The Twilight of Heliozoa and Rise of Rhizaria, an Emerging Supergroup of Amoeboid Eukaryotes

Total Page:16

File Type:pdf, Size:1020Kb

The Twilight of Heliozoa and Rise of Rhizaria, an Emerging Supergroup of Amoeboid Eukaryotes The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes Sergey I. Nikolaev†,Ce´ dric Berney‡, Jose´ F. Fahrni‡, Ignacio Bolivar‡, Stephane Polet‡, Alexander P. Mylnikov§, Vladimir V. Aleshin†, Nikolai B. Petrov†, and Jan Pawlowski‡¶ †A. N. Belozersky Institute of Physico-Chemical Biology, Department of Evolutionary Biochemistry, Moscow State University, Moscow 119992, Russia; ‡Department of Zoology and Animal Biology, University of Geneva, 1211 Geneva 4, Switzerland; and §Institute for Biology of Inland Waters, Russian Academy of Sciences, Yaroslavskaya oblast, Borok 152742, Russia Edited by W. Ford Doolittle, Dalhousie University, Halifax, Nova Scotia, Canada, and approved April 9, 2004 (received for review December 23, 2003) Recent molecular phylogenetic studies revealed the extraordinary heterogeneous class, which comprised from five (12) to eight diversity of single-celled eukaryotes. However, the proper assess- (13) orders. However, based on differences in the patterns of ment of this diversity and accurate reconstruction of the eukaryote ultrastructural organization, it has also been proposed that phylogeny are still impeded by the lack of molecular data for some Heliozoa are composed of several evolutionarily unrelated major groups of easily identifiable and cultivable protists. Among groups (14, 15). In a recent classification of protists, four them, amoeboid eukaryotes have been notably absent from mo- monophyletic heliozoan orders have been distinguished (Acti- lecular phylogenies, despite their diversity, complexity, and abun- nophryida, Centrohelida, Desmothoracida, and Gymnospha- dance. To partly fill this phylogenetic gap, we present here com- erida), whereas the rest of heliozoan-like taxa, including Sti- bined small-subunit ribosomal RNA and actin sequence data for the cholonche zanclea, the only member of the order Taxopodida, three main groups of ‘‘Heliozoa’’ (Actinophryida, Centrohelida, was classified as ‘‘other Heliozoa’’ (16). and Desmothoracida), the heliozoan-like Sticholonche, and the The advent of molecular phylogenies did little to resolve the radiolarian group Polycystinea. Phylogenetic analyses of our se- position of Actinopoda in the tree of life. The first analysis of quences demonstrate the polyphyly of heliozoans, which branch SSU rRNA gene sequences of the radiolarian Acantharea and either as an independent eukaryotic lineage (Centrohelida), within Polycystinea suggested an independent origin for these groups stramenopiles (Actinophryida), or among cercozoans (Desmotho- (17), yet more recent analyses challenged this result using racida), in broad agreement with previous ultrastructure-based environmental SSU rRNA gene sequences (18). The first SSU studies. Our data also provide solid evidence for the existence of rRNA sequences of the heliozoan order Centrohelida and of a the Rhizaria, an emerging supergroup of mainly amoeboid eu- Dimorpha-like strain were only recently published (19, 20). karyotes that includes desmothoracid heliozoans, all radiolarians, Finally, we obtained very recently the first SSU rRNA data on Sticholonche, and foraminiferans, as well as various filose and the third group of radiolarians, the Phaeodarea, revealing that reticulose amoebae and some flagellates. this taxon is not related to acanthareans and polycystines (21). However, SSU rRNA gene sequence data are still lacking for olecular phylogenetic studies have demonstrated the ex- most heliozoans, and there are no protein data available yet for Mistence of an extraordinary diversity of unicellular eu- any member of the Actinopoda. karyotes, which form up to eight major groups in the eukaryotic To fill this gap and to unravel the origins of the different tree of life (1, 2). This diversity might even be higher, according axopodia-bearing protists, we obtained and analyzed sequence to recent environmental DNA studies that revealed a number of data for most groups classically belonging to Actinopoda. Our extremely small undescribed taxa among these major groups, as study includes previously undescribed SSU rRNA and actin gene well as some candidate phylotypes representing new higher-level sequences for representatives of the three main orders of diversity among eukaryotes (3, 4). However, the proper assess- Heliozoa (Actinophryida, Centrohelida, and Desmothoracida), ment of this diversity is impeded by the fact that there are still the SSU rRNA gene sequence of the taxopodid S. zanclea, as well numerous major groups of easily identifiable and cultivable as actin gene sequences for two species of Polycystinea and the protists for which only little or no molecular data exist (2). DNA filose amoebae Gromia oviformis (Cercozoa: Gromiidae), sequences are particularly scarce for amoeboid eukaryotes. Only Lecythium sp. (Cercozoa: Chlamydophryidae), and Nuclearia recently did sequence data for a broad taxonomic sampling of simplex (Opisthokonts: Nucleariidae). lobose amoebae become available (5–7). Here, we present Materials and Methods combined small-subunit ribosomal RNA (SSU rRNA) and actin Cell Cultures, DNA, and RNA Extractions. genes sequence data for the main groups of heliozoans and Cultures of the desmotho- radiolarians, which together form the bulk of axopodia-bearing racids Clathrulina elegans and Hedriocystis cf. spinifera, the protists (the Actinopoda), the last group of amoeboid protists freshwater centrohelids Chlamydaster sterni and Pterocystis eri- naceoides Heterophrys marina remaining largely unexplored at the molecular level. , the marine centrohelid , and the Lecythium Traditionally, all free-living heterotrophic protists character- filose amoeba sp. were taken from the culture col- lection of the Institute for the Biology of Inland Waters of the ized by long radial axopodia supported by a bundle of microtu- Russian Academy of Sciences (IBIW RAS). Cultures of the bules were grouped into the superclass Actinopoda (8). This centrohelid Raphidiophrys ambigua; the actinophryids Actino- group included the marine, usually planktonic, radiolarians and the primarily freshwater heliozoans, also called sun-animalcules. Originally, Radiolaria were classified by Ernst Haeckel (9) into This paper was submitted directly (Track II) to the PNAS office. three groups: Acantharea, Phaeodarea, and Polycystinea, con- Abbreviations: BV, bootstrap support value; ML, maximum likelihood; PP, posterior prob- sidered later as three independent classes based on differences ability; SSU rRNA, small-subunit ribosomal RNA. in the composition of the skeleton and the structure of the Data deposition: The sequences reported in this paper have been deposited in the Gen- central capsule (10). The Heliozoa, another group described by Bank͞EMBL database (accession nos. AY268041–AY26843, AY268045, AY283744– Haeckel (11), included initially only two freshwater actinophry- AY283746, AY283754–AY283762, AY305008–AY305013, and AY507123–AY507125). ids, Actinophrys and Actinosphaerium. Later, several other ax- ¶To whom correspondence should be addressed. E-mail: [email protected]. opodia-bearing protists were added to this taxon, forming a large © 2004 by The National Academy of Sciences of the USA 8066–8071 ͉ PNAS ͉ May 25, 2004 ͉ vol. 101 ͉ no. 21 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0308602101 Downloaded by guest on September 24, 2021 sphaerium eichhornii, Actinosphaerium nucleofilum, and Acti- tances and was used as a starting tree for the ML search, then nophrys sol; and the filose amoeba N. simplex were taken from swapped with the tree-bisection-reconnection algorithm. The the Culture Collection of Algae and Protozoa (CCAP) culture