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

SummaryPhylogenetic 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.

[1]  S. Osawa,et al.  Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. , 1987, Molecular biology and evolution.

[2]  E. B. Meyer,et al.  Ciliate evolution: The ribosomal phylogenies of the tetrahymenine ciliates , 1989, Journal of Molecular Evolution.

[3]  D. Martindale,et al.  Codon usage in Tetrahymena and other ciliates. , 1989, The Journal of protozoology.

[4]  C F Brunk,et al.  Phylogenetic relationships among Tetrahymena species determined using the polymerase chain reaction. , 1990, Journal of molecular evolution.

[5]  C. Jahn,et al.  Differential use of termination codons in ciliated protozoa. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[6]  J. Felsenstein.  DISTANCE METHODS: A REPLY TO FARRIS , 1986, Cladistics : the international journal of the Willi Hennig Society.

[7]  G. Olsen,et al.  Nucleotide sequence of the Dictyostelium discoideum small-subunit ribosomal ribonucleic acid inferred from the gene sequence: evolutionary implications , 1983 .

[8]  K. Eisler.  Electron microscopical observations on the ciliate Furgasonia blochmanni Fauré-Fremiet, 1967: Part I: An update on morphology. , 1988, European journal of protistology.

[9]  D. Lynn,et al.  A new macrosystem for the phylum Ciliophora doflein, 1901. , 1981, Bio Systems.

[10]  J. Messing,et al.  Cloning and sequencing of the ribosomal RNA genes in maize: the 17S region. , 1984, DNA.

[11]  G. Moore,et al.  Fitting the gene lineage into its species lineage , 1979 .

[12]  M. Sogin,et al.  Assessment of phylogenetic relationships among ciliated protists using partial ribosomal RNA sequences derived from reverse transcripts. , 1988, Bio Systems.

[13]  Y. Kuchino,et al.  Dramatic events in ciliate evolution: alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in two Tetrahymena tRNAsGln , 1986, The EMBO journal.

[14]  S. Allen,et al.  Nucleotide sequence divergence among DNA fractions of different syngens of Tetrahymena pyriformis , 1974, Biochemical Genetics.

[15]  M. Goodman,et al.  Maximum parsimony approach to construction of evolutionary trees from aligned homologous sequences. , 1990, Methods in enzymology.

[16]  C. Van Bell.  5S and 5.8S ribosomal RNA evolution in the suborder Tetrahymenina (Ciliophora: Hymenostomatida). , 1985, Journal of molecular evolution.

[17]  L. Maroteaux,et al.  Dinoflagellate 17S rRNA sequence inferred from the gene sequence: Evolutionary implications. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Sogin,et al.  Phylogenetic relationships of Blepharisma americanum and Colpoda inflata within the phylum ciliophora inferred from complete small subunit rRNA gene sequences. , 1991, The Journal of protozoology.

[19]  R. Gutell,et al.  The nucleotide sequence of a rat 18 S ribosomal ribonucleic acid gene and a proposal for the secondary structure of 18 S ribosomal ribonucleic acid. , 1984, The Journal of biological chemistry.

[20]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D Penny,et al.  Estimating the reliability of evolutionary trees. , 1986, Molecular biology and evolution.

[22]  J. Farris.  DISTANCE DATA REVISITED , 1985, Cladistics : the international journal of the Willi Hennig Society.

[23]  M. Goodman,et al.  Decoding the pattern of protein evolution. , 1981, Progress in biophysics and molecular biology.

[24]  A Gajdos,et al.  [Evolution of protein molecules. I. Protein synthesis]. , 1972, La Nouvelle presse medicale.

[25]  Morris Goodman,et al.  Phylogenetic origins and adaptive evolution of avian and mammalian haemoglobin genes , 1982, Nature.

[26]  M. Sogin,et al.  Primary structure of the Paramecium tetraurelia small-subunit rRNA coding region: phylogenetic relationships within the Ciliophora. , 1986, Journal of molecular evolution.

[27]  G. Volckaert,et al.  Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. , 1984, Nucleic acids research.

[28]  J. Farris.  DISTANCES AND STATISTICS , 1986, Cladistics : the international journal of the Willi Hennig Society.

[29]  M. Morch,et al.  Stop making sense: or Regulation at the level of termination in eukaryotic protein synthesis. , 1988, FEBS letters.

[30]  E. L. Cabot,et al.  Simultaneous editing of multiple nucleic acid and protein sequences with ESEE , 1989, Comput. Appl. Biosci..

[31]  M. Sogin,et al.  The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. , 1988, Gene.

[32]  J. Corliss.  Reduced Status. (Book Reviews: The Ciliated Protozoa. Characterization, classification, and guide to the literature) , 1979 .

[33]  M. Sogin,et al.  Molecular evolution in hypotrichous ciliates: Sequence of the small subunit ribosomal RNA genes fromOnychodromus quadricornutus andOxytricha granulifera (Oxytrichidae, Hypotrichida, Ciliophora) , 2005, Journal of Molecular Evolution.

[34]  G. Olsen,et al.  The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. , 1985, Molecular biology and evolution.

[35]  J. Messing.  [2] New M13 vectors for cloning , 1983 .

[36]  M. Sogin,et al.  Primary structure of theParamecium tetraurelia small-subunit rRNA coding region: Phylogenetic relationships within the caliophora , 2005, Journal of Molecular Evolution.

[37]  J. Corliss,et al.  Observations on the ultrastructure of the buccal apparatus in thigmotrich ciliates and their bearing on thigmotrich-peritrich affinities. , 1968, The Journal of protozoology.

[38]  T. Jukes.  CHAPTER 24 – Evolution of Protein Molecules , 1969 .

[39]  G. Olsen.  Phylogenetic analysis using ribosomal RNA. , 1988, Methods in enzymology.

[40]  M. Melli,et al.  Isolation and structural characterization of cDNA clones encoding the mating pheromone Er-1 secreted by the ciliate Euplotes raikovi. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Osawa,et al.  The rates of evolution in some ribosomal components , 1977, Journal of Molecular Evolution.

[42]  P. Didier,et al.  Caractéristiques ultrastructurales du cortex somatique et buccal du cilié Colpidium campylum (Oligohymenophora, Tetrahymenina) quant à la position systématique de Turaniella , 1978 .

[43]  C. Bell.  5S and 5.8S ribosomal RNA evolution in the suborder tetrahymenina (Ciliophora: Hymenostomatida) , 2005, Journal of Molecular Evolution.

[44]  E. Blackburn,et al.  The nucleotide sequence of the 17S ribosomal RNA gene of Tetrahymena thermophila and the identification of point mutations resulting in resistance to the antibiotics paromomycin and hygromycin. , 1985, The Journal of biological chemistry.

[45]  K. Eisler.  Electron microscopical observations on the ciliate Furgasonia blochmanni Fauré-Fremiet, 1967: Part II: Morphogenesis and phylogenetic conclusions. , 1989, European journal of protistology.

[46]  M. Nei,et al.  Relative efficiencies of the maximum parsimony and distance-matrix methods in obtaining the correct phylogenetic tree. , 1988, Molecular biology and evolution.

[47]  R. Peck.  Ultrastructure of the Somatic and Buccal Cortex of the Tetrahymenine Hymenostome Glaucoma chattoni , 1978 .

[48]  P. Legendre,et al.  Essai ďApplication de ľAnalyse Phénétique à la Classification du Phylum des Ciliophora , 1984 .

[49]  E. Blackburn,et al.  Sequence-specific fragmentation of macronuclear DNA in a holotrichous ciliate , 1981, Cell.

[50]  Mark A. