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A New Subspecies of Oxytricha Granulifera (Hypotrichia: Oxytrichidae) from Mexico, with Notes on Its Morphogenesis and Phylogenetic Position

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A New Subspecies of Oxytricha Granulifera (Hypotrichia: Oxytrichidae) from Mexico, with Notes on Its Morphogenesis and Phylogenetic Position Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE A New Subspecies of Oxytricha granulifera (Hypotrichia: Oxytrichidae) from Mexico, with Notes on its Morphogenesis and Phylogenetic Position Daniel Mendez-S anchez a , Rosaura Mayen-Estrada a, Xiaotian Luob & Xiaozhong Hub a Laboratorio de Protozoologıa, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico, Circuito Ext. s/num. Ciudad Universitaria, Av. Universidad 3000, Coyoacan, 04510 Ciudad de Mexico, Mexico b Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China Keywords ABSTRACT Cell division; Chiapas; dorsal kineties; Oxytri- cha granulifera chiapasensis; SSU rRNA; The genus Oxytricha Bory de Saint-Vincent in Lamouroux, Bory de Saint-Vin- undulating membranes. cent and Deslongchamps, 1824 comprises about 38 species distributed world- wide and has been considered to be a nonmonophyletic group. Based on Correspondence living observations, protargol preparations, and a small subunit ribosomal RNA D. Mendez-S anchez, Laboratorio de Proto- (SSU rRNA) gene sequence, we describe a new subspecies Oxytricha granulif- zoologıa, Facultad de Ciencias, Universidad era chiapasensis n. subsp. This new taxon is morphologically characterized by Nacional Autonoma de Mexico, Circuito Ext. undulating membranes basically in a Stylonychia-pattern, six dorsal kineties, s/num., Av. Universidad 3000 Ciudad size in vivo ca. 60–120 9 20–40 lm, 21–30 right and 21–31 left marginal cirri, Universitaria, C. P. 04510, Coyoacan, Ciudad 22–29 adoral membranelles, and spherical cortical granules arranged in longitu- de Mexico, Mexico dinal rows on the dorsal side. In terms of the SSU rRNA gene sequence, the Telephone number: +(525)56224924; new subspecies differs from populations of O. granulifera from GENBANK by FAX number: +(525)56224828; 7–35 nucleotides. Phylogenetic analyses showed that Oxytricha granulifera e-mail: [email protected] gene sequences were nested into three groups, with the new subspecies included in one of them. Oxytricha granulifera chiapasensis n. subsp. is differ- Received: 31 March 2017; revised 2 ent from Oxytricha granulifera granulifera Foissner and Adam, 1983 and Oxytri- October 2017; accepted October 6, 2017. cha granulifera quadricirrata Blatterer and Foissner, 1988 based on: Early View publication November 10, 2017 (i) undulating membranes in Stylonychia-pattern, (ii) formation of a sixth dorsal kinety during morphogenesis, (iii) the adoral membranelles number, and doi:10.1111/jeu.12479 (iv) inhabiting freshwater habitats. OXYTRICHIDS are a species-rich group of ciliates with marine environments, and also soil, mosses, decaying high morphological and molecular variation (Foissner 2016; wood mass, and water of bromeliad tanks worldwide (Ber- Hu et al. 2011). Ciliates belonging to the genus Oxytricha ger 1999; Berger and Foissner 1989; Duran-Ram ırez et al. Bory de Saint-Vincent in Lamouroux, Bory de Saint-Vincent 2015; Foissner 1997, 1999, 2016; Kwon and Shin 2004, and Deslongchamps, 1824, have a flexible body, and are 2008, 2013; Tirjakova and Bartosov a 2004; Weisse et al. characterized by an adoral zone of membranelles resem- 2013). To our knowledge, only five species, i.e. Oxytricha bling a question mark, undulating membranes arranged in discifera (Aladro-Lubel et al. 2006), O. fallax (Aladro-Lubel an Oxytricha-pattern (slightly curved and intersected spa- et al. 2006; Lugo-Vazquez et al. 1991; Moreno-Baron and tially), 18 frontal–ventral–transverse cirri (with frontoventral Lopez-Ochoterena 1976; Rico-Ferrat and Lopez-Ochote- cirri in a V-shape pattern), one right and one left row of rena 1976; Sokoloff and Ancona 1937), O. hymenostoma marginal cirri, usually five or six dorsal kineties in Oxytri- (Sokoloff 1936), O. opisthomuscorum (Duran-Ram ırez cha-pattern, and caudal cirri present (Berger 1999; Shao et al. 2015), and Oxytricha sp. (Aladro-Lubel et al. 2006; et al. 2011, 2015). Duran-Ram ırez et al. 2015; Lugo-Vazquez et al. 1998) have Within this family, Oxytricha is a species-rich genus, been recorded in Mexico. and, so far, comprises around 38 nominal species (Berger The genus Oxytricha has been considered to be a non- 1999; Foissner 1999, 2016; Shao et al. 2011, 2014; monophyletic group (Hu et al. 2011; Paiva et al. 2009; Weisse et al. 2013). They inhabit freshwater, brackish and Schmidt et al. 2007; Shao et al. 2014) by using © 2017 The Author(s) Journal of Eukaryotic Microbiology © 2017 International Society of Protistologists Journal of Eukaryotic Microbiology 2018, 65, 357–371 357 New Mexican Subspecies of Oxytricha granulifera Mendez-S anchez et