reliability of internal branches was assessed by using the poste- collection. Freshwater cultures were maintained on artificial rior probabilities (PP) calculated with MRBAYES. Additionally, ͞ ϫ ͞ Pratt medium (KNO3 0.1‰ K2HPO4 3H2O 0.01‰ MgSO4 the bootstrap method (30) was used with 1,000 replicates for ϫ ͞ ϫ 7H2O 0.01‰ FeCl3 6H2O 0.001‰, pH 6.5–7.5). Marine distance analyses, performed with PAUP* as described above. cultures were maintained on artificial Shmaltz–Pratt medium The actin protein sequences were manually aligned by using ͞ ͞ ϫ ͞ ϫ (NaCl 16.07‰ KCl 0.38‰ MgCl2 6H2O 3.15‰ MgSO4 GDE. Sequences from public databases were selected so that all ͞ ϫ ͞ ͞ ϫ 7H2O 3.95‰ CaCl2 H2O 0.83‰ KNO3 0.06‰ K2HPO4 available taxonomic groups of eukaryotes were represented, 3H2O 0.006‰,pH6.5–7.5). Marine heliozoans from the IBIW but the highly diverging actin sequences of ciliates, microspo- RAS culture collection were fed with Procryptobia sorokini, and ridians, diplomonads, and trichomonads were discarded. Sixty- marine heliozoans from the CCAP culture collection were fed eight sequences were included, and a total of 241 amino acid with Tetrahymena sp. The freshwater heliozoans were fed with positions were used in the phylogenetic analyses. A Bayesian Bodo saltans. All food sources were cultivated separately from analysis of the data was performed with MRBAYES by using the their predator and fed with Aerobacter aerogenes. The taxopodid Whelan and Goldman (WAG) substitution matrix (31) and S. zanclea and the polycystines Collozoum inerme and Thalassi- taking into account a proportion of invariable sites and a colla pellucida were collected in the Mediterranean Sea (Ville- ␥-shaped distribution of the rates of substitution among vari- franche-sur-Mer, France). These species were processed directly able sites, with eight rate categories. Two million seven after isolation; the DNA extracts
Recommended publications
  • Molecular Phylogenetic Position of Hexacontium Pachydermum Jørgensen (Radiolaria)
    Marine Micropaleontology 73 (2009) 129–134 Contents lists available at ScienceDirect Marine Micropaleontology journal homepage: www.elsevier.com/locate/marmicro Molecular phylogenetic position of Hexacontium pachydermum Jørgensen (Radiolaria) Tomoko Yuasa a,⁎, Jane K. Dolven b, Kjell R. Bjørklund b, Shigeki Mayama c, Osamu Takahashi a a Department of Astronomy and Earth Sciences, Tokyo Gakugei University, Koganei, Tokyo 184-8501, Japan b Natural History Museum, University of Oslo, P.O. Box 1172, Blindern, 0318 Oslo, Norway c Department of Biology, Tokyo Gakugei University, Koganei, Tokyo 184-8501, Japan article info abstract Article history: The taxonomic affiliation of Hexacontium pachydermum Jørgensen, specifically whether it belongs to the Received 9 April 2009 order Spumellarida or the order Entactinarida, is a subject of ongoing debate. In this study, we sequenced the Received in revised form 3 August 2009 18S rRNA gene of H. pachydermum and of three spherical spumellarians of Cladococcus viminalis Haeckel, Accepted 7 August 2009 Arachnosphaera myriacantha Haeckel, and Astrosphaera hexagonalis Haeckel. Our molecular phylogenetic analysis revealed that the spumellarian species of C. viminalis, A. myriacantha, and A. hexagonalis form a Keywords: monophyletic group. Moreover, this clade occupies a sister position to the clade comprising the spongodiscid Radiolaria fi Entactinarida spumellarians, coccodiscid spumellarians, and H. pachydermum. This nding is contrary to the results of Spumellarida morphological studies based on internal spicular morphology, placing H. pachydermum in the order Nassellarida Entactinarida, which had been considered to have a common ancestor shared with the nassellarians. 18S rRNA gene © 2009 Elsevier B.V. All rights reserved. Molecular phylogeny. 1. Introduction the order Entactinarida has an inner spicular system homologenous with that of the order Nassellarida.
    [Show full text]
  • Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life
    Smith ScholarWorks Biological Sciences: Faculty Publications Biological Sciences 10-1-2010 Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life Laura Wegener Parfrey University of Massachusetts Amherst Jessica Grant Smith College Yonas I. Tekle Smith College Erica Lasek-Nesselquist Marine Biological Laboratory Hilary G. Morrison Marine Biological Laboratory See next page for additional authors Follow this and additional works at: https://scholarworks.smith.edu/bio_facpubs Part of the Biology Commons Recommended Citation Parfrey, Laura Wegener; Grant, Jessica; Tekle, Yonas I.; Lasek-Nesselquist, Erica; Morrison, Hilary G.; Sogin, Mitchell L.; Patterson, David J.; and Katz, Laura A., "Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life" (2010). Biological Sciences: Faculty Publications, Smith College, Northampton, MA. https://scholarworks.smith.edu/bio_facpubs/126 This Article has been accepted for inclusion in Biological Sciences: Faculty Publications by an authorized administrator of Smith ScholarWorks. For more information, please contact [email protected] Authors Laura Wegener Parfrey, Jessica Grant, Yonas I. Tekle, Erica Lasek-Nesselquist, Hilary G. Morrison, Mitchell L. Sogin, David J. Patterson, and Laura A. Katz This article is available at Smith ScholarWorks: https://scholarworks.smith.edu/bio_facpubs/126 Syst. Biol. 59(5):518–533, 2010 c The Author(s) 2010. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: [email protected] DOI:10.1093/sysbio/syq037 Advance Access publication on July 23, 2010 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, 3 3 5 1,2, HILARY G.
    [Show full text]
  • Sex Is a Ubiquitous, Ancient, and Inherent Attribute of Eukaryotic Life
    PAPER Sex is a ubiquitous, ancient, and inherent attribute of COLLOQUIUM eukaryotic life Dave Speijera,1, Julius Lukešb,c, and Marek Eliášd,1 aDepartment of Medical Biochemistry, Academic Medical Center, University of Amsterdam, 1105 AZ, Amsterdam, The Netherlands; bInstitute of Parasitology, Biology Centre, Czech Academy of Sciences, and Faculty of Sciences, University of South Bohemia, 370 05 Ceské Budejovice, Czech Republic; cCanadian Institute for Advanced Research, Toronto, ON, Canada M5G 1Z8; and dDepartment of Biology and Ecology, University of Ostrava, 710 00 Ostrava, Czech Republic Edited by John C. Avise, University of California, Irvine, CA, and approved April 8, 2015 (received for review February 14, 2015) Sexual reproduction and clonality in eukaryotes are mostly Sex in Eukaryotic Microorganisms: More Voyeurs Needed seen as exclusive, the latter being rather exceptional. This view Whereas absence of sex is considered as something scandalous for might be biased by focusing almost exclusively on metazoans. a zoologist, scientists studying protists, which represent the ma- We analyze and discuss reproduction in the context of extant jority of extant eukaryotic diversity (2), are much more ready to eukaryotic diversity, paying special attention to protists. We accept that a particular eukaryotic group has not shown any evi- present results of phylogenetically extended searches for ho- dence of sexual processes. Although sex is very well documented mologs of two proteins functioning in cell and nuclear fusion, in many protist groups, and members of some taxa, such as ciliates respectively (HAP2 and GEX1), providing indirect evidence for (Alveolata), diatoms (Stramenopiles), or green algae (Chlor- these processes in several eukaryotic lineages where sex has oplastida), even serve as models to study various aspects of sex- – not been observed yet.
