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Morphology and Phylogeny of Four Marine Or Brackish Water Spirotrich Ciliates (Protozoa, Ciliophora) from China, with Descriptio

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Morphology and Phylogeny of Four Marine Or Brackish Water Spirotrich Ciliates (Protozoa, Ciliophora) from China, with Descriptio Available online at www.sciencedirect.com ScienceDirect European Journal of Protistology 72 (2020) 125663 Morphology and phylogeny of four marine or brackish water spirotrich ciliates (Protozoa, Ciliophora) from China, with descriptions of two new species Chunyu Liana,b, Xiaotian Luob, Alan Warrenc, Yan Zhaod,∗∗, Jiamei Jiange,f,g,∗ aInstitute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, 266003, China bKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China cDepartment of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK dCollege of Life Sciences, Capital Normal University, Beijing, 100048, China eShanghai Universities Key Laboratory of Marine Animal Taxonomy and Evolution, Shanghai Ocean University, Shanghai, 201306, China f Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Shanghai, 201306, China gNational Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, 201306, China Received 9 June 2019; received in revised form 25 November 2019; accepted 30 November 2019 Available online 7 December 2019 Abstract In this study, we investigated the morphology and molecular phylogeny of four marine or brackish spirotrichean cili- ates found in China, namely: Caryotricha sinica sp. nov., Prodiscocephalus orientalis sp. nov., P. cf. borrori, and Certesia quadrinucleata. Caryotricha sinica is characterized by its small size, seven cirral rows extending posteriorly to about 65% of the cell length, and four transverse cirri. Prodiscocephalus orientalis differs from its congeners mainly by the number of cirri in the “head” region and on the ventral side. The SSU rDNA sequence of P. cf. borrori differs from that of other population of P. borrori by ca. 40 bp. Consequently, the nominal species P. borrori is considered to be a species-complex. New data are provided for Certesia quadrinucleata. The Chinese population of C. quadrinucleata, for example, has fewer left marginal cirri than the other populations for which such data are available. Phylogenetic analy- ses based on SSU rDNA sequence data show that the genus Caryotricha is monophyletic. All typical “discocephalids” with a discoid “head” form a strongly supported clade that is sister to the unstable uronychiids + pseudoamphisiellids clade within the Euplotia. The genus Certesia forms a sister group to the Euplotes clade, also within the Euplotia assem- blage. © 2019 Elsevier GmbH. All rights reserved. Keywords: Discocephalida; Euplotia; Hypotrichia; Phylogeny; Taxonomy Introduction ∗Corresponding author at: Key Laboratory of Exploration and Utiliza- tion of Aquatic Genetic Resources, Shanghai Ocean University, Shanghai, Spirotrich ciliates are one of the most diverse groups 201306, China. ∗∗ in the phylum Ciliophora and are widely distributed in Corresponding author. College of Life Sciences, Capital Normal Uni- marine, freshwater, and terrestrial biotopes (e.g., Berger versity, Beijing, 100048, China. E-mail addresses: [email protected] (Y. Zhao), 2011; Dragesco and Dragesco-Kernéis 1986; Foissner 2016; [email protected] (J. Jiang). https://doi.org/10.1016/j.ejop.2019.125663 0932-4739/© 2019 Elsevier GmbH. All rights reserved. 2 C. Lian, X. Luo, A. Warren et al. / European Journal of Protistology 72 (2020) 125663 Lu et al. 2018; Luo et al. 2018; Lyu et al. 2018a,b; Song et al. detail by Lin et al. (2004) and Shao et al. (2008). Here, 2009). Many nominal species are, however, poorly known we provide morphological and molecular data for two and their systematic positions remain uncertain due to the populations of Prodiscocephalus, one of which represents lack of information concerning their infraciliature, morpho- a new species and the other belongs to the P. borrori- genesis, and gene sequences. Since the routine application complex. of silver staining and gene sequencing for documenting the Fabre-Domergue (1885) discovered a Euplotes-like cili- diversity of spirotricheans, this situation has greatly improved ate with a left marginal row for which he created the genus (Abraham et al. 2019; Chen L et al. 2018; Chen X et al. 2018; Certesia, with C. quadrinucleata the type species by mono- Hu et al. 2019; Lyu et al. 2018c; Park et al. 2019; Santoferrara typy. This species has been redescribed several times (Cui et al. 2016; Shin and Kim 1995; Wang et al. 2019; Yanetal. et al. 2009; Kahl 1932; Lin and Song 2004; Sauerbrey 1928; 2018; Zhao et al. 2018). Recently, several new species of Wicklow 1983). Chen et al. (2010) provided details of its spirotricheans have been established based on a