al. phylogenetic analyses based on the SSU rRNA gene and Blood and Tissue kit (Qiagen, Hilden, Germany). For PCR other molecular markers; however, the incongruence amplification, two universal primers were used: Euk A (50- between morphology and molecular information suggests AACCTGGTTGATCCTGCCAGT-30) and Euk B (50- that Oxytricha is a genus with high genetic divergence TGATCCTTCTGCAGGTTCACCTAC-30) (Medlin et al. 1988). (Foissner 2016) and, thus, has been considered to be an The cycles were started at 98 °C for 30 s, followed by 35 artificial genus (Berger 1999; Hu et al. 2011). cycles of 10 s each at 94 °C, 30 s at 48 °C, and 1 min Oxytricha granulifera Foissner and Adam, 1983, type- and 30 s at 65 °C, and finally 1 cycle for 5 min at 65 °C. species of the genus (Berger and Foissner 1997; Foissner The PCR product was sequenced directly using primers 1989), has been well-characterized both morphologically Euk A, Euk B, and three internal primers (Wang et al. and morphogenetically (Foissner and Adam 1983). This 2016). species is more often found in terrestrial environments (Berger 1999), but has also been isolated from freshwater Phylogenetic analysis environments (Kwon and Shin 2013). Geographically, O. granulifera has been recorded in the Neotropical, The SSU rRNA gene sequence obtained was aligned with Palearctic, Ethiopian, and Australian biogeographical 67 hypotrichid sequences available from GENBANK by regions (Berger 1999; Foissner 1997, 1999, 2016; Foissner using the MUSCLE algorithm (Edgar 2004) on the GUI- and Adam 1983; Foissner et al. 2002, 2005, 2008; Kwon DANCE web server. Ambiguous columns with a confi- and Shin 2013; Shao et al. 2014; Tirjakova and Bartosov a dence score below 0.93 were removed (Penn et al. 2010), 2004). and the alignment was then manually edited in MEGA 7.0 The goal of this study was to describe the morphology (Kumar et al. 2016) to remove ambiguous gaps (both pri- of a new subspecies, Oxytricha granulifera chiapasensis n. mers were cut off). The resulting alignment was 1,718 subsp., which is first documented from Montebello, a characters. For phylogenetic analysis, the GTR + I + G Mexican lake, based on its morphological features, mor- model was used according to Weisse et al. (2013) and phogenetic pattern, and its unique SSU rRNA gene Shao et al. (2014). Maximum likelihood (ML) analysis was sequence. carried out using RAxML-HPC2 on XSEDE v. 8.2.9 (Sta- matakis 2014) with 1,000 bootstraps replication. Bayesian Inference (BI) was performed with MrBayes 3.2 (Ronquist MATERIALS AND METHODS et al. 2012), with four chains of 10,000,000 generations, with trees sampled every 100 generations, of which the Sampling, morphology and morphogenesis first 25,000 generations were discarded as burn-in. Both Freshwater samples were collected in June of 2015 in the ML and BI were performed via the CIPRES Science Gate- littoral zone of Montebello Lake, in Tziscao Ecoturistic way website. Novistrombidium orientale FJ422988, National Park within the southern portion of Chiapas, Mex- Stombidium apolatum DQ662848, Strombidinopsis acumi- ico (16°6018.22″N, 91°4204.79″W) (Fig. S1). The lake is sur- nate FJ790209, and Parastrombidinopsis minima rounded by a pine-oak forest at 1,500 masl. Specimens DQ393786 were selected as the outgroup taxa. To visua- were isolated and maintained as nonclonal cultures (pure lize tree topologies, MEGA 7.0 was used (Kumar et al. cultures) in Petri dishes at room temperature using mi- 2016). The gene sequence obtained was aligned with the neral water with nonsterile rice grains to enrich bacteria Oxytricha granulifera gene sequences used for the phylo- as food resource. Living observations were made with genetic tree, the alignment was manually edited in MEGA bright field and differential interference contrast (DIC) 7.0 and both primers were cut off, in order to generate microscopy. Cells were stained with in-house synthesized the similarity structural matrix (pairwise analysis) and the protargol (Pan et al. 2013), following the protocol of Wil- number of nucleotides differences (absolute distance bert (1975) to reveal the infraciliature and nuclear appara- matrix) using MEGA 7.0 (Kumar et al. 2016). tus. We observed several well-impregnated dividers in different stages to partially characterize the morpho- RESULTS genetic pattern. Measurements and counts of stained cells were carried Morphological description of Oxytricha granulifera out with an ocular micrometer at 1,000X magnification, chiapasensis n. subsp including stages of morphogenesis. Drawings are based on photomicrographs. Terminology and systematic classifi- Morphological description cation are according to Berger (1999, 2006), Shao et al. Live cells about 60–120 9 20–40 lm, with an adoral zone (2011, 2015), and Lynn (2008). of membranelles occupying around 30% of the cell length. Cell shape ellipsoidal with left border slightly convex (Fig. 1A, 2A–C),
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