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Phylogenomics Supports the Monophyly of the Cercozoa T ⁎ Nicholas A.T
Molecular Phylogenetics and Evolution 130 (2019) 416–423 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogenomics supports the monophyly of the Cercozoa T ⁎ Nicholas A.T. Irwina, , Denis V. Tikhonenkova,b, Elisabeth Hehenbergera,1, Alexander P. Mylnikovb, Fabien Burkia,2, Patrick J. Keelinga a Department of Botany, University of British Columbia, Vancouver V6T 1Z4, British Columbia, Canada b Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok 152742, Russia ARTICLE INFO ABSTRACT Keywords: The phylum Cercozoa consists of a diverse assemblage of amoeboid and flagellated protists that forms a major Cercozoa component of the supergroup, Rhizaria. However, despite its size and ubiquity, the phylogeny of the Cercozoa Rhizaria remains unclear as morphological variability between cercozoan species and ambiguity in molecular analyses, Phylogeny including phylogenomic approaches, have produced ambiguous results and raised doubts about the monophyly Phylogenomics of the group. Here we sought to resolve these ambiguities using a 161-gene phylogenetic dataset with data from Single-cell transcriptomics newly available genomes and deeply sequenced transcriptomes, including three new transcriptomes from Aurigamonas solis, Abollifer prolabens, and a novel species, Lapot gusevi n. gen. n. sp. Our phylogenomic analysis strongly supported a monophyletic Cercozoa, and approximately-unbiased tests rejected the paraphyletic topologies observed in previous studies. The transcriptome of L. gusevi represents the first transcriptomic data from the large and recently characterized Aquavolonidae-Treumulida-'Novel Clade 12′ group, and phyloge- nomics supported its position as sister to the cercozoan subphylum, Endomyxa. These results provide insights into the phylogeny of the Cercozoa and the Rhizaria as a whole. -
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1 BROADLY SAMPLED TREE OF EUKARYOTIC LIFE Broadly Sampled Multigene Analyses Yield a Well-resolved Eukaryotic Tree of Life Laura Wegener Parfrey1†, Jessica Grant2†, Yonas I. Tekle2,6, Erica Lasek-Nesselquist3,4, Hilary G. Morrison3, Mitchell L. Sogin3, David J. Patterson5, Laura A. Katz1,2,* 1Program in Organismic and Evolutionary Biology, University of Massachusetts, 611 North Pleasant Street, Amherst, Massachusetts 01003, USA 2Department of Biological Sciences, Smith College, 44 College Lane, Northampton, Massachusetts 01063, USA 3Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, 7 MBL Street, Woods Hole, Massachusetts 02543, USA 4Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Providence, Rhode Island 02912, USA 5Biodiversity Informatics Group, Marine Biological Laboratory, 7 MBL Street, Woods Hole, Massachusetts 02543, USA 6Current address: Department of Epidemiology and Public Health, Yale University School of Medicine, New Haven, Connecticut 06520, USA †These authors contributed equally *Corresponding author: L.A.K - [email protected] Phone: 413-585-3825, Fax: 413-585-3786 Keywords: Microbial eukaryotes, supergroups, taxon sampling, Rhizaria, systematic error, Excavata 2 An accurate reconstruction of the eukaryotic tree of life is essential to identify the innovations underlying the diversity of microbial and macroscopic (e.g. plants and animals) eukaryotes. Previous work has divided eukaryotic diversity into a small number of high-level ‘supergroups’, many of which receive strong support in phylogenomic analyses. However, the abundance of data in phylogenomic analyses can lead to highly supported but incorrect relationships due to systematic phylogenetic error. Further, the paucity of major eukaryotic lineages (19 or fewer) included in these genomic studies may exaggerate systematic error and reduces power to evaluate hypotheses. -
New Phylogenomic Analysis of the Enigmatic Phylum Telonemia Further Resolves the Eukaryote Tree of Life
