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Morphology, Cell-Division, and Phylogeny of Schmidingerothrix Elongata Spec

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Morphology, Cell-Division, and Phylogeny of Schmidingerothrix Elongata Spec Available online at www.sciencedirect.com ScienceDirect European Journal of Protistology 62 (2018) 24–42 Morphology, cell-division, and phylogeny of Schmidingerothrix elongata spec. nov. (Ciliophora, Hypotricha), and brief guide to hypotrichs with Gonostomum-like oral apparatus Xiaoteng Lua,b,c,1, Jie Huangd,1, Chen Shaoa,∗, Helmut Bergere,∗ aThe Key Laboratory of Biomedical Information Engineering, Ministry of Education, School of Life Science and Technology, Xi’an Jiaotong University, Xi’an 710049, China bUniversity of Innsbruck, Research Institute for Limnology, Mondseestrasse 9, 5310 Mondsee, Austria cInstitute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China dKey Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China eConsulting Engineering Office for Ecology, Radetzkystrasse 10, 5020 Salzburg, Austria Received 29 June 2017; received in revised form 2 November 2017; accepted 6 November 2017 Abstract The hypotrich Schmidingerothrix elongata spec. nov., discovered in saline (20‰) soil of the Longfeng Wetland, Daqing, northern China, was studied using live observation and protargol impregnation. It is characterized, inter alia, by colorless cortical granules arranged in short rows, three frontoventral cirral rows with the rightmost extending far posteriorly, and 4–8, usually six macronuclear nodules. Cell division proceeds as in congeners and confirms the lack of dorsal ciliature. In phylogenetic analyses based on SSU rDNA, S. elongata is sister of S. salinarum + Paracladotricha salina. A re-investigation of the type slides of P. salina, type of Paracladotricha, revealed a misobservation in the original description. Since P. salina lacks, like Schmidingerothrix spp., a dorsal ciliature, Paracladotricha becomes a junior, subjective synonym of Schmidingerothrix with S. salina comb. nov. as fourth species. A review of the phylogenetic analyses dealing with Schmidingerothrix shows that its position is variable. However, together with the gonostomatid oral apparatus it can be hypothesized that Schmidingerothrix is a member of the Gonostomatidae or a close relative. A list of genera (14) and species (58) which have – like Schmidingerothrix – a gonostomatid oral apparatus, as well as a key to these genera are provided. © 2017 Elsevier GmbH. All rights reserved. Keywords: China; Guide; Longfeng Wetland; Saline habitat; Soil biology; Taxonomy Introduction Schmidingerothrix was established by Foissner (2012) for ∗Corresponding authors. S. extraordinaria Foissner, 2012, a peculiar hypotrichous cil- E-mail addresses: [email protected] (C. Shao), iate from highly saline soils in Africa. Somewhat later, two [email protected] (H. Berger). further species were described from saline waters in Europe 1 Co-first author. https://doi.org/10.1016/j.ejop.2017.11.001 0932-4739/© 2017 Elsevier GmbH. All rights reserved. X. Lu et al. / European Journal of Protistology 62 (2018) 24–42 25 and China, respectively, namely S. salinarum Foissner et al., China, on 6 May 2014. Samples were malodorous (very likely 20141 and Paracladotricha salina Shao et al., 2017, type due to hydrogen sulfide), and filled with rotten leaves and of Paracladotricha Shao et al., 20171. A re-analysis of the branches. For preservation and future isolation, samples were type material of P. salina showed that the dorsal ciliature dried at room temperature (about 24 ◦C) immediately after was incorrectly described resulting in synonymy of Para- collection. cladotricha and Schmidingerothrix. Ciliates were made to excyst by applying the non-flooded In January 2015, an obviously undescribed hypotrich was Petri dish method (Foissner et al., 2014). They were then isolated from saline soil of Longfeng Wetland, a district of isolated and non-clonal cultures were established at room Daqing, northern China. The analysis of its morphology and temperature (about 24 ◦C) in Petri dishes containing filtered cell division as well as the sequence of the small subunit soil percolate and squeezed rice grains to enrich the bacterial ribosomal DNA (SSU rDNA) indicate that it represents a food. further Schmidingerothrix species. Living specimens were observed using bright field and dif- The phylogenetic position of Schmidingerothrix in molec- ferential interference contrast microscopy (Foissner 2014). ular trees is uncertain for two reasons, namely (i) the type Protargol preparation was used to reveal the ciliature and the species was not sequenced (Foissner 2012), and (ii) the nuclear apparatus (Wilbert 1975). Counts and measurements other species can be found at various positions, for exam- of prepared specimens