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Phylogenetic relationships within the class Oligohymenophorea, phylum Cilophora, inferred from the complete small subunit rRNA gene sequences ofColpidium campylum, Glaucoma chattoni, andOpisthonecta henneguyi

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Summary

Phylogenetic relationships within the class Oligohymenophorea, phylum Ciliophora, were investigated by determining the complete small subunit rRNA (SSrRNA) gene sequences for the hymenostomesColpidium campylum, Glaucoma chattoni, and the peritrichOpisthonecta henneguyi. The affiliations of the oligohymenophoreans were assessed using both distance matrix (DM) and maximum parsimony (MP) analyses. Variations do exist in the phylogenies created by the two methods. However, the basic tree topologies are consistent. In both the DM and MP analyses the hymenostomes (C. campylum, G. chattoni, and the tetrahymenas) all form a very tight group associated with the peritrichO. henneguyi. TheTetrahymena lineage was monophyletic whereasColpidium andGlaucoma were more closely related to each other than either was to the tetrahymenas. The monophyly of the genusTetrahymena in the present analysis supports the phylogenies determined from morphological data and molecular sequence data from the histone H3II/H4II region of the genome. The perplexing and controversial phylogenetic position of the peritrichs is once again depicted in the present analysis. The distinctiveness of the peritrichOpisthonecta from both hymenostome and nassophorean ciliates based on evolutionary distances suggests that the elevation of the peritrichs to a higher taxonomic rank should be reconsidered.

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References

  • Allen SL, Li CI (1974) Nucleotide sequence divergence among DNA fractions of different syngens ofTetrahymena pyriformis. Biochem Genet 12:213–233

    Google Scholar 

  • Bardele CF (1980) The imprints of ciliate phylogeny revealed by comparative freeze-fracture study of the ciliary membrane. In: Schwemmler W, Schenk HEA (eds) Endocytobiology, endosymbiosis and cell biology. Walter de Gruyter, Berlin, pp 51–61

    Google Scholar 

  • Baroin A, Perasso R, Qu LH, Brugerolle G, Bachellerie JP, Adoutte A (1988) Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S ribosomal RNA. Proc Natl Acad Sci USA 85:3474–3478

    Google Scholar 

  • Brunk CF, Kahn RW, Sadler LA (1990) Phylogenetic relationships amongTetrahymena species determined using the polymerase chain reaction. J Mol Evol 30:290–297

    Google Scholar 

  • Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acids and protien sequences with ESEE. Comput Appl Biosci 5:233–234

    Google Scholar 

  • Chan Y, Gutell R, Noller HF, Wool IG (1984) The nucleotide sequence of a rat 18S ribosomal ribonucleic acid gene and proposal for the secondary structure of 18S ribosomal ribonucleic acid. J Biol Chem 259:224–230

    Google Scholar 

  • Corliss JO (1968) the value of ontogenetic data in reconstructing protozoan phylogenies. Trans Am Microsc Soc 87:1–20

    Google Scholar 

  • Corliss JO (1974) The chaning world of ciliate systematics: historical analysis of past efforts and a newly proposed phylogenetic scheme of classification for the protistan phylum Ciliophora. Syst Zool 23:91–138

    Google Scholar 

  • Corliss JO (1979) The ciliated protozoa: characterization, classification, and guide to the literature, ed 2. Pergamon, New York

    Google Scholar 

  • Czelusniak J, Goodman M, Hewett-Emmett D, Weiss ML, Venta PJ, Tashian RE (1982) Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes. Nature 298:297–300

    Google Scholar 

  • Czelusniak J, Goodman M, Moncreif ND, Kehoe SM (1990) Maximum parsimony approach to construction of evolutionary trees from aligned homologous sequences. In: Doolittle RF (ed) Methods in enzymology: molecular evolution: computer analysis of protein and nucleic acid sequences, vol 183. Academic Press, New York, pp 601–615