bioRxiv preprint doi: https://doi.org/10.1101/403329; this version posted August 30, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life Jürgen F. H. Strassert1, Mahwash Jamy1, Alexander P. Mylnikov2, Denis V. Tikhonenkov2, Fabien Burki1,* 1Department of Organismal Biology, Program in Systematic Biology, Uppsala University, Uppsala, Sweden 2Institute for Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavl Region, Russia *Corresponding author: E-mail: [email protected] Keywords: TSAR, Telonemia, phylogenomics, eukaryotes, tree of life, protists bioRxiv preprint doi: https://doi.org/10.1101/403329; this version posted August 30, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Abstract The broad-scale tree of eukaryotes is constantly improving, but the evolutionary origin of several major groups remains unknown. Resolving the phylogenetic position of these ‘orphan’ groups is important, especially those that originated early in evolution, because they represent missing evolutionary links between established groups. Telonemia is one such orphan taxon for which little is known. The group is composed of molecularly diverse biflagellated protists, often prevalent although not abundant in aquatic environments. -
A Single Origin of the Photosynthetic Organelle in Different Paulinella Lineages
BMC Evolutionary Biology BioMed Central Research article Open Access A single origin of the photosynthetic organelle in different Paulinella lineages Hwan Su Yoon*†1, Takuro Nakayama†2, Adrian Reyes-Prieto†3, Robert A Andersen1, Sung Min Boo4, Ken-ichiro Ishida2 and Debashish Bhattacharya3 Address: 1Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine, USA, 2Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan, 3Department of Biology and Roy J. Carver Center for Comparative Genomics, University of Iowa, Iowa City, Iowa, USA and 4Department of Biology, Chungnam National University, Daejeon, Korea Email: Hwan Su Yoon* - [email protected]; Takuro Nakayama - [email protected]; Adrian Reyes-Prieto - adrian- [email protected]; Robert A Andersen - [email protected]; Sung Min Boo - [email protected]; Ken- ichiro Ishida - [email protected]; Debashish Bhattacharya - [email protected] * Corresponding author †Equal contributors Published: 13 May 2009 Received: 24 November 2008 Accepted: 13 May 2009 BMC Evolutionary Biology 2009, 9:98 doi:10.1186/1471-2148-9-98 This article is available from: http://www.biomedcentral.com/1471-2148/9/98 © 2009 Yoon et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Gaining the ability to photosynthesize was a key event in eukaryotic evolution because algae and plants form the base of the food chain on our planet. -
Foraminifera and Cercozoa Share a Common Origin According to RNA Polymerase II Phylogenies
International Journal of Systematic and Evolutionary Microbiology (2003), 53, 1735–1739 DOI 10.1099/ijs.0.02597-0 ISEP XIV Foraminifera and Cercozoa share a common origin according to RNA polymerase II phylogenies David Longet,1 John M. Archibald,2 Patrick J. Keeling2 and Jan Pawlowski1 Correspondence 1Dept of zoology and animal biology, University of Geneva, Sciences III, 30 Quai Ernest Jan Pawlowski Ansermet, CH 1211 Gene`ve 4, Switzerland [email protected] 2Canadian Institute for Advanced Research, Department of Botany, University of British Columbia, #3529-6270 University Blvd, Vancouver, British Columbia, Canada V6T 1Z4 Phylogenetic analysis of small and large subunits of rDNA genes suggested that Foraminifera originated early in the evolution of eukaryotes, preceding the origin of other rhizopodial protists. This view was recently challenged by the analysis of actin and ubiquitin protein sequences, which revealed a close relationship between Foraminifera and Cercozoa, an assemblage of various filose amoebae and amoeboflagellates that branch in the so-called crown of the SSU rDNA tree of eukaryotes. To further test this hypothesis, we sequenced a fragment of the largest subunit of the RNA polymerase II (RPB1) from five foraminiferans, two cercozoans and the testate filosean Gromia oviformis. Analysis of our data confirms a close relationship between Foraminifera and Cercozoa and points to Gromia as the closest relative of Foraminifera. INTRODUCTION produces an artificial grouping of Foraminifera with early protist lineages. The long-branch attraction phenomenon Foraminifera are common marine protists characterized by was suggested to be responsible for the position of granular and highly anastomosed pseudopodia (granulo- Foraminifera and some other putatively ancient groups of reticulopodia) and, typically, an organic, agglutinated or protists in rDNA trees (Philippe & Adoutte, 1998). -