    [Show full text]
  • Rare Phytomyxid Infection on the Alien Seagrass Halophila Stipulacea In
    Research Article Mediterranean Marine Science Indexed in WoS (Web of Science, ISI Thomson) and SCOPUS The journal is available on line at http://www.medit-mar-sc.net DOI: http://dx.doi.org/10.12681/mms.14053 Rare phytomyxid infection on the alien seagrass Halophila stipulacea in the southeast Aegean Sea MARTIN VOHNÍK1,2, ONDŘEJ BOROVEC1,2, ELIF ÖZGÜR ÖZBEK3 and EMINE ŞÜKRAN OKUDAN ASLAN4 1 Department of Mycorrhizal Symbioses, Institute of Botany, Czech Academy of Sciences, Průhonice, 25243 Czech Republic 2 Department of Plant Experimental Biology, Faculty of Science, Charles University, Prague, 12844 Czech Republic 3 Marine Biology Museum, Antalya Metropolitan Municipality, Antalya, Turkey 4 Department of Marine Biology, Faculty of Fisheries, Akdeniz University, Antalya, Turkey Corresponding author: [email protected] Handling Editor: Athanasios Athanasiadis Received: 31 May 2017; Accepted: 9 October 2017; Published on line: 8 December 2017 Abstract Phytomyxids (Phytomyxea) are obligate endosymbionts of many organisms such as algae, diatoms, oomycetes and higher plants including seagrasses. Despite their supposed significant roles in the marine ecosystem, our knowledge of their marine diversity and distribution as well as their life cycles is rather limited. Here we describe the anatomy and morphology of several developmental stages of a phytomyxid symbiosis recently discovered on the petioles of the alien seagrass Halophila stipulacea at a locality in the southeast Aegean Sea. Its earliest stage appeared as whitish spots already on the youngest leaves at the apex of the newly formed rhizomes. The infected host cells grew in volume being filled with plasmodia which resulted in the formation of characteristic macroscopic galls.
    [Show full text]
  • Rhizaria, Cercozoa)
    Protist, Vol. 166, 363–373, July 2015 http://www.elsevier.de/protis Published online date 28 May 2015 ORIGINAL PAPER Molecular Phylogeny of the Widely Distributed Marine Protists, Phaeodaria (Rhizaria, Cercozoa) a,1 a a b Yasuhide Nakamura , Ichiro Imai , Atsushi Yamaguchi , Akihiro Tuji , c d Fabrice Not , and Noritoshi Suzuki a Plankton Laboratory, Graduate School of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido 041–8611, Japan b Department of Botany, National Museum of Nature and Science, Tsukuba 305–0005, Japan c CNRS, UMR 7144 & Université Pierre et Marie Curie, Station Biologique de Roscoff, Equipe EPPO - Evolution du Plancton et PaléoOcéans, Place Georges Teissier, 29682 Roscoff, France d Institute of Geology and Paleontology, Graduate School of Science, Tohoku University, Sendai 980–8578, Japan Submitted January 1, 2015; Accepted May 19, 2015 Monitoring Editor: David Moreira Phaeodarians are a group of widely distributed marine cercozoans. These plankton organisms can exhibit a large biomass in the environment and are supposed to play an important role in marine ecosystems and in material cycles in the ocean. Accurate knowledge of phaeodarian classification is thus necessary to better understand marine biology, however, phylogenetic information on Phaeodaria is limited. The present study analyzed 18S rDNA sequences encompassing all existing phaeodarian orders, to clarify their phylogenetic relationships and improve their taxonomic classification. The mono- phyly of Phaeodaria was confirmed and strongly supported by phylogenetic analysis with a larger data set than in previous studies. The phaeodarian clade contained 11 subclades which generally did not correspond to the families and orders of the current classification system. Two families (Challengeri- idae and Aulosphaeridae) and two orders (Phaeogromida and Phaeocalpida) are possibly polyphyletic or paraphyletic, and consequently the classification needs to be revised at both the family and order levels by integrative taxonomy approaches.