were performed at a magnification ple isolated as single branch (e.g., Foissner et al., 2014; Lu of 1000×. Drawings of protargol-prepared cells were made et al. 2015; present work), as sistergroup of the urostylids with the aid of a drawing device (camera lucida). To illustrate (Li et al. 2014; Luo et al. 2016, 2017), or in a cluster the changes occurring during morphogenesis, old (parental) with Gonostomum (Heber et al. 2014; Huang et al. 2016). structures are depicted by contour whereas new ones are Foissner (2012) put Schmidingerothrix into the monotypic shaded black. family Schmidingerotrichidae. In the discussion of division, Foissner et al. (2014, p. 73) compared Schmidingerothrix Terminology salinarum with “some supposed relatives, viz. Cladotricha, Gonostomum, and Wallackia”. The similarity with these gen- General terminology is mainly according to Lynn (2008); era is mainly due to the oral apparatus, which is more or less for terms specific for hypotrichs, see Berger (1999, 2006, gonostomatid in all these taxa. 2008, 2011) and Foissner and Al-Rasheid (2006). The tail- Berger (2011) assigned 33 species in seven genera to the length was measured according to the “1/3-method” (Chen Gonostomatidae Small & Lynn, 1985. However, since then et al. 2016). The frontoventral cirral rows are designated as several new species and genera have been described. Thus, ontogenetic numbering (Shao et al. 2014, 2017), that is, the we provide an updated list of genera and species with such an rows have the same designation as the anlagen from which oral apparatus. Together with an updated key to the genera, they originate. It should be noted that the Schmidingerothrix this will simplify the identification of species described after extraordinaria (type species of the genus) lacks cirral row I the revision of Gonostomum by Berger (2011). and II, thus frontoventral cirral row (FR) in Foissner (2012) is row III in the present paper; whereas the frontoventral cirral rows (V1–3) of S. salinarum (Foissner 2014) equal to row Material and Methods III–V in the present paper. Sample collection, isolation, and identification ZooBank registration Saline soil samples (0–10 cm; salinity of soil percolate ZooBank registration of present work (see Recom- about 20‰; pH 10.0) were collected in the Longfeng Wet- ◦ ◦ mendation 8A of ICZN 2012): urn:lsid:zoobank.org:pub: land (lat 46 35 30 N, long 125 13 08 E), Daqing, northern 410D9370-F872-4D66-8FED-460082AAEA5A. 1 The names Schmidingerothrix salinarum Foissner et al., 2014, Para- cladotricha Shao et al., 2014, and Paracladotricha salina Shao et al., 2014 DNA extraction, PCR amplification and have been mentioned in online-only (electronic-only) papers which lack a sequencing ZooBank registration in the work itself (Foissner et al. 2014; Shao et al. 2014). Due to this lack, these two works are not published in the sense of Genomic DNA was extracted from single cells using nomenclature and the new names mentioned therein are not available (ICZN, 2012, Article 8.5.3; further papers suffering on the same problem and cited DNeasy Tissue kit (Qiagen, CA) following the manufac- in the present work are those by Heber et al. 2014 and Bharti et al. 2015). turer’s instructions, with the modification that 25% of the In the present work, all names mentioned in such “unpublished” papers are volume suggested for each reagent solution was used. The disclaimed for nomenclatural purposes (ICZN, 1999, Article 8.3). The orig- SSU rDNA gene was amplified according to Gao et al. (2014), inal description of Paracladotricha and P. salina was recently published by using the primers 18S-F (5-AAC CTG GTT GAT CCT GCC Shao et al. (2017), the original description of S. salinarum is in preparation. AGT-3) and 18S-R (5-TGA TCC TTC TGC AGG TTC ACC However, as explained by Shao et al. (2017), such an “unpublished” paper remains available as a source of published descriptions and illustrations. TAC-3 )(Medlin et al. 1988). 26 X. Lu et al. / European Journal of Protistology 62 (2018) 24–42 Phylogenetic analyses ventral membranelles. Three, rarely four frontoventral cirral rows with three (row II), five (III), and 23 (IV) cirri on aver- The SSU rDNA sequence of Schmidingerothrix elongata age. Right and left marginal cirral row composed of about spec. nov. and those of 69 other hypotrichs were downloaded 27 and 22 cirri on average, respectively. 4–8, usually seven from GenBank database for the phylogenetic analyses (for (median) macronuclear nodules arranged in or slightly left of accession numbers, see Fig. 6). In preliminary tests, we used body midline, 1–4 micronuclei. euplotids as outgroup. Usually, the core urostylids were sister Type locality. Saline soil from the Longfeng Wetland, to the large clade containing Schmidingerothrix (or its junior Daqing, northern
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