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A Case Study of Trachelomonas (Euglenaceae)

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A Case Study of Trachelomonas (Euglenaceae) View metadata, citation and similar papers at core.ac.uk brought to you by CORE Žerdoner Čalasan & al. • Taxonomic clarification of Trachelomonas taxa TAXON 69 (1) • February 2020:provided 28 –by42 Open Access LMU SYSTEMATICS AND PHYLOGENY Contemporary integrative taxonomy for sexually deprived protists: A case study of Trachelomonas (Euglenaceae) from western Ukraine Anže Žerdoner Čalasan,1,2 Juliane Kretschmann1 & Marc Gottschling1 1 Department Biologie, Systematische Botanik und Mykologie, GeoBio-Center, Ludwig-Maximilians-Universität München, Menzinger Str. 67, 80 638 Munich, Germany 2 Fachbereich 5: Biologie/Chemie, Botanik, Universität Osnabrück, Barbarastr. 11, 49 076 Osnabrück, Germany Address for correspondence: Marc Gottschling, [email protected] DOI https://doi.org/10.1002/tax.12206 Abstract As many other protist groups, euglenophytes are prone to false identification based solely on morphology because of a lim- ited amount of morphological features and cryptic speciation. One of the supposedly completely asexual groups within the freshwater phototrophic representatives of euglenophytes is Trachelomonas, capable of forming an inorganic shell around its cell (i.e., the lorica). The International Code of Nomenclature for algae, fungi, and plants regulates the taxonomy not only of flowering plants, but explic- itly also of phototrophic protists, and provides powerful tools to resolve various taxonomic challenges. To exemplify some of the problems and potential solutions, a number of Trachelomonas strains were collected from the muddy, lake-rich region of Dobrostany and cultivated under stable laboratory conditions. Being a type locality of 58 unclarified Trachelomonas names, this region in western Ukraine is of great taxonomic importance. Based on light and electron microscopy, and on RAxML and MrBayes phylogenetics using multiple loci and a representative taxon sample, a detailed description of investigated strains and their systematic placement is pro- vided. Morphologically, the strains differed slightly but consistently in minute characters such as size, lorica shape and ornamentation. The presently most comprehensive molecular tree of the Euglenaceae indicated to the existence of at least five different species pre- sent in the newly investigated samples, although they were collected from localities in very close vicinity to each other and at the same date. Based on morphological comparisons with type illustrations of species validly described 100 or more years ago, biological mate- rial was used to epitypify three names of Trachelomonas, eternally linking morphology with reliable genetic information. This taxo- nomic application is one of the powerful methods to clarify ambiguous scientific names, which has particular importance in character- poor protists such as the euglenophytes. Keywords asexual organism; epitypification; Euglenida; Euglenophyta; molecular phylogenetics; morphology; ribosomal RNA; type locality Supporting Information may be found online in the Supporting Information section at the end of the article. ■ INTRODUCTION and approved algal taxonomy can be assured only by a powerful federal organisation such as the International Association for Unambiguous scientific names are the prerequisite for Plant Taxonomy (IAPT) with its periodical Taxon. proper identification and, therefore, any subsequent applica- The exemplary subject of this study to demonstrate a good tion of biological species. The taxonomy not only of flowering practice to resolve taxonomic challenges in protists are eugle- plants, but also of phototrophic protists, is regulated by the nophytes. These represent an ecologically and economically International Code of Nomenclature for algae, fungi, and important group of unicellular plankton organisms, as they plants (ICN; Turland & al., 2018). Unicellular organisms, include numerous primary producers but can cause massive which can only be identified under the microscope, are partic- algal blooms, resulting in fish culture losses (Kulczycka ularly prone to taxonomic confusion (De Clerck & al., 2013; & al., 2018). Trachelomonas Ehrenb. comprises of not less Manoylov, 2014), and corresponding “standard” (i.e., type) than 1700 uncritically listed scientific names at the species material is often poorly preserved or entirely lost. Diverging level and below (Guiry & Guiry, 2017). Together with Cola- methodological approaches have led to some deviations of cium Ehrenb., Cryptoglena Ehrenb., Discoplastis Triemer, phycological research within botany, which is also expressed Euglena Ehrenb., Euglenaformis M.S.Bennett & Triemer, by explicitly disregarding Rec. 46A of the Code (i.e., author Euglenaria Karnkowska-Ishikawa & al., Eutreptia Perty, abbreviations of scientific names) in a number of distin- Eutreptiella A.G.Cunha, Lepocinclis Perty, nom. cons. (Senn guished phycological journals. However, effective, sustainable in Briquet, 1930; Silva, 1960; Ross, 1966), Monomorphina Article history: Received: 10 Jun 2019 | accepted: 16 Dec 2019 | published online: 10 Apr 2020 | Associate Editor: Øjvind Moestrup | © 2020 The Authors. TAXON published by John Wiley & Sons Ltd on behalf of International Association for Plant Taxonomy. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 28 Version of Record TAXON 69 (1) • February 2020: 28–42 Žerdoner Čalasan & al. • Taxonomic clarification of Trachelomonas taxa Mereschk., Phacus Dujard., nom. cons. (Silva, 1960; Ross, regulatory system of crossing over. Nevertheless, asexual 1966) and Strombomonas Deflandre, Trachelomonas repre- clones still possess a consistent set of traits, which are the sents an integral element of the freshwater Euglenophyceae result of natural selection, and in this manner resemble organ- as inferred from molecular phylogenetics (Kim & al., 2015; isms with sexual reproduction (Gottschling, 2008). However, Bicudo & Menezes, 2016). asexually propagating organisms such as cyanobacteria and The striking apomorphy of all euglenophytes is the bdelloid rotifers are still equally ranking in taxonomy with pellicle. It is a unique surface structure, comprised of a micro- “regular” biological species. tubular system, endoplasmic reticulum cisterns and a plasma During the past decades, molecular DNA sequence data membrane, connected with protein layers (Arnott & Walne, have gained great importance for taxonomic delimitations 1967). In addition, euglenophytes are capable of producing in the microbial world including Trachelomonas.Asin and secreting an additional mucilage layer (Dunlap & Walne, many other protist species, cryptic speciation is also 1985). In some cases, such as Strombomonas and Trachelo- observed here (Kim & al., 2013; Przybos & Tarcz, 2016), monas, this extracellular matrix becomes thicker and gets resulting in a number of morphologically indistinguishable impregnated with inorganic substances, forming an inorganic species. In turn, it is also highly plausible that size varia- shell termed lorica (Pringsheim, 1953; Leedale, 1975). Chem- tions and different ecological forms of the same species ical analyses show that the main inorganic compounds found have been described as several distinct species due to their in loricae of Trachelomonas are iron and manganese (Rino plasticity (Bicudo & Menezes, 2016). Thus, diversity of & Pereira, 1991), which are together with a great deal of other Trachelomonas has been continuously under- and overesti- elements incorporated in the lorica via non-active physical mated at the same time. processes (Pereira & al., 2003). Depending on its mineral Because of cryptic speciation, it is important to link DNA composition, the colour of the lorica varies from translucent sequence data to a type specimen, but the original material of to brown or reddish-brown (Pringsheim, 1953). microscopic organisms consists in many (particularly older) Within Euglenaceae, state reconstruction indicates that a cases of illustrations only. Since protists frequently lack diag- lorica is a synapomorphic feature shared by the sister groups nostic morphological features (Pawlowski & al., 2012), type Strombomonas and Trachelomonas (Karnkowska & al., specimens (including illustrations) cannot provide for unam- 2015). Trachelomonas can be distinguished from Strombomo- biguous identification of certain species. As one is not able to nas based on lorica ontogeny: Strombomonas loricae namely connect a type illustration to a DNA sequence, the same prob- alwaysdevelopprogressivelyfrom theanterior towards thepos- lem arises, as if the type material is in poor condition. In such terior part of the cell, whereas the formation of Trachelomonas cases, it is recommended to designate an epitype via epitypifi- loricae takes place evenly across the entire cell (Brosnan & al., cation (Hyde & Zhang, 2008). This powerful tool has already 2005). Additionally, Strombomonas loricae do not possess been applied to solve taxonomic ambiguities in various protis- pores, whereas Trachelomonas loricae are always ornamented tan groups such as green algae (Demchenko & al., 2012) and (i.e., possessing poresand/or spines) at least at one stage of their dinophytes (Zinßmeister & al., 2011; John & al., 2014; development (Brosnan & al., 2003). A diversity of spines and Kretschmann & al., 2015, 2018a,b; Tillmann & al., 2017)
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