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New Classification of the Dictyostelids Sanea Sheikh

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New Classification of the Dictyostelids Sanea Sheikh Washington University in St. Louis Washington University Open Scholarship Biology Faculty Publications & Presentations Biology 2-2018 New Classification of the Dictyostelids Sanea Sheikh Mats Thulin James C. Cavender Ricardo Escalante Shin-ichi Kawakami See next page for additional authors Follow this and additional works at: https://openscholarship.wustl.edu/bio_facpubs Part of the Biology Commons, Molecular Genetics Commons, and the Other Ecology and Evolutionary Biology Commons Recommended Citation Sheikh, Sanea; Thulin, Mats; Cavender, James C.; Escalante, Ricardo; Kawakami, Shin-ichi; Lado, Carlos; Landolt, John C.; Nanjundiah, Vidyanand; Queller, David C.; Strassmann, Joan E.; Spiegel, Frederick W.; Stephenson, Steven L.; Vadell, Eduardo M.; and Baldauf, Sandra L., "New Classification of the Dictyostelids" (2018). Biology Faculty Publications & Presentations. 151. https://openscholarship.wustl.edu/bio_facpubs/151 This Article is brought to you for free and open access by the Biology at Washington University Open Scholarship. It has been accepted for inclusion in Biology Faculty Publications & Presentations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. Authors Sanea Sheikh, Mats Thulin, James C. Cavender, Ricardo Escalante, Shin-ichi Kawakami, Carlos Lado, John C. Landolt, Vidyanand Nanjundiah, David C. Queller, Joan E. Strassmann, Frederick W. Spiegel, Steven L. Stephenson, Eduardo M. Vadell, and Sandra L. Baldauf This article is available at Washington University Open Scholarship: https://openscholarship.wustl.edu/bio_facpubs/151 Manuscript Click here to view linked References 1 2 ORIGINAL PAPER 3 4 A New Classification of the Dictyostelids 5 6 Sanea Sheikha, Mats Thulina, James C. Cavenderb, Ricardo Escalantec, Shin-ichi Kawakamid, 7 Carlos Ladoe, John C. Landoltf, Vidyanand Nanjundiahg, David C. Quellerh, Joan E. 8 Strassmannh, Frederick W. Spiegeli, Steven L. Stephensoni, Eduardo M. Vadellj, and Sandra 9 a,1 10 L. Baldauf 11 12 13 a Programme in Systematic Biology, Uppsala University, Norbyvägen 18D, Uppsala SE- 14 15 75236, Sweden 16 b 17 Departmental of Environmental and Plant Biology, Ohio University, Athens, Ohio 45701, 18 USA 19 c 20 IIB, Instituto de Investigaciones Biomédicas “Alberto Sols”, CSIC-UAM. Arturo Duperier 4, 21 28029-Madrid, Spain 22 d 23 Yamagata Prefectural Museum, 1-8 Kajo-machi, Yamagata-shi, Yamagata-ken 990-0826, 24 Japan 25 e 26 Real Jardín Botánico de Madrid, CSIC, Plaza de Murillo 2, 28014 Madrid, Spain 27 f 28 Department of Biology, Shepherd University, Shepherdstown, West Virginia 25443, USA 29 g 30 Centre for Human Genetics, BioTech Park, Electronic City (Phase I), Bangalore 560100, 31 India 32 h 33 Department of Biology, Washington University in Saint Louis, Campus Box 1137, One 34 Brookings Drive, Saint Louis, MO, USA 35 i 36 Department of Biological Sciences, SCEN 601, 850 W. Dickson 1, University of Arkansas, 37 Fayetteville, AR 72701 USA 38 39 jEscuela de Farmacia y Bioquímica, J.F. Kennedy University, Buenos Aires, Argentina 40 41 42 43 Submitted March 3, 2017; Accepted October 17, 2017 44 45 Monitoring Editor: Alastair Simpson 46 47 48 49 Running title: New Classification of Dictyostelids 50 51 52 1 53 Corresponding author; e-mail [email protected] (S. L. Baldauf). 54 55 56 57 58 59 60 61 62 63 64 65 1 2 Traditional morphology-based taxonomy of dictyostelids is rejected by molecular 3 4 phylogeny. A new classification is presented based on monophyletic entities with 5 consistent and strong molecular phylogenetic support and that are, as far as possible, 6 7 morphologically recognizable. All newly named clades are diagnosed with small subunit 8 ribosomal RNA (18S rRNA) sequence signatures plus morphological synapomorphies 9 10 where possible. The two major molecular clades are given the rank of order, as 11 Acytosteliales ord. nov. and Dictyosteliales. The two major clades within each of these 12 13 orders are recognized and given the rank of family as, respectively, Acytosteliaceae and 14 15 Cavenderiaceae fam. nov. in Acytosteliales, and Dictyosteliaceae and Raperosteliaceae 16 fam. nov. in Dictyosteliales. Twelve genera are recognized: Cavenderia gen. nov. in 17 18 Cavenderiaceae, Acytostelium, Rostrostelium gen. nov. and Heterostelium gen. nov. in 19 Acytosteliaceae, Tieghemostelium gen. nov., Hagiwaraea gen. nov., Raperostelium gen. 20 21 nov. and Speleostelium gen. nov. in Raperosteliaceae, and Dictyostelium and 22 Polysphondylium in Dictyosteliaceae. The “polycephalum” complex is treated as 23 24 Coremiostelium gen. nov. (not assigned to family) and the “polycarpum” complex as 25 Synstelium gen. nov. (not assigned to order and family). Coenonia, which may not be a 26 27 dictyostelid, is treated as a genus incertae sedis. Eighty-eight new combinations are 28 29 made at species and variety level, and Dictyostelium ammophilum is validated. 