachmann) Bütschli seawater and transferred into a polycarbonate bottle. Single (Mertens et al. 2018b). Salgado et al.(2018) considered this motile ceratocorioid cells were immediately isolated by means species to belong to Ceratocorys. Mertens et al.(2018a, b)dis- of drawn-out Pasteur pipettes and using an Eclipse TS100 agreed because of the insert type epithecal configuration in these inverted microscope (Nikon, Tokyo, Japan) to establish clonal strains, unlike the episert type in Ceratocorys horrida, the type cultures. Thirteen strains of Ceratocorys and Pentaplacodinium species of Ceratocorys. However, episert (type I) was also were initially established in ES-DK medium at 25 °C (Kokinos & reported in Pentaplacodinium saltonense (Salgado et al. 2018, Anderson 1995) in Malaysia. These clonal cultures were trans- as Ceratocorys mariaovidiorum). Pentaplacodinium is a sister ferred to Xiamen and maintained with f/2-Si medium (Guillard – – clade of Ceratocorys in the molecular phylogeny based on ribo- &Ryther1962) at 20 °C, 90 µmol quanta·m 2·s 1 under a 12:12 somal DNA sequence, but has not been assigned to a family. h light: dark cycle (hereafter called ‘standard culture condi- Protoceratium reticulatum is a common dinoflagellate tions’). Plankton samples were also collected using a 20 µm originally described from Bergen Fjord, Norway, by mesh-size plankton net by vertical and horizontal hauls at sub- Claparède & Lachmann (1858)asPeridinium reticulatum surface water of Rawa Island in 2016. The samples were fixed Claparède & Lachmann. Protoceratium Bergh was erected with 2% Lugol’s solution, and later for SEM examination. by Bergh (1881, p. 242) with P. aceros as the type species In Hawaii, sediment sampling was done using an Ekman (fig. 36) collected at Strib, Denmark. The plate formula for grab in nearby Haleiwa Harbour on 4 March 2014 (water depth P. reticulatum was first provided by Wołoszyńska (1929)as 3.0 m; Table 1). The top 2 cm of sediment were sliced off and 4′, 0a, 6′′,6′′′,1p,1′′′′, based on the Baltic Sea specimens. stored in the dark at 4 °C until further treatment. Reinecke (1967) described a similar species as Gonyaulax Approximately 5 g of wet sediment was mixed with 20 ml of grindleyi Reinecke based on specimens
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