Small but Manifold – Hidden Diversity in “

Published by the International Society of Protistologists Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Small but Manifold – Hidden Diversity in “Spumella-like Flagellates” Lars Grossmanna, Christina Bocka, Michael Schweikertb & Jens Boenigka a Department of Biodiversity, University of Duisburg-Essen, Universitatsstrasse€ 5, 45141 Essen, Germany b Department of Zoology, University of Stuttgart, Pfaffenwaldring 57, 70550 Stuttgart, Germany Keywords ABSTRACT Bacterivorous protists; biodiversity; Chrysomonads; Chrysophyceae; hetero- Colourless, nonscaled chrysophytes comprise morphologically similar or even trophic nanoflagellates; microbial food web; indistinguishable flagellates which are important bacterivors in water and soil microbial loop; Monas; Stramenopiles; crucial for ecosystem functioning. However, phylogenetic analyses indicate a taxonomy. multiple origin of such colourless, nonscaled flagellate lineages. These flagellates are often referred to as “Spumella-like flagellates” in ecological and biogeo- Correspondence graphic studies. Although this denomination reflects an assumed polyphyly, it L. Grossmann, Department of Biodiversity, obscures the phylogenetic and taxonomic diversity of this important flagellate University of Duisburg-Essen, Univer- group and, thus, hinders progress in lineage- and taxon-specific ecological sur- sitatsstrasse€ 5, 45141 Essen, Germany veys. The smallest representatives of colourless chrysophytes have been Telephone number: +49-(0)201-183-3200; addressed in very few taxonomic studies although they are among the dominant FAX number: +49-(0)201-183-4290; flagellates in field communities. To overcome the blurred picture and set the field e-mail: [email protected] for further investigation in biogeography and ecology of the organisms in ques- tion, we studied a set of strains of specifically small, colourless, nonscaled chry- Received: 7 March 2014; revised 16 somonad flagellates by means of electron microscopy and molecular analyses. October 2015; accepted November 9, 2015. They were isolated by a filtration-acclimatisation approach focusing on flagellates of around 5 lm. We present the phylogenetic position of eight different lineages doi:10.1111/jeu.12287 on both the ordinal and the generic level. Accordingly, we describe the new genera Apoikiospumella, Chromulinospumella, Segregatospumella, Cornospumella and Acrispumella Boenigk et Grossmann n. g. and different species within them. NONSCALED, coulourless chrysomonad flagellates (=non- nonscaled chrysomonad flagellates are not monophyletic, scaled, colourlesschrysphytes) are major phagotrophs in but have lost photosynthesis at least five times indepen- freshwater and soil food webs (Boenigk and Arndt 2002; dently in different lineages and, thus, became Spumella- Del Campo and Massana 2011; Ekelund et al. 2001; Finlay like in morphology (Boenigk 2008a; Boenigk et al. 2005; and Esteban 1998; Richards and Bass 2005) and are Cavalier-Smith and Chao 2006; Stoeck et al. 2008). The among the dominant feeders on bacteria (Berninger et al. terms “Spumella-like flagellates”, “Spumella-like cells” or 1991; Simek et al. 2013). “Spumella sensu Cienkowsky” often used in the ecologi- Scaled, colourless chrysomonad flagellates have cal literature hint at the current uncertainties and the recently been revised, specifically the genus Para- potential polyphyly of the genus Spumella (Berglund et al. physomonas and the newly erected genus Clathromonas 2005; Boenigk et al. 2005; Charvet et al. 2012; Lepere (Scoble and Cavalier-Smith 2014). Colourless chrysomonad et al. 2006). Eventually, this genus must be divided into taxa lacking surface scales seem to be at least as diverse several genera (Boenigk 2005; Findenig et al. 2010; Scoble (Boenigk 2008b). Due to the lack of surface scales, these and Cavalier-Smith 2014). latter taxa are even harder to distinguish based on morphology. As one consequence, these flagellates have Generic affiliation of colourless, nonscaled often been merged as Spumella spp. (Boenigk 2008a; chrysomonad taxa Boenigk et al. 2005) irrespective of the molecular diversity and polyphyly of this group (Boenigk 2008a) calling for Several colourless, nonscaled chrysophyte genera have major revisions. As rDNA phylogenies suggest, colourless, been described including Spumella Cienkowsky 1870, © 2015 The Author(s). Journal of The Journal of Eukaryotic Microbiology published by Wiley Periodicals, Inc. on behalf of International Society of Protistologists. Journal of Eukaryotic Microbiology 2015, 0, 1–21 1 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. Hidden Diversity in “Spumella-like Flagellates” Grossmann et al. Monas