    Google Scholar 

  • Eisler K (1988) Electron microscopical observations on the ciliateFurgasonia blochmanni Fauré-Fremiet, 1967, Part 1: an update on morphology. Eur J Protistol 24:75–93

    Google Scholar 

  • Eisler K (1989) Electron microscopical observations on the ciliateFurgasonia blochmanni Fauré-Fremiet, 1967, Part 2: morphogenesis and phylogenetic conclusions. Eur J Protistol 24:181–199

    Google Scholar 

  • Elwood HJ, Olsen GJ, Sogin ML (1985) The small subunit ribosomal RNA gene sequences from the hypotrichous ciliatesOxytricha nova andStylonychia pustulata. Mol Biol Evol 2:399–410

    Google Scholar 

  • Farris JS (1981) Distance data in phylogenetic analysis. In: Funk VA, Brooks DR (eds) Advances in cladistics: proceedings of the first Willi Hennig Society. New York Botanical Garden, Bronx, pp 3–23

    Google Scholar 

  • Farris JS (1985) Distance data revisited. Cladistics 1:67–85

    Google Scholar 

  • Farris JS (1986) Distances and statistics. Cladistics 2:144–157

    Google Scholar 

  • Fauré-Fremiet E (1965) Morphologie comparée des ciliés Peritrichida. Prog Protozool, pp 13–14

  • Felsenstein J (1981) A likelihood approach to character weighting and what it tells us about parsimony and compatibility. Biol J Linn Soc 16:183–196

    Google Scholar 

  • Felsenstein J (1984) Distance methods for inferring phylogenies: a justification. Evolution 38:16–24

    Google Scholar 

  • Felsenstein J (1986) Distance methods: a reply to Farris. Cladistics 2:130–143

    Google Scholar 

  • Finley HE (1974) The peritrichs, now and then: 1676 to 1973. Trans Am Microsc Soc 93:307–313

    Google Scholar 

  • Goodman M (1981) Decoding the pattern of protein evolution. Prog Biophys Mol Biol 37:105–164

    Google Scholar 

  • Goodman M, Czelusniak J, Moore GW, Romero-Herrera AE, Matsuda G (1979) Fitting the gene lineage into its species lineage, a parsimony strategy illustrated by cladograms constructed from globin sequences. Syst Zool 28:132–163

    Google Scholar 

  • Greenwood SJ, Schlegel M, Sogin ML, Lynn DH (1991) Phylogenetic relationships ofBlepharisma americanum andColpoda inflata within the phylum Ciliophora inferred from complete small subunit rRNA gene sequences. J Protozool 38:1–6

    Google Scholar 

  • Gunderson JH, Elwood HJ, Ingold A, Kindle K, Sogin ML (1987) Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. Proc Natl Acad Sci USA 84: 5823–5827

    Google Scholar 

  • Hanyu N, Kichino Y, Nishimura S, Beier H (1986) Dramatic events in ciliate evolution: alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in twoTetrahymena tRNAsgln. EMBO J 5:1307–1311

    Google Scholar 

  • Harper DS, Jahn, CL (1989) Differential use of termination codons in ciliated protozoa. Proc Natl Acad Sci USA 86: 3252–3256

    Google Scholar 

  • Herzog M, Maroteaux L (1986) Dinoflagellate 17S rRNA sequence inferred from the gene sequence: evolutionary implications. Proc Natl Acad Sci USA 83:8644–8648

    Google Scholar 

  • Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 9:191–201

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 22–126

    Google Scholar 

  • Kahl A (1933) Ciliata libera et ectocommensalia. In: Grimpe G, Wagler E (eds), Die Tierwelt der Nord- und Ostee, Lief 23. Leipzig, pp 29–146

  • Katzen AL, Cann GM, Blackburn EH (1981) Sequence-specific fragmentation of macronuclear DNA in a holotrichous ciliate. Cell 24:313–320

    Google Scholar 

  • Lom J, Corliss JO, Noirot-Timothée C (1968) Observations on the ultrastructure of the buccal apparatus in thigmotrich ciliates and their bearing on thigmotrich-peritrich affinities. J Protozool 15:824–840

