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Morphology and Molecular Phylogeny of a New Hypotrich Ciliate, Anteholosticha Songi Nov. Spec., and an American Population of Ho

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Morphology and Molecular Phylogeny of a New Hypotrich Ciliate, Anteholosticha Songi Nov. Spec., and an American Population of Ho Available online at www.sciencedirect.com ScienceDirect European Journal of Protistology 72 (2020) 125646 Morphology and molecular phylogeny of a new hypotrich ciliate, Anteholosticha songi nov. spec., and an American population of Holosticha pullaster (Müller, 1773) Foissner et al., 1991 (Ciliophora, Hypotrichia) Lingyun Chena,1, Jingyi Dongb,1, Weining Wuc,1, Yuanyuan Xina, Alan Warrend, Yingzhi Ninga,∗, Yan Zhaoe,∗ aLaboratory of Microbiota, College of Life Science, Northwest Normal University, Lanzhou 730070, China bInstitute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China cCollege of Resources and Environmental Sciences, Gansu Agricultural University, Lanzhou 730070, China dDepartment of Life Sciences, Natural History Museum, London SW7 5BD, UK eCollege of Life Sciences, Capital Normal University, Beijing 100048, China Received 29 August 2019; received in revised form 19 October 2019; accepted 21 October 2019 Available online 31 October 2019 Abstract A new urostylid ciliate, Anteholosticha songi nov. spec., isolated from forest soil in Tibet, and an American population of Holosticha pullaster (Müller, 1773) Foissner et al., 1991, isolated from a freshwater pond in the USA, are investigated in terms of their morphology, ontogenesis, and molecular biology. Anteholosticha songi nov. spec. is characterized by a slender to ellipsoidal body measuring 160–205 × 40–55 ␮m in vivo; rod-shaped yellowish cortical granules arranged in irregular short rows; four dorsal kineties; adoral zone consisting of 35–40 membranelles; three frontal, one buccal, one parabuccal, two frontoterminal, two pretransverse, and four to six transverse cirri and 14–25 midventral pairs; 12–22 ellipsoidal macronuclear nodules longitudinally arranged in pairs left of cell mid-line. Supplemental information on morphogenesis in Holosticha pullaster is also presented. The phylogenetic relationship of Anteholosticha and Holosticha inferred from SSU rDNA sequence data are concordant with previous studies and showing that Holosticha is monophyletic whereas Anteholosticha is polyphyletic and should be split into two or more genera. © 2019 Elsevier GmbH. All rights reserved. Keywords: China; Morphogenesis; SSU rDNA; Taxonomy; Urostylida Introduction 2019; Kumar et al. 2018; Li et al. 2018; Lu et al. 2018; Luo et al. 2017; Lynn 2008; Méndez-Sánchez et al. 2018; Shao About 200 hypotrich species have been reported in the et al. 2007, 2019; Wang et al. 2019a; Zhang et al. 2018; Zhu past decade (e.g., Bai et al. 2018; Berger 2001, 2006, 2008, et al. 2019). Nevertheless, recent studies have indicated that 2011; Deng et al. 2018; Foissner 2016; Jung and Berger there are many more taxa awaiting discovery (e.g., Li et al. 2017, 2019; Luo et al. 2018; Lyu et al. 2018a,b; Shao et al. 2013, 2015; Song and Shao 2017; Song et al. 2009). Further- ∗Corresponding authors. more, the classification, validity, and delimitation of some E-mail addresses: [email protected] (Y. Ning), [email protected] of these hypotrich species have been problematic and have (Y. Zhao). been resolved differently by various authors (Gao et al. 2016, 1 These three authors contributed equally. https://doi.org/10.1016/j.ejop.2019.125646 0932-4739/© 2019 Elsevier GmbH. All rights reserved. 2 L. Chen, J. Dong, W. Wu et al. / European Journal of Protistology 72 (2020) 125646 2017; Huang et al. 2010, 2016; Lyu et al. 2018c; Sheng et al. pH 6.5. The samples were air-dried for one month and then 2018). Among them, the taxonomic history and complexity sealed in a large paper envelope until they were processed of Holosticha and its allies are rather complicated and have during May to October 2018. The non-flooded Petri dish been debated by many authors (Berger 2003, 2006; Chen method was used to stimulate ciliates to excyst (Foissner et al. et al. 2018; Fan et al. 2016; Zhao et al. 2015). 2002). Clonal cultures were established at room temperature Holosticha was established by Wrzesniowski´ (1877) and (about 25 ◦C) in Petri dishes using mineral water (Nongfu over the following ca. 125 years numerous nominal species Spring) with rice grains to enrich the growth of bacteria as were described from marine, limnetic and terrestrial habi- a food resource for the ciliates (Foissner et al. 2002). Other tats (for details, see Berger 2003, 2006; Gong et al. 2001; hypotrichs such as Pattersoniella sp., Hemiurosoma sp. and Hu and Song, 2001, Hu et al., 2003; Kim et al. 2017; Lei Gonostomum sp. were also found in samples. et al. 2005; Luo et al. 2015; Song and Wilbert 1997, 2002; Holosticha pullaster was collected from the surface Song et al. 