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Euglenozoa: Taxonomy, Diversity and Ecology, Symbioses and Viruses

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Euglenozoa: Taxonomy, Diversity and Ecology, Symbioses and Viruses Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses † † † royalsocietypublishing.org/journal/rsob Alexei Y. Kostygov1,2, , Anna Karnkowska3, , Jan Votýpka4,5, , Daria Tashyreva4,†, Kacper Maciszewski3, Vyacheslav Yurchenko1,6 and Julius Lukeš4,7 1Life Science Research Centre, Faculty of Science, University of Ostrava, Ostrava, Czech Republic Review 2Zoological Institute, Russian Academy of Sciences, St Petersburg, Russia 3Institute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Cite this article: Kostygov AY, Karnkowska A, Warsaw, Warsaw, Poland 4 Votýpka J, Tashyreva D, Maciszewski K, Institute of Parasitology, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic 5Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic Yurchenko V, Lukeš J. 2021 Euglenozoa: 6Martsinovsky Institute of Medical Parasitology, Tropical and Vector Borne Diseases, Sechenov University, taxonomy, diversity and ecology, symbioses Moscow, Russia and viruses. Open Biol. 11: 200407. 7Faculty of Sciences, University of South Bohemia, České Budějovice (Budweis), Czech Republic https://doi.org/10.1098/rsob.200407 AYK, 0000-0002-1516-437X; AK, 0000-0003-3709-7873; KM, 0000-0001-8556-9500; VY, 0000-0003-4765-3263; JL, 0000-0002-0578-6618 Euglenozoa is a species-rich group of protists, which have extremely diverse Received: 19 December 2020 lifestyles and a range of features that distinguish them from other eukar- Accepted: 8 February 2021 yotes. They are composed of free-living and parasitic kinetoplastids, mostly free-living diplonemids, heterotrophic and photosynthetic euglenids, as well as deep-sea symbiontids. Although they form a well-supported monophyletic group, these morphologically rather distinct groups are almost never treated together in a comparative manner, as attempted here. Subject Area: We present an updated taxonomy, complemented by photos of repre- cellular biology/microbiology sentative species, with notes on diversity, distribution and biology of euglenozoans. For kinetoplastids, we propose a significantly modified tax- Keywords: onomy that reflects the latest findings. Finally, we summarize what is Euglenida, Kinetoplastida, Diplonemida, known about viruses infecting euglenozoans, as well as their relationships with ecto- and endosymbiotic bacteria. microbial eukaryotes, systematics, phylogeny Author for correspondence: 1. Introduction š Julius Luke It is generally accepted that Euglenozoa belong to the most unusual eukaryotes [1– e-mail: [email protected] 3]. This is based on a substantial body of evidence showing that in a number of cellular processes and structures, these almost invariably mono- or bi-flagellated protists departed from what can be considered the ‘eukaryotic consensus’.How- ever, this consensus was defined by the studies of just a handful of model organisms, most of which are multicellular [4]. Hence, since the majority of the extant eukaryotic diversity is hidden in protists [5], we prefer to use a ‘protist-cen- tric’ view, which postulates that these unicellular forms actually are the eukaryotic standard, while the other lineages represent departures from the norm. The phylum Euglenozoa splits into three well-defined lineages—euglenids, kinetoplastids and diplonemids—with different life strategies and distinct mor- phologies, yet still unified by a number of common features [6]. Although the euglenids are sometimes further subdivided into Euglenida and Symbiontida [3], both groups are usually treated together due to their morphological simi- larity, and we still cannot compare their genomic features in the absence of † such data from the latter taxon [7]. A recent multigene phylogenetic reconstruc- These authors contributed equally to this tion pointed to the potentially sister relationship between Symbiontida and study. Glycomonada (Kinetoplastea + Diplonemea) [8], suggesting that Symbiontida may become a separate group when more data become available (tree A). © 2021 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Euglenida the euglenozoan common ancestor, euglenids, diplonemids 2 and kinetoplastids have acquired significant differences royalsocietypublishing.org/journal/rsob over the course of evolution. This is particularly striking in the case of cis-splicing, since spliceosomal introns are E almost absent in the latter group [20], while they are abun- U G dantly present in euglenids and diplonemids, many being Symbiontida L seemingly non-canonical [11,21]. Another clear difference E rests in the size of both nuclear and mitochondrial genomes. N G The