    [Show full text]
  • Massisteria Marina Larsen & Patterson 1990
    l MARINE ECOLOGY PROGRESS SERIES Vol. 62: 11-19, 1990 1 Published April 5 l Mar. Ecol. Prog. Ser. l Massisteria marina Larsen & Patterson 1990, a widespread and abundant bacterivorous protist associated with marine detritus David J. patterson', Tom ~enchel~ ' Department of Zoology. University of Bristol. Bristol BS8 IUG. United Kingdom Marine Biological Laboratory, Strandpromenaden, DK-3000 Helsinger, Denmark ABSTRACT: An account is given of Massisteria marina Larsen & Patterson 1990, a small phagotrophic protist associated with sediment particles and with suspended detrital material in littoral and oceanic marine waters. It has been found at sites around the world. The organism has an irregular star-shaped body from which radiate thin pseudopodia with extrusomes. There are 2 inactive flagella. The organism is normally sedentary but, under adverse conditions, the arms are resorbed, the flagella become active, and the organism becomes a motile non-feeding flagellate. The ecological niche occupied by this organism and its phylogenetic affinities are discussed. INTRODUCTION (Patterson & Fenchel 1985, Fenchel & Patterson 1986, 1988, V~rs1988, Larsen & Patterson 1990). Here we Much of the carbon fixed in marine ecosystems is report on a protist, Massisteria marina ', that is specifi- degraded by microbial communities and it is held that cally associated with planktonic and benthic detritus protists, especially flagellates under 10 pm in size, and appears to be widespread and common. exercise one of the principal controlling influences over bacterial growth rates and numbers (Fenchel 1982, Azam et al. 1983, Ducklow 1983, Proctor & Fuhrman MATERIALS AND METHODS 1990). Detrital aggregates, whether benthic or in the water column, may support diverse and active microbial Cultures were established by dilution series from communities that include flagellates (Wiebe & Pomeroy water samples taken in the Limfjord (Denmark), and 1972, Caron et al.
    [Show full text]
  • Multigene Eukaryote Phylogeny Reveals the Likely Protozoan Ancestors of Opis- Thokonts (Animals, Fungi, Choanozoans) and Amoebozoa
    Accepted Manuscript Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opis- thokonts (animals, fungi, choanozoans) and Amoebozoa Thomas Cavalier-Smith, Ema E. Chao, Elizabeth A. Snell, Cédric Berney, Anna Maria Fiore-Donno, Rhodri Lewis PII: S1055-7903(14)00279-6 DOI: http://dx.doi.org/10.1016/j.ympev.2014.08.012 Reference: YMPEV 4996 To appear in: Molecular Phylogenetics and Evolution Received Date: 24 January 2014 Revised Date: 2 August 2014 Accepted Date: 11 August 2014 Please cite this article as: Cavalier-Smith, T., Chao, E.E., Snell, E.A., Berney, C., Fiore-Donno, A.M., Lewis, R., Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa, Molecular Phylogenetics and Evolution (2014), doi: http://dx.doi.org/10.1016/ j.ympev.2014.08.012 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. 1 1 Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts 2 (animals, fungi, choanozoans) and Amoebozoa 3 4 Thomas Cavalier-Smith1, Ema E. Chao1, Elizabeth A. Snell1, Cédric Berney1,2, Anna Maria 5 Fiore-Donno1,3, and Rhodri Lewis1 6 7 1Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
    [Show full text]
  • Protistology Review of Diversity and Taxonomy of Cercomonads
    Protistology 3 (4), 201217 (2004) Protistology Review of diversity and taxonomy of cercomonads Alexander P. Myl’nikov 1 and Serguei A. Karpov 2 1 Institute for the Biology of Inland Waters, Borok, Yaroslavl district, Russia 2 Biological Faculty, Herzen Pedagogical State University, St. Petersburg, Russia Summary Cercomonads are very common heterotrophic flagellates in water and soil. Phylogenetically they are a key group of a protistan phylum Cercozoa. Morphological and taxonomical analysis of cercomonads reveals that the order Cercomonadida (Vickerman) Mylnikov, 1986 includes two families: Cercomonadidae Kent, 1880 (=Cercobodonidae Hollande, 1942) and Heteromitidae Kent, 1880 em. Mylnikov, 2000 (=Bodomorphidae Hollande, 1952), which differ in several characters: body shape, temporary/habitual pseudopodia, presence/absence of plasmodia stage and microtubular cone, type of extrusomes. The family Cercomonadidae includes Cercomonas Dujardin, 1841 and Helkesimastix Woodcock et Lapage, 1914. All species of Cercobodo are transferred to the genus Cercomonas. The family Heteromitidae includes Heteromita Dujardin, 1841 emend. Mylnikov et Karpov, Protaspis Skuja, 1939, Allantion Sandon, 1924, Sainouron Sandon, 1924, Cholamonas Flavin et al., 2000 and Katabia Karpov et al., 2003. The names Bodomorpha and Sciviamonas are regarded as junior synonyms of Heteromita. The genus Proleptomonas Woodcock, 1916 according to its morphology is not a cercomonad, and is not included in the order. The genus Massisteria Larsen and Patterson, 1988 is excluded from