    Google Scholar 

  • Lynn DH, Didier P (1978) Caractéristiques ultrastructurales du cortex somatique et buccal du ciliéColpidium campylum (Oligohymenophora, Tetrahymenina) quant à la position sytématique duTuraniella. Can J Zool 56:2336–2343

    Google Scholar 

  • Lynn DH, Sogin ML (1988) Assessment of the phylogenetic relationships among ciliated protists using partial ribosomal RNA sequences derived from reverse transcripts. BioSystems 21:249–254

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold-Spring Harbor Laboratory, Cold Spring Harbor NY

    Google Scholar 

  • Martindale DW (1989) Codon usage inTetrahymena and other ciliates. J Protozool 36:29–34

    Google Scholar 

  • McCarroll R, Olsen GJ, Stahl YD, Woese CR, Sogin ML (1983) Nucleotide sequence ofDictyostelium discoideum small subunit ribosomal ribonucleic acid inferred from the gene sequence: evolutionary implications. Biochemistry 22:5858–5868

    Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA coding regions. Gene 71:491–499

    Google Scholar 

  • Messing J (1983) New M13 vectors for cloning. In: Wu R, Grossman LG, Moldave K (eds) Methods in enzymology: recombinant DNA, vol 101. Academic Press, New York, pp 20–78

    Google Scholar 

  • Messing J, Carlson J, Hagen G, Rubenstein I, Oleson A (1984) Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. DNA 3:31–40

    Google Scholar 

  • Miceli C, La Terza A, Melli ML (1989) Isolation and structural characterization of cDNA clones encoding the mating pheromone Er-1 secreted by the ciliateEuplotes raikovi. Proc Natl Acad Sci USA 86:3016–3020

    Google Scholar 

  • Moore GW, Barnabas J, Goodman M (1973) A method for constructing maximum parsimony ancestral amino acid sequences on a given network. J Theor Biol 38:459–485

    Google Scholar 

  • Nanney DL, Meyer EB, Simon EM, Preparata RM (1989a) Comparison of ribosomal and isozymic phylogenies of tetrahymenine ciliates. J Protozool 36:1–8

    Google Scholar 

  • Nanney DL, Preparata RM, Preparata FP, Meyer EB, Simon EM (1989b) Shifting ditypic site analysis: heuristics for extending the phylogenetic range of nucleotide sequences in Sankoff analyses. J Mol Evol 28:451–459

    Google Scholar 

  • Nelles L, Fang B, Volckaert G, Vandenberghe A, DeWachter R (1984) Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. Nucleic Acids Res 12:8749–8768

    Google Scholar 

  • Olsen GJ (1988) Phylogenetic analysis using ribosomal RNA. In: Wu R, Grossman LG (eds) Methods in enzymology: ribosomes, vol 164. Academic Press, New York, pp 793–812

    Google Scholar 

  • Peck RK (1978) Ultrastructure of the somatic and buccal cortex of the tetrahymenine hymenostomeGlaucoma chattoni. J Protozool 25:186–198

    Google Scholar 

  • Penny D, Hendy M (1986) Estimating the reliability of evolutionary trees. Mol Biol Evol 3:403–417

    Google Scholar 

  • Preparata RM, Meyer EB, Preparata FP, Simon EM, Vossbrinck CR, Nanney DL (1989) Ciliate evolution: the ribosomal phylogenies of the tetrahymenine ciliates. J Mol Evol 28:427–441

    Google Scholar 

  • Puytorac P de, Grain J, Legendre P, Devaux J (1984) Essai d'application de l'analyse phénétique à la classification du phylum des Ciliophora. J Protozool 31:496–507

    Google Scholar 

  • Puytorac P de, Grain J, Mignot J-P (1987) Précis de protistologie. Société Nouvelle des Éditions Boubée, Paris