Systema Naturae. the Classification of Living Organisms
Systema Naturae. The classification of living organisms. c Alexey B. Shipunov v. 5.601 (June 26, 2007) Preface Most of researches agree that kingdom-level classification of living things needs the special rules and principles. Two approaches are possible: (a) tree- based, Hennigian approach will look for main dichotomies inside so-called “Tree of Life”; and (b) space-based, Linnaean approach will look for the key differences inside “Natural System” multidimensional “cloud”. Despite of clear advantages of tree-like approach (easy to develop rules and algorithms; trees are self-explaining), in many cases the space-based approach is still prefer- able, because it let us to summarize any kinds of taxonomically related da- ta and to compare different classifications quite easily. This approach also lead us to four-kingdom classification, but with different groups: Monera, Protista, Vegetabilia and Animalia, which represent different steps of in- creased complexity of living things, from simple prokaryotic cell to compound Nature Precedings : doi:10.1038/npre.2007.241.2 Posted 16 Aug 2007 eukaryotic cell and further to tissue/organ cell systems. The classification Only recent taxa. Viruses are not included. Abbreviations: incertae sedis (i.s.); pro parte (p.p.); sensu lato (s.l.); sedis mutabilis (sed.m.); sedis possi- bilis (sed.poss.); sensu stricto (s.str.); status mutabilis (stat.m.); quotes for “environmental” groups; asterisk for paraphyletic* taxa. 1 Regnum Monera Superphylum Archebacteria Phylum 1. Archebacteria Classis 1(1). Euryarcheota 1 2(2). Nanoarchaeota 3(3). Crenarchaeota 2 Superphylum Bacteria 3 Phylum 2. Firmicutes 4 Classis 1(4). Thermotogae sed.m. 2(5). -
Lineage-Specific Molecular Probing Reveals Novel Diversity and Ecological Partitioning of Haplosporidians
The ISME Journal (2014) 8, 177–186 & 2014 International Society for Microbial Ecology All rights reserved 1751-7362/14 www.nature.com/ismej ORIGINAL ARTICLE Lineage-specific molecular probing reveals novel diversity and ecological partitioning of haplosporidians Hanna Hartikainen1, Oliver S Ashford1,Ce´dric Berney1, Beth Okamura1, Stephen W Feist2, Craig Baker-Austin2, Grant D Stentiford2,3 and David Bass1 1Department of Life Sciences, The Natural History Museum, London, UK; 2Centre for Environment, Fisheries and Aquaculture Science (Cefas), The Nothe, UK and 3European Union Reference Laboratory for Crustacean Diseases, Centre for Environment, Fisheries and Aquaculture Science (Cefas), The Nothe, UK Haplosporidians are rhizarian parasites of mostly marine invertebrates. They include the causative agents of diseases of commercially important molluscs, including MSX disease in oysters. Despite their importance for food security, their diversity and distributions are poorly known. We used a combination of group-specific PCR primers to probe environmental DNA samples from planktonic and benthic environments in Europe, South Africa and Panama. This revealed several highly distinct novel clades, novel lineages within known clades and seasonal (spring vs autumn) and habitat- related (brackish vs littoral) variation in assemblage composition. High frequencies of haplospor- idian lineages in the water column provide the first evidence for life cycles involving planktonic hosts, host-free stages or both. The general absence of haplosporidian lineages from all large online sequence data sets emphasises the importance of lineage-specific approaches for studying these highly divergent and diverse lineages. Combined with host-based field surveys, environmental sampling for pathogens will enhance future detection of known and novel pathogens and the assessment of disease risk. -
Diversity and Community Structure of Testate Amoebae (Protista) In