    [Show full text]
  • Molecular Identity of Strains of Heterotrophic Flagellates Isolated from Surface Waters and Deep-Sea Sediments of the South Atlantic Based on SSU Rdna
    AQUATIC MICROBIAL ECOLOGY Vol. 38: 239–247, 2005 Published March 18 Aquat Microb Ecol Molecular identity of strains of heterotrophic flagellates isolated from surface waters and deep-sea sediments of the South Atlantic based on SSU rDNA Frank Scheckenbach1, Claudia Wylezich1, Markus Weitere1, Klaus Hausmann2, Hartmut Arndt1,* 1Department of General Ecology and Limnology, Zoological Institute, University of Cologne, 50923 Cologne, Germany 2Institute of Biology/Zoology, Free University of Berlin, Research Group Protozoology, 14195 Berlin, Germany ABSTRACT: Whereas much is known about the biodiversity of prokaryotes and macroorganisms in the deep sea, knowledge on the biodiversity of protists remains very limited. Molecular studies have changed our view of marine environments and have revealed an astonishing number of previously unknown eukaryotic organisms. Morphological findings have shown that at least some widely dis- tributed nanoflagellates can also be found in the deep sea. Whether these flagellates have contact with populations from other habitats is still uncertain. We performed a molecular comparison of strains isolated from deep-sea sediments (>5000 m depth) and surface waters on the basis of their small subunit ribosomal DNA (SSU rDNA). Sequences of Rhynchomonas nasuta, Amastigomonas debruynei, Ancyromonas sigmoides, Cafeteria roenbergensis and Caecitellus parvulus were analysed, and 2 contrasting results obtained. Firstly, we found nearly identical genotypes within 1 morphospecies (C. roenbergensis), and secondly, quite different genotypes within certain morpho- species (R. nasuta, A. sigmoides and C. parvulus). In addition, high genetic distances between the dif- ferent strains of A. sigmoides and C. parvulus indicate that these morphospecies should be divided into different at least genetically distinguishable species. In contrast, some heterotrophic nanoflagel- lates must indeed be regarded as being cosmopolitan.
    [Show full text]
  • Protist Phylogeny and the High-Level Classification of Protozoa
    Europ. J. Protistol. 39, 338–348 (2003) © Urban & Fischer Verlag http://www.urbanfischer.de/journals/ejp Protist phylogeny and the high-level classification of Protozoa Thomas Cavalier-Smith Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK; E-mail: [email protected] Received 1 September 2003; 29 September 2003. Accepted: 29 September 2003 Protist large-scale phylogeny is briefly reviewed and a revised higher classification of the kingdom Pro- tozoa into 11 phyla presented. Complementary gene fusions reveal a fundamental bifurcation among eu- karyotes between two major clades: the ancestrally uniciliate (often unicentriolar) unikonts and the an- cestrally biciliate bikonts, which undergo ciliary transformation by converting a younger anterior cilium into a dissimilar older posterior cilium. Unikonts comprise the ancestrally unikont protozoan phylum Amoebozoa and the opisthokonts (kingdom Animalia, phylum Choanozoa, their sisters or ancestors; and kingdom Fungi). They share a derived triple-gene fusion, absent from bikonts. Bikonts contrastingly share a derived gene fusion between dihydrofolate reductase and thymidylate synthase and include plants and all other protists, comprising the protozoan infrakingdoms Rhizaria [phyla Cercozoa and Re- taria (Radiozoa, Foraminifera)] and Excavata (phyla Loukozoa, Metamonada, Euglenozoa, Percolozoa), plus the kingdom Plantae [Viridaeplantae, Rhodophyta (sisters); Glaucophyta], the chromalveolate clade, and the protozoan phylum Apusozoa (Thecomonadea, Diphylleida). Chromalveolates comprise kingdom Chromista (Cryptista, Heterokonta, Haptophyta) and the protozoan infrakingdom Alveolata [phyla Cilio- phora and Miozoa (= Protalveolata, Dinozoa, Apicomplexa)], which diverged from a common ancestor that enslaved a red alga and evolved novel plastid protein-targeting machinery via the host rough ER and the enslaved algal plasma membrane (periplastid membrane).