2002; Wilbert and Song 2008). Holosticha kess- water (0–10 cm) of a small freshwater pond near the leri (Wrzesniowski,´ 1877), a subjective junior synonym of H. Duke Garden in the center of Duke University cam- gibba (Müller, 1786), is the type species by subsequent desig- pus (36◦0002N, 78◦5608W), North Carolina, USA nation (Borror 1972). Holosticha was taxonomically revised on 11 January 2015 (for details of location, see URL: by Berger (2003, 2006, 2008), who divided its members https://gardens.duke.edu/visit/duke-gardens-map and Fig. 1). into four genera, namely Holosticha Wrzesniowski,´ 1877, The water temperature was 10 ◦C and pH 7.0. Specimens Anteholosticha Berger, 2003, Caudiholosticha Berger, 2003 were isolated and a clonal culture was maintained using the and Biholosticha Berger, 2003. To date, there are eight valid same methods as for A. songi nov. spec. species of Holosticha, however phylogenetic relationships Living and stained specimens were observed by bright among these are largely unresolved due to the lack of molec- field and differential interference contrast microscopy (Leica ular data for most of them (Berger 2003, 2006, 2008; Luo DM5000). Protargol staining was utilized to reveal the infra- et al. 2015). ciliature and nuclear apparatus (Wilbert 1975). The protargol Anteholosticha was established for species previously powder was made according to Pan et al. (2013). Counts assigned to Holosticha sensu Kahl (1932) and Borror (1972) and measurements of cellular structures in stained specimens that lack appropriate apomorphies (for details, see Berger were performed at a magnification of 1000×. Drawings of 2003, 2006). Analyses of the molecular phylogeny and pat- stained specimens were performed with the help of a drawing terns of morphogenesis have revealed that this genus is device. Terminology and classification are mainly according extremely divergent (Berger 2006, 2008; Chen et al. 2018; to Berger (2006) and Lynn (2008). Huang et al. 2014; Lv et al. 2015; Park et al. 2012, 2013; Zhao et al. 2015). Consequently, in order to gain a better under- DNA extraction and PCR amplification standing of the systematics and taxonomy of Anteholosticha, the 27 constituent species need to be reinvestigated using A single cell of each species was isolated, washed and modern methods including molecular phylogenetic analyses. transferred into a microfuge tube (1.5 ml). DNA was extracted In the present paper, we describe a new species of Ante- using DNeasy Blood & Tissue Kit (Qiagen, CA) accord- holosticha, i.e., A. songi nov. spec., and reinvestigate an ing to manufacturer instructions and Huang et al. (2018). American population of Holosticha pullaster (Müller, 1773) The SSU rDNA sequence was amplified using the universal Foissner et al., 1991. We also present their phylogenetic primers EukA and EukB (Medlin et al. 1988). PCR condi- relationships inferred from SSU rDNA sequence data and tions, cycling parameters and sequencing were according to describe the morphogenesis of Holosticha pullaster in order Wang et al. (2019b). to evaluate their systematic relationships. Phylogenetic analyses Material and methods The newly sequenced SSU rDNA of Anteholosticha Sampling, morphology and morphogenesis songi nov. spec. and Holosticha pullaster, plus another 100 hypotrich ciliate sequences obtained from GenBank Anteholosticha songi nov. spec. was isolated from the database (for accession numbers, see Fig. 7), were used upper 5 cm layer of soil in the Motuo Virgin Forest to infer phylogenetic relationships of Anteholosticha and (29◦2541N, 95◦2414E), Tibet, most of which is over Holosticha. The GenBank accession numbers of the 2000 m above sea level. The mean annual temperature is seven species of Oxytrichidae are as follows: Gastrostyla 12–16 ◦C and annual precipitation is 2300 mm. The vegeta- steinii AF508758, Sterkiella nova AF508771, Pleu- tion is dominated by Lagerstroemia minuticarpa, Schefflera rotricha lanceolata AF508768, Sterkiella histriomuscorum heptaphylla, Sambucus williamsii and Senecio scandens. AF508770, Stylonychia mytilus AF508774, Cyrtohymena Four soil samples (about 500 g each) were collected in citrina AF164135, Paraurostyla weissei AF508767. Six December 2016 when the air temperature was 15 ◦C and soil euplotids, namely Uronychia setigera, U. multicirrus, Dio- L. Chen, J. Dong, W. Wu et al. / European Journal of Protistology 72 (2020) 125646 3 Fig. 1. A–D. Locations of the sample sites. (A) Map showing the location of Motuo, Tibet Autonomous Region. (B) Location where Anteholosticha songi nov. spec. was collected. (C, D) Location where Holosticha pullaster was collected. phrys scutum, Paradiophrys zhangi, Apodiophrys ovalis and Family Urostylidae Bütschli, 1889 Pseudodiophrys nigricans, were selected as the outgroup Genus Anteholosticha Berger, 2003 taxa. The sequences were aligned using the MUSCLE pro- gram implemented in the GUIDANCE 2 web
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