combination morphogenesis. Here, we provide the results of an integrative of morphological, morphogenetic, and molecular data (Shao phylogenetic and systematic study based on a new population et al. 2018; Syberg-Olsen et al. 2016; Zhang et al. 2018). of C. quadrinucleata. To explore the species diversity of this group, we surveyed The main aim of this study is to provide detailed informa- Chinese coastal waters of the South China Sea and Yellow tion on the taxonomy and molecular phylogeny of these four Sea and isolated four species belonging to three genera, i.e., spirotrichean ciliates isolated from Chinese coastal waters. Caryotricha, Prodiscocephalus, and Certesia. Kiitrichidae Nozawa, 1941 is a poorly known family of the subclass Hypotrichia that is characterized by an ancestral infraciliature pattern, i.e., ciliated dikinetids on the dorsal Material and methods side and uniform ventral cirri with no differentiation of marginal cirral rows, and has been widely considered as Sampling and morphological methods an early branching group within the hypotrichous ciliates (Fig. 1A–D) sensu lato (Borror 1972; Lynn 2008; Shi 1999; Song and Wilbert 1997). According to Shi (1999), there are only three Caryotricha sinica sp. n. was found on 11 April genera in the family Kiitrichidae, i.e., Transitella Gellert, 2018 in a brackish water pond that formerly was con- 1950, Kiitricha Nozawa, 1941, and Caryotricha Kahl, 1932. nected to the sea, near Kuipeng Road (22◦3515.76N, Lynn (2008) also recognizes three genera of kiitrichids, i.e., 114◦2610.28E), Huizhou, Guangdong Province, China, Kiitricha, Caryotricha and Musajevella Alekperov, 1984, where the water temperature was 25.5 ◦C and the salinity Transitella being regarded as a possible junior synonym of was 19‰. Prodiscocephalus orientalis sp. n. was isolated on Balantidioides Penard in Kahl, 1930. Caryotricha is recog- 14 May 2018 from a reef off Xiao Lajia (22◦3648.84N, nized by the following combination of characters: (1) the 114◦3738.88E), Huizhou, Guangdong Province, China, simple, ancestral pattern of the dorsal dikinetids (both basal where the water temperature was 25.5 ◦C and the salin- bodies of each dikinetid bearing one short cilium); (2) uni- ity was 33‰. Prodiscocephalus cf. borrori was isolated form distribution of ventral cirri; and (3) the presence of from samples collected on 12 October 2018 from a reef a short, postoral row of cirri called the migratory cirral off Yinshatan (35◦5522.84N, 120◦1217.44E), Qingdao, row. To date, only three species of Caryotricha have been Shandong Province, China, where the water temperature reported: C. convexa Kahl, 1932 (type species), C. minuta was 23 ◦C and the salinity was 30‰. Certesia quadrin- (Xu et al., 2008) Miao et al., 2009, and C. rariseta Jiang ucleata was collected on 16 October 2018 from sandy et al., 2013. Here, we describe a new Caryotricha species that littoral sediments near Wanggezhuang (36◦1634.06N, is characterized by its distinctive cirral rows and transverse 120◦4016.65E), Qingdao, Shandong Province, China, cirri. where the water temperature was 22 ◦C and the salin- Discocephalids are rarely reported and their taxonomy ity was 30‰ (Fig. 1). Cells were maintained in habitat is poorly understood (Curds and Wu 1983; Ehrenberg water for further studies. Although clonal cultures were 1831; Jankowski 1978; Jiang et al. 2013; Kahl 1932; not established, no similar morphotypes were present in Lin et al. 2004; Song and Shao 2017; Wicklow 1982). the protargol preparations, indicating that morphological Prodiscocephalus Jankowski, 1979 is a genus of marine and molecular studies of each isolate dealt with a single Discocephalus-like ciliates. It can be distinguished from species. other discocephalids by the presence of a right marginal Cells were observed in vivo using bright field and dif- cirral row and sparsely distributed ventral cirri. There are ferential interference contrast microscopy at 100–1000× two known species: P. minimus (Dragesco, 1968) Jankowski, magnification. The infraciliature and nuclear apparatus were 1979 (type species) and P. borrori (Wicklow, 1982) Lin revealed by protargol staining (Pan et al. 2014; Wilbert 1975). et al., 2004 (type species of Psammocephalus Wicklow, Counts and measurements were performed at magnifications 1982, which is now regarded as a junior synonym of Prodis- of 1000×. Drawings of stained specimens were made with the cocephalus). Prodiscocephauls borrori was redescribed in help of a drawing attachment and photomicrographs. Taxon- C. Lian, X. Luo, A. Warren et al. / European Journal of Protistology 72 (2020) 125663 3 Fig. 1. A–D. Map of China showing the sampling locations and photographs showing the sampling sites. (A) A hole in the intertidal area at Wanggezhuang, Qingdao, from which Certesia quadrinucleata
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