    [Show full text]
  • Radiozoa (Acantharia, Phaeodaria and Radiolaria) and Heliozoa
    MICC16 26/09/2005 12:21 PM Page 188 CHAPTER 16 Radiozoa (Acantharia, Phaeodaria and Radiolaria) and Heliozoa Cavalier-Smith (1987) created the phylum Radiozoa to Radiating outwards from the central capsule are the include the marine zooplankton Acantharia, Phaeodaria pseudopodia, either as thread-like filopodia or as and Radiolaria, united by the presence of a central axopodia, which have a central rod of fibres for rigid- capsule. Only the Radiolaria including the siliceous ity. The ectoplasm typically contains a zone of frothy, Polycystina (which includes the orders Spumellaria gelatinous bubbles, collectively termed the calymma and Nassellaria) and the mixed silica–organic matter and a swarm of yellow symbiotic algae called zooxan- Phaeodaria are preserved in the fossil record. The thellae. The calymma in some spumellarian Radiolaria Acantharia have a skeleton of strontium sulphate can be so extensive as to obscure the skeleton. (i.e. celestine SrSO4). The radiolarians range from the A mineralized skeleton is usually present within the Cambrian and have a virtually global, geographical cell and comprises, in the simplest forms, either radial distribution and a depth range from the photic zone or tangential elements, or both. The radial elements down to the abyssal plains. Radiolarians are most useful consist of loose spicules, external spines or internal for biostratigraphy of Mesozoic and Cenozoic deep sea bars. They may be hollow or solid and serve mainly to sediments and as palaeo-oceanographical indicators. support the axopodia. The tangential elements, where Heliozoa are free-floating protists with roughly present, generally form a porous lattice shell of very spherical shells and thread-like pseudopodia that variable morphology, such as spheres, spindles and extend radially over a delicate silica endoskeleton.
    [Show full text]
  • Barthelonids Represent a Deep-Branching Metamonad Clade with Mitochondrion-Related Organelles Generating No
    bioRxiv preprint doi: https://doi.org/10.1101/805762; this version posted October 29, 2019. 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 2 3 Barthelonids represent a deep-branching Metamonad clade with mitochondrion-related 4 organelles generating no ATP. 5 6 Euki Yazaki1*, Keitaro Kume2, Takashi Shiratori3, Yana Eglit 4,5,, Goro Tanifuji6, Ryo 7 Harada7, Alastair G.B. Simpson4,5, Ken-ichiro Ishida7,8, Tetsuo Hashimoto7,8 and Yuji 8 Inagaki7,9* 9 10 1Department of Biochemistry and Molecular Biology, Graduate School and Faculty of 11 Medicine, The University of Tokyo, Tokyo, Japan 12 2Faculty of Medicine, University of Tsukuba, Ibaraki, Japan 13 3Department of Marine Diversity, Japan Agency for Marine-Earth Science and Technology, 14 Yokosuka, Japan 15 4Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada 16 5Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, 17 Halifax, Nova Scotia, Canada 18 6Department of Zoology, National Museum of Nature and Science, Ibaraki, Japan 19 7Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 20 Ibaraki, Japan 21 8Faculty of Life and Environmental Sciences, University of Tsukuba, Ibaraki, Japan 22 9Center for Computational Sciences, University of Tsukuba, Tsukuba, Ibaraki, Japan 23 24 Running head: Phylogeny and putative MRO functions in a new metamonad clade. 25 26 *Correspondence addressed to Euki Yazaki, [email protected] and Yuji Inagaki, 27 [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/805762; this version posted October 29, 2019.
    [Show full text]