    Google Scholar 

  • Rabbe Z (1964) The taxonomic position and rank of the Peritricha. Acta Protozool 2:19–32

    Google Scholar 

  • Rothschild LJ, Ragan MA, Coleman AW, Heywood P, Gerbi SA (1986) Are rRNA sequence comparisons the Rosetta stone of phylogenetics? Cell 47:640

    Google Scholar 

  • Rubtsov PM, Musakhanov MM, Zakharyev VM, Krayev AS, Skryabin KG, Bayev AA (1980) The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene fromSaccharomyces cerevisiae. Nucleic Acids Res 8:5779–5794

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467

    Google Scholar 

  • Schlegel M, Elwood HJ, Sogin ML (1991) Molecular evolution in hypotrichous ciliates: Sequence of the small subunit ribosomal RNA genes fromOnychodromus quadricornutus andOxytricha granulifera (Oxytrichidae, Hypotrichida, Ciliphora). J Mol Evol 32:64–69

    Google Scholar 

  • Small EB, Lynn DH (1981) A new macrosystem for the phylum Ciliophora Doflein, 1901. BioSystems 14:387–401

    Google Scholar 

  • Small EB, Lynn DH (1985) Phylum Ciliophora. In: Lee JJ, Hutner SH, Bovee EC (eds) An illustrated guide to the protozoa. Society of Protozoology, Lawrence KS, pp 393–575

    Google Scholar 

  • Sogin ML, Elwood HJ (1986) Primary structure of theParamecium tetraurelia small-subunit rRNA coding region: phylogenetic relationships within the Ciliophora. J Mol Evol 23:53–60

    Google Scholar 

  • Sogin ML, Ingold A, Karlok M, Nielsen H, Enberg J (1986a) Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the majorTetrahymena groups. EMBO J 5:3625–3630

    Google Scholar 

  • Sogin ML, Miotto K, Miller L (1986b) Primary structure of theNeurospora crassa small subunit ribosomal RNA coding region. Nucleic Acids Res 14:9540

    Google Scholar 

  • Sogin ML, Swanton MT, Gunderson JH, Elwood HJ (1986c) Sequence for the small subunit ribosomal RNA gene from the hypotrichous ciliateEuplotes aediculatus. J Protozool 33:26–29

    Google Scholar 

  • Sourdis J, Nei M (1988) Relative efficiencies of the maximum parsimony and distance matrix methods in obtaining the corect phylogenetic tree. Mol Biol Evol 5:298–311

    Google Scholar 

  • Spangler EA, Blackburn EH (1985) The nucleotide sequence of the 17S ribosomal RNA gene ofTetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin. J Biol Chem 260:6334–6340

    Google Scholar 

  • Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer, Sunderland MA, pp 411–500

    Google Scholar 

  • Valle RPC, Morch M-D (1988) Stop making sense or regulation at the level of termination in eukaryotic protein synthesis. FEBS Lett 235:1–15

    Google Scholar 

  • Van Bell CT (1985) 5S and 5.8S ribosomal RNA evolution in the suborder Tetrahymenina (Ciliophora: Hymenostomatida). J Mol Evol 22:231–236

    Google Scholar 

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Authors and Affiliations

  1. Department of Zoology, University of Guelph, N1G 2W1, Guelph, Ontario, Canada

    Spencer J. Greenwood & Denis H. Lynn

  2. Center for Molecular Evolution, Marine Biology Laboratory, 02543, Woods Hole, MA, USA

    Mitchell L. Sogin

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  1. Spencer J. Greenwood
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  2. Mitchell L. Sogin
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Greenwood, S.J., Sogin, M.L. & Lynn, D.H. Phylogenetic relationships within the class Oligohymenophorea, phylum Cilophora, inferred from the complete small subunit rRNA gene sequences ofColpidium campylum, Glaucoma chattoni, andOpisthonecta henneguyi . J Mol Evol 33, 163–174 (1991). https://doi.org/10.1007/BF02193631

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  • DOI: https://doi.org/10.1007/BF02193631

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