30 31 32 33 Key words: Classification; dictyostelids; molecular characters; nomenclature; phylogeny; 34 taxonomy. 35 36 37 38 39 Introduction 40 41 42 Dictyostelids are heterotrophic amoebae, also known informally as cellular slime molds or 43 44 social amoebae. They are commonly isolated from a variety of soils worldwide and are 45 46 ecologically important as predators of soil bacteria. Dictyostelids are particularly well known 47 and widely studied because of their lifestyle, which alternates regularly between unicellular 48 49 and multicellular (sorocarpic) stages. This “aggregative multicellular” behaviour has also led 50 to their widespread use as molecular and evolutionary models, beginning largely with 51 52 Dictyostelium discoideum but now including a handful of taxa from across the phylogeny 53 (Singh et al. 2015). The identification and taxonomy of dictyostelids has traditionally been 54 55 56 57 58 59 60 61 62 63 64 65 1 2 based on the morphology of their sorocarps and related characters, as their amoebae appear to 3 4 be indistinguishable. While new species continue to be identified based on morphological 5 characters (e.g. Cavender et al. 2016), molecular phylogeny indicates that much of the 6 7 traditional taxonomy is fundamentally flawed, particularly at the deepest taxonomic levels. 8 Therefore, major taxonomic revision has been needed for some time. 9 10 11 The first dictyostelid was isolated and described by Oskar Brefeld as 12 Dictyostelium mucoroides (Brefeld 1869), the genus name from the Greek “dictyon” (net) and 13 14 “stele” (column) referring to the net-like appearance of the cells in the stalks of the 15 fructifications (sorocarps). By the end of the 19th century three further species of 16 17 Dictyostelium had been described, D. lacteum and D. roseum by van Tieghem (1880), and D. 18 sphaerocephalum by Saccardo and Marchal (Marchal 1885), the latter based on Hyalostilbum 19 20 sphaerocephalum (Oudemans 1885). Two new genera were also added, Coenonia with the 21 C. denticulata Polysphondylium 22 single species (van Tieghem 1884) and with the single 23 species P. violaceum (Brefeld 1884). Coenonia was characterized, in part, by the crampon- 24 25 shaped base of the stalks and by the cupule-like structure containing the spores, whereas 26 Polysphondylium was characterized, above all, by whorls of regularly spaced side branches on 27 28 the main axial stalk of the sorocarp. In 1900 dictyostelids were known from Europe only, but 29 since then well over a hundred species of Dictyostelium and more than 30 species of 30 31 Polysphondylium have been described from all over the world (see Raper 1984 for an 32 excellent summary of the period up to then). In addition, one further genus was added, 33 34 Acytostelium (Raper 1956), characterized mainly by the acellular stalks of the sorocarps. This 35 36 differs from all other dictyostelids, in which a substantial portion of the aggregate is sacrificed 37 to form a stalk composed of dead cells. Acytostelium has 16 described species to date, and 38 39 new species of Dictyostelium, Polysphondylium and Acytostelium are being added 40 continuously. However, the enigmatic Coenonia denticulata was lost and never recollected 41 42 (Raper 1984) and the genus remains monospecific, with no available material. 43 44 During the last 15 years, increasingly refined cladistic analyses (Swanson et al. 45 46 2002) together with molecular phylogenetics (Romeralo et al. 2007, 2011; Schaap et al. 2006; 47 Sheikh et al. 2014; Singh et al. 2016) have shown that the traditional, morphology-based 48 49 taxonomy of the dictyostelids does not reflect phylogenetic relationships. Instead of three 50 genera, eight distinct molecular clades have been consistently and robustly identified based 51 52 primarily on well-resolved small subunit ribosomal RNA (SSU rRNA) trees (Romeralo et al. 53 2011; Schaap et al. 2006). Where tested, these relationships have also been confirmed by 54 55 56 57 58 59 60 61 62 63 64 65 1 2 cladistics analysis of morphological characters (Swanson et al. 2002) and/or molecular 3 4 phylogeny based on alpha-tubulin (atub) and atub + SSU rRNA (Schaap et al. 2006), 5 internally transcribed spacer (ITS) + 5.8S rRNA (Romeralo et al. 2007), ITS + SSU rRNA 6 7 (Romeralo et al. 2011), and multi-protein phylogeny (Romeralo et al. 2013; Sheikh et al. 8 2015; Singh et al. 2016). 9 10 11 Most importantly, none of the eight main molecular clades correspond to 12 traditional genera. Until now, these clades have been informally denoted as Groups 1, 2A, 2B, 13 14 3, and 4, plus complexes “polycarpum”,
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