dearth of high-quality data for nuclear genomes of eugle- Diplonemea L O Y Z nids and their absence in the case of diplonemids are due to C O the large size and repetitive character of the latter. The tran- O A M scriptomes from both groups contain an extremely high O number of protein-coding genes, probably reflecting their N A metabolic versatility [6,13]. The situation is quite different Open Biol. Kinetoplastea D in kinetoplastids, the parasitic lifestyle of which led to gene A reduction and streamlining [6]. Moreover, due to their small Tree A. Euglenozoa. A consensus tree based on multiple phylogenetic recon- and compact genomes, they belong to the most sequenced 11 structions showing relationships among major clades. The unstable position of eukaryotes [22]. : 200407 Symbiontida is marked with a dotted line and further described in the section Unexpected differences among the main euglenozoan on euglenid taxonomy. lineages recently became apparent for their mitochondrial genomes and transcriptomes. Kinetoplastids harbour in their mitochondrial DNA in the form of relaxed (rarely super- Apart from summarizing taxonomic works, the eugle- coiled) circular molecules, either catenated or free, of two nozoans are almost never treated together in the literature. types—maxicircles and minicircles, with the former carrying The kinetoplastid flagellates are by far the best-studied repre- all protein-coding genes, while the latter encode guide RNA sentatives (almost exclusively from a parasitology-centric genes required for the editing of the maxicircle transcripts perspective), with most attention given to the causative [23]. The size of maxicircles is rather uniform, while the mini- agents of serious diseases, such as sleeping sickness, circles come in different variants [24]. In diplonemids, the Chagas disease and leishmaniases [9,10]. The diplonemids, single type of non-catenated circles uniquely encodes frag- as detailed below, were considered a marginal group with ments of protein-coding genes, the transcripts of which no ecological relevance. That has changed recently [11,12], have to be massively trans-spliced and edited in order to but still very few molecular data other than 18S rRNA are become translatable [25]. However, in both groups, the mito- available for this almost exclusively marine group. Finally, chondrial DNA is inflated, and its transcripts are extensively the photosynthetic and heterotrophic euglenids are ecologi- edited [26]. This contrasts with euglenids that lack any form cally significant, primarily in freshwater ecosystems, and of editing in their mitochondrion, which also contains a small have potential in biotechnologies [2,13]. genome composed of heavily fragmented linear molecules The striking differences in lifestyles and cellular (ultra)- [27]. Probably, the most important difference among these structure obscure the significant similarities in basic groups is the presence of a secondary green plastid solely molecular processes. Firstly, all these groups distinguish in euglenids, which have acquired it after their divergence themselves from other eukaryotes by transcribing nuclear from other euglenozoans [2,28]. genes in a polycistronic manner [14]. In neither case are the Until recently, our knowledge of different groups within co-transcribed genes functionally related, which dis- euglenozoans was much influenced by the availability of tinguishes them from the prokaryotic operons. The usually full-size nuclear genome sequences. While hundreds of very long polycistronic mRNA is subsequently processed high-quality genomes are available for trypanosomatids into monomeric transcripts, which are subject to another [22], only one such genome is available for bodonids [29] process that is found in eukaryotes rather infrequently— and euglenids [13], respectively, and none for diplonemids. trans-splicing. At the 50 end of each monocistronic mRNA, However, this is bound to change soon, mostly due to the short spliced leader (SL) RNA, already equipped with a ever-decreasing costs and improving sequencing technol- methylated cap, becomes attached. The corresponding SL ogies. Recent comparative analyses of molecular features RNA gene is invariably multicopy, and highly conserved, among kinetoplastids, euglenids and diplonemids were yet with minor species-specific differences [15]. based on transcriptomes available for all of them [30]. The similarities do not stop there. In their single or dual Future studies of euglenozoans will be heavily influenced flagella, all euglenozoans evolved an extra-axonemal struc- by the accessibility of their representatives to (efficient) gen- ture termed the paraflagellar rod, which supports their etic manipulations.
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