DIVERSITY AND COMMUNITY STRUCTURE OF TESTATE AMOEBAE (PROTISTA) IN TROPICAL MONTANE RAIN FORESTS OF SOUTHERN ECUADOR: ALTITUDINAL GRADIENT, ABOVEGROUND HABITATS AND NUTRIENT LIMITATION Vom Fachbereich Biologie der Technischen Universität Darmstadt zur Erlangung des akademischen Grades eines Doctor rerum naturalium genehmigte Dissertation von Dipl.-Biol. Valentyna Krashevs’ka aus Zhovti Vody Berichterstatter: Prof. Dr. Stefan Scheu Mitberichterstatter: PD Dr. Mark Maraun Tag der Einreichung: 24.10.2008 Tag der mündlichen Prüfung: 19.12.2008 Darmstadt 2008 D 17 Für meine Familie „Egal wie weit der Weg ist, man muß den ersten Schritt tun.“ Mao Zedong CONTENTS Summary..........................................................................................................................................I Zusammenfassung.........................................................................................................................III Chapter One – General Introduction 1.1. Tropical montane rain forests...................................................................................................1 1.2. Testate amoebae.......................................................................................................................4 1.3. Objectives...............................................................................................................................10 Chapter Two – Testate amoebae (protista) of an elevational gradient in the tropical mountain rain forest of Ecuador 2.1. Abstract...................................................................................................................................13 -
Marine Biological Laboratory) Data Are All from EST Analyses
TABLE S1. Data characterized for this study. rDNA 3 - - Culture 3 - etK sp70cyt rc5 f1a f2 ps22a ps23a Lineage Taxon accession # Lab sec61 SSU 14 40S Actin Atub Btub E E G H Hsp90 M R R T SUM Cercomonadida Heteromita globosa 50780 Katz 1 1 Cercomonadida Bodomorpha minima 50339 Katz 1 1 Euglyphida Capsellina sp. 50039 Katz 1 1 1 1 4 Gymnophrea Gymnophrys sp. 50923 Katz 1 1 2 Cercomonadida Massisteria marina 50266 Katz 1 1 1 1 4 Foraminifera Ammonia sp. T7 Katz 1 1 2 Foraminifera Ovammina opaca Katz 1 1 1 1 4 Gromia Gromia sp. Antarctica Katz 1 1 Proleptomonas Proleptomonas faecicola 50735 Katz 1 1 1 1 4 Theratromyxa Theratromyxa weberi 50200 Katz 1 1 Ministeria Ministeria vibrans 50519 Katz 1 1 Fornicata Trepomonas agilis 50286 Katz 1 1 Soginia “Soginia anisocystis” 50646 Katz 1 1 1 1 1 5 Stephanopogon Stephanopogon apogon 50096 Katz 1 1 Carolina Tubulinea Arcella hemisphaerica 13-1310 Katz 1 1 2 Cercomonadida Heteromita sp. PRA-74 MBL 1 1 1 1 1 1 1 7 Rhizaria Corallomyxa tenera 50975 MBL 1 1 1 3 Euglenozoa Diplonema papillatum 50162 MBL 1 1 1 1 1 1 1 1 8 Euglenozoa Bodo saltans CCAP1907 MBL 1 1 1 1 1 5 Alveolates Chilodonella uncinata 50194 MBL 1 1 1 1 4 Amoebozoa Arachnula sp. 50593 MBL 1 1 2 Katz lab work based on genomic PCRs and MBL (Marine Biological Laboratory) data are all from EST analyses. Culture accession number is ATTC unless noted. GenBank accession numbers for new sequences (including paralogs) are GQ377645-GQ377715 and HM244866-HM244878. -
1 New Barcoded Primers for Efficient Retrieval of Cercozoan Sequences In
bioRxiv preprint doi: https://doi.org/10.1101/171611; this version posted August 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 New barcoded primers for efficient retrieval of cercozoan sequences in high-throughput environmental diversity surveys, with emphasis on worldwide biological soil crusts Anna Maria Fiore-Donno,a# Christian Rixen,b Martin Rippin,c Karin Glaser,d Elena Samolov,d Ulf Karsten,d Burkhard Becker,c Michael Bonkowskia Institute of Zoology, Terrestrial Ecology, Cluster of Excellence in Plant Sciences, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germanya; Institute for Snow and Avalanche Research SLF, Flüelastrasse 11, 7260 Davos Dorf, Switzerlandb; Institute of Botany, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germanyc; University of Rostock, Institute of Biological Sciences, Applied Ecology and Phycology, Albert-Einstein-Strasse 3, 18059 Rostock, Germanyd. Running title: New barcoded cercozoan primers Correspondence: Anna Maria Fiore-Donno, Institute of Zoology, Department of Terrestrial Ecology, University of Cologne, Zülpicher Str. 47b, 50674 Cologne, Germany; Fax: +492214705038; E-mail: [email protected]. Keywords: Cercozoa, environmental sampling, protists, metabarcoding, 18S V4 variable region. Abstract We describe the performance of a new metabarcoding approach to investigate the environmental diversity of a prominent group of widespread unicellular organisms, the Cercozoa. Cercozoa is an immensely large group of protists and although it may dominate in soil and aquatic ecosystems, its environmental diversity remains undersampled. -
Amoebae and Amoeboid Protists Form a Large and Diverse Assemblage of Eukaryotes Characterized by Various Types of Pseudopodia
J. Eukaryot. Microbiol., 56(1), 2009 pp. 16–25 r 2009 The Author(s) Journal compilation r 2009 by the International Society of Protistologists DOI: 10.1111/j.1550-7408.2008.00379.x Untangling the Phylogeny of Amoeboid Protists1 JAN PAWLOWSKI and FABIEN BURKI Department of Zoology and Animal Biology, University of Geneva, Geneva, Switzerland ABSTRACT. The amoebae and amoeboid protists form a large and diverse assemblage of eukaryotes characterized by various types of pseudopodia. For convenience, the traditional morphology-based classification grouped them together in a macrotaxon named Sarcodina. Molecular phylogenies contributed to the dismantlement of this assemblage, placing the majority of sarcodinids into two new supergroups: Amoebozoa and Rhizaria. In this review, we describe the taxonomic composition of both supergroups and present their small subunit rDNA-based phylogeny. We comment on the advantages and weaknesses of these phylogenies and emphasize the necessity of taxon-rich multigene datasets to resolve phylogenetic relationships within Amoebozoa and Rhizaria. We show the importance of environmental sequencing as a way of increasing taxon sampling in these supergroups. Finally, we highlight the interest of Amoebozoa and Rhizaria for understanding eukaryotic evolution and suggest that resolving their phylogenies will be among the main challenges for future phylogenomic analyses. Key Words. Amoebae, Amoebozoa, eukaryote, evolution, Foraminifera, Radiolaria, Rhizaria, SSU, rDNA. FROM SARCODINA TO AMOEBOZOA AND RHIZARIA ribosomal genes. The most spectacular fast-evolving lineages, HE amoebae and amoeboid protists form an important part of such as foraminiferans (Pawlowski et al. 1996), polycystines Teukaryotic diversity, amounting for about 15,000 described (Amaral Zettler, Sogin, and Caron 1997), pelobionts (Hinkle species (Adl et al. -
Gymnophrys Cometa and Lecythium Sp. Are Core Cercozoa: Evolutionary Implications
Acta Protozool. (2003) 42: 183 - 190 Gymnophrys cometa and Lecythium sp. are Core Cercozoa: Evolutionary Implications Sergey I. NIKOLAEV1, Cédric BERNEY2, José FAHRNI2, Alexander P. MYLNIKOV3, Vladimir V. ALESHIN1, Nikolai B. PETROV1 and Jan PAWLOWSKI2 1A. N. Belozersky Institute of Physico-Chemical Biology, Department of Evolutionary Biochemistry, Moscow State University, Moscow, Russian Federation; 2Department of Zoology and Animal Biology, University of Geneva, Switzerland; 3Institute for Biology of Inland Waters, RAS, Yaroslavskaya obl., Borok, Russian Federation Summary. Recent phylogenetic analyses based on different molecular markers have revealed the existence of the Cercozoa, a group of protists including such morphologically diverse taxa as the cercomonad flagellates, the euglyphid testate filose amoebae, the chloroplast- bearing chlorarachniophytes, and the plasmodiophorid plant pathogens. Molecular data also indicate a close relationship between Cercozoa and Foraminifera (Granuloreticulosea). Little is known, however, about the origin of both groups and their phylogenetic relationships. Here we present the complete small-subunit ribosomal RNA (SSU rRNA) sequence of Gymnophrys cometa, formerly included in the athalamid Granuloreticulosea, as well as that of the test-bearing filose amoeba Lecythium sp. Our study shows that the two organisms clearly belong to the Cercozoa, and indicates that Gymnophrys is not closely related to Foraminifera, supporting the view that Granuloreticulosea sensu lato do not form a natural assemblage. Phylogenetic analyses including most available SSU rRNA sequences from Cercozoa suggest that a rigid, external cell envelope appeared several times independently during the evolution of the group. Furthermore, our results bring additional evidence for the wide morphological variety among Cercozoa, which now also include protists bearing granular pseudopodia and exhibiting mitochondria with flattened cristae.