Muller€ 1773, Oikomonas Kent 1880 (also Eucomo- type strain is unavailable and has never been found again. nas or Oicomonas), Synoikomonas Skuja 1964 and Para- However, Ochromonas moestrupii Andersen 2011 is very monas Kent 1880. Several further generic names have similar to O. triangulata and has even been proposed as a been proposed but are considered to be synonyms of one promising candidate for an epitype (Andersen 2011). of the above names, specifically Heterochromulina Based on the presumable monophyly of O. triangulata and Pascher 1912 and Heterochromonas Pascher 1912. O. moestrupii, the molecular affiliation of the type species The genus Monas Muller€ 1773 is one of the first flagel- of Ochromonas can, therefore, be deduced although late genera ever described [Muller€ 1773; “Vermis incon- molecular data for the type species itself are missing. spicuus, simplicissimus, pellucidus, punctiformis” Heterochromonas may be considered sister to the clade (inconspicuous, most simple, transparent and punctiform comprising O. moestrupii, which clusters close to Dino- worm)]. Organisms affiliated with most major branches of bryon in phylogenetic analyses, but not with one of the eukaryotes and even bacteria have subsequently been strains described herein. lumped into this genus. Later, many of these organisms Related to the above case of the genus Hete- have been removed, however, still leaving the genus rochromonas is the potential inclusion of some colourless, Monas as a polyphyletic collection of species and consid- nonscaled chrysomonad flagellates within the genus erable doubts about the identity of its lectotype, Monas Ochromonas. Wysotzki (1887) described two species from mica Muller€ 1773, selected by Diesing (1850). which O. triangulata Wysotzki was designated as lecto- Spumella Cienkowski 1870 has been synonymised with type for the genus by Bourrelly (1957). The polyphyly of Monas Muller€ 1773, but Silva (1960) and later Preisig et al. Ochromonas, as shown in molecular studies, indicates (1991) recommended that the genus Monas should be that there are several genera that have a similar morphol- abandoned because of the uncertainties pertaining to the ogy (i.e. they are naked single cells with two heterody- identity of its lectotype. The strains of Spumella investi- namic flagella, but otherwise are distinctive genetically) gated so far were all characterised by a naked cell surface, (Andersen 2011). Nomenclaturally, the name Ochromonas heterokont flagella emerging from an apical depression will be applied to the clade containing the type species with mastigonemes on the long flagellum, while the short (Andersen 2011). Despite intensive investigations of the flagellum is naked, and mitochondria with tubular cristae. type locality (Lake Veisovo, a salt lake in the Ukraine) by A number of other structures differed between strains; for Andersen 2011, the type species could not be found instance, they may or may not possess a leucoplast, a again. As there are neither sequence data nor type mate- flagellar swelling, an eyespot or mucocysts (Bruchmuller€ rial to make such sequence data available, the molecular 1998; Preisig and Hibberd 1983). Only a few studies have identity of the type species cannot be verified. It is, how- investigated the stomatocysts in colourless, nonscaled ever, very likely that O. moestrupii is a very close relative chrysomonad flagellates with a Spumella–like morphology as it resembles O. triangulata in several ways; further- (Belcher and Swale 1976; Cienkowsky 1870; Findenig more, both species originate from salt water. Based on et al. 2010; Yubuki et al. 2008). Cyst morphology, as well the close resemblance of both species, O. moestrupii has as scale morphology in scaled chrysophycean taxa, is been proposed as a potential epitype and is, therefore, believed to be species-specific and thus a suitable crite- the currently best choice for rooting the genus Ochromo- rion for differentiating species (Findenig et al. 2010; Sand- nas in molecular trees (Andersen 2011). Species which gren 1991). Based on the morphology of stomatocysts, are affiliated with Ochromonas, but are phylogenetically Findenig et al. (2010) designated an epitype for Spumella affiliated with other clades, therefore, probably do not vulgaris Cienkowsky 1870, i.e. for the type species of the belong into the genus Ochromonas and await taxonomic genus. revision. Heterochromonas Pascher 1912 has been proposed as For heterotrophic, nonscaled chrysomonad flagellates a generic name for biflagellated, colourless, and non- with a largely reduced second flagellum the generic scaled chrysomonad flagellates based on the

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