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Revisions to the Classification, Nomenclature, and Diversity Of Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes Sina M. Adla,* , David Bassb,c , Christopher E. Laned, Julius Lukese,f , Conrad L. Schochg, Alexey Smirnovh, Sabine Agathai, Cedric Berneyj , Matthew W. Brownk,l, Fabien Burkim,PacoCardenas n , Ivan Cepi cka o, Lyudmila Chistyakovap, Javier del Campoq, Micah Dunthornr,s , Bente Edvardsent , Yana Eglitu, Laure Guillouv, Vladimır Hamplw, Aaron A. Heissx, Mona Hoppenrathy, Timothy Y. Jamesz, Anna Karn- kowskaaa, Sergey Karpovh,ab, Eunsoo Kimx, Martin Koliskoe, Alexander Kudryavtsevh,ab, Daniel J.G. Lahrac, Enrique Laraad,ae , Line Le Gallaf , Denis H. Lynnag,ah , David G. Mannai,aj, Ramon Massanaq, Edward A.D. Mitchellad,ak , Christine Morrowal, Jong Soo Parkam , Jan W. Pawlowskian, Martha J. Powellao, Daniel J. Richterap, Sonja Rueckertaq, Lora Shadwickar, Satoshi Shimanoas, Frederick W. Spiegelar, Guifre Torruellaat , Noha Youssefau, Vasily Zlatogurskyh,av & Qianqian Zhangaw a Department of Soil Sciences, College of Agriculture and Bioresources, University of Saskatchewan, Saskatoon, S7N 5A8, SK, Canada b Department of Life Sciences, The Natural History Museum, Cromwell Road, London, SW7 5BD, United Kingdom c Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Barrack Road, The Nothe, Weymouth, Dorset, DT4 8UB, United Kingdom d Department of Biological Sciences, University of Rhode Island, Kingston, Rhode Island, 02881, USA e Institute of Parasitology, Biology Centre, Czech Academy of Sciences, Cesk e Budejovice, 37005, Czechia f Faculty of Science, University of South Bohemia, Cesk e Budejovice, 37005, Czechia g National Institute for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, 20892, USA h Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Saint Petersburg, 199034, Russia i Department of Biosciences, University of Salzburg, Hellbrunnerstrasse 34, Salzburg, A-5020, Austria j CNRS, UMR 7144 (AD2M), Groupe Evolution des Protistes et Ecosystemes Pelagiques, Station Biologique de Roscoff, Place Georges Teissier, Roscoff, 29680, France k Department of Biological Sciences, Mississippi State University, Starkville, 39762, Mississippi, USA l Institute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Starkville, 39762, Mississippi, USA m Department of Organismal Biology, Program in Systematic Biology, Science for Life Laboratory, Uppsala University, Uppsala, 75236, Sweden n Pharmacognosy, Department of Medicinal Chemistry, Uppsala University, BMC Box 574, Uppsala, SE-75123, Sweden o Department of Zoology, Faculty of Science, Charles University, Vinicna 7, Prague, 128 44, Czechia p Core Facility Centre for Culture Collection of Microorganisms, Saint Petersburg State University, Saint Petersburg, 198504, Russia q Institut de Ciencies del Mar, CSIC, Passeig Marıtim de la Barceloneta, 37-49, Barcelona, 08003, Catalonia, Spain r Department of Ecology, University of Kaiserslautern, Erwin-Schroedinger Street, Kaiserslautern, D-67663, Germany s Department of Eukaryotic Microbiology, University of Duisburg-Essen, Universitatsstrasse€ 5, Essen, D-45141, Germany t Department of Biosciences, University of Oslo, P.O. Box 1066 Blindern, Oslo, 0316, Norway u Department of Biology, Dalhousie University, Halifax, B3H 4R2, NS, Canada v Sorbonne Universite, Universite Pierre et Marie Curie - Paris 6, CNRS, UMR 7144 (AD2M), Station Biologique de Roscoff, Place Georges Teis- sier, CS90074, Roscoff, 29688, France w Department of Parasitology, Faculty of Science, Charles University, BIOCEV, Prumyslova 595, Vestec, 252 42, Czechia x Department of Invertebrate Zoology, American Museum of Natural History, New York City, New York, 10024, USA y Senckenberg am Meer, DZMB – German Centre for Marine Biodiversity Research, Wilhelmshaven, 26382, Germany z Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, 48109, USA aa Department of Molecular Phylogenetics and Evolution, University of Warsaw, Warsaw, 02-089, Poland ab Laboratory of Parasitic Worms and Protistology, Zoological Institute RAS, Saint Petersburg, 199034, Russia ac Department of Zoology, Institute of Biosciences, University of Sao Paulo, Matao Travessa 14 Cidade Universitaria, Sao Paulo, 05508-090, Sao Paulo, Brazil ad Laboratory of Soil Biodiversity, University of Neuchatel,^ Rue Emile-Argand 11, Neuchatel,^ 2000, Switzerland ae Real Jardın Botanico, CSIC, Plaza de Murillo 2, Madrid, 28014, Spain af Institut de Systematique, Evolution, Biodiversite, Museum National d’Histoire Naturelle, Sorbonne Universites, 57 rue Cuvier, CP 39, Paris, 75005, France ag Department of Integrative Biology, University of Guelph, Summerlee Science Complex, Guelph, ON, N1G 2W1, Canada ah Department of Zoology, University of British Columbia, 4200-6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada ai Royal Botanic Garden, Edinburgh, EH3 5LR, United Kingdom aj Institute for Agrifood Research and Technology, C/Poble Nou km 5.5, Sant Carles de La Rapita, E-43540, Spain ak Jardin Botanique de Neuchatel,^ Chemin du Perthuis-du-Sault 58, Neuchatel,^ 2000, Switzerland al Department of Natural Sciences, National Museums Northern Ireland, 153 Bangor Road, Holywood, BT18 OEU, United Kingdom © 2018 The Authors Journal of Eukaryotic Microbiology published by Wiley Periodicals, Inc. on behalf of International Society of Protistologists 4 Journal of Eukaryotic Microbiology 2019, 66, 4–119 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Adl et al. Classification of Eukaryotes am Department of Oceanography and Kyungpook Institute of Oceanography, School of Earth System Sciences, Kyungpook National University, Daegu, Korea an Department of Genetics and Evolution, University of Geneva, 1211, Geneva 4, Switzerland ao Department of Biological Sciences, The University of Alabama, Tuscaloosa, Alabama, 35487, USA ap Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marıtim de la Barceloneta 37-49, Barcelona, 08003, Catalonia, Spain aq School of Applied Sciences, Edinburgh Napier University, Edinburgh, EH11 4BN, United Kingdom ar Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas, AR 72701, USA as Science Research Centre, Hosei University, 2-17-1 Fujimi, Chiyoda-ku, Tokyo, 102-8160, Japan at Laboratoire Evolution et Systematique, Universite Paris-XI, Orsay, 91405, France au Department of Microbiology and Molecular Genetics, Oklahoma State University, Stillwater, Oklahoma, 74074, USA av Department of Organismal Biology, Systematic Biology Program, Uppsala University, Uppsala, SE-752 36, Sweden aw Yantai Institute of Coastal Zone Research, Chinese Academy of Science, Yantai, 264003, China Keywords ABSTRACT Algae; amoebae; biodiversity; ciliate; ecol- ogy; flagellate; fungus; microbiology; para- This revision of the classification of eukaryotes follows that of Adl et al., 2012 site; plankton; protozoa; systematics; [J. Euk. Microbiol. 59(5)] and retains an emphasis on protists. Changes since taxonomy. have improved the resolution of many nodes in phylogenetic analyses. For some clades even families are being clearly resolved. As we had predicted, Correspondence environmental sampling in the intervening years has massively increased the S.M. Adl, Department of Soil Sciences, genetic information at hand. Consequently, we have discovered novel clades, College of Agriculture and Bioresources, exciting new genera and uncovered a massive species level diversity beyond University of Saskatchewan, 51 Campus the morphological species descriptions. Several clades known from environ- Drive, Saskatoon, SK, S7N 5A8 Canada mental samples only have now found their home. Sampling soils, deeper mar- Telephone number: 306 966 6866 ine waters and the deep sea will continue to fill us with surprises. The main e-mail: [email protected] changes in this revision are the confirmation that eukaryotes form at least two domains, the loss of monophyly in the Excavata, robust support for the Hap- Received: 2 September 2018; accepted tista and Cryptista. We provide suggested primer sets for DNA sequences September 4, 2018. from environmental samples that are effective for each clade. We have pro- vided a guide to trophic functional guilds in an appendix, to facilitate the inter- doi:10.1111/jeu.12691 pretation of environmental samples, and a standardized taxonomic guide for East Asian users. THIS revision of the classification of eukaryotes updates background information, and to Adl et al. 2007 for a dis- that of the International Society of Protistologists (Adl cussion. Briefly, we adopted a hierarchical system with- et al. 2012). Since then, there has been a massive out formal rank designations. The hierarchy is increase in DNA sequence information of phylogenetic rel- represented by indented paragraphs. The nomenclatural evance from environmental samples. We now have a priority is given to the oldest name (and its authority) that much better sense of the undescribed biodiversity in our correctly assembled genera or higher groups together environment (De Vargas et al. 2015; Pawlowski et al. into a clade, except where its composition was substan- 2012). While significant, it still remains a partial estimation tially modified. In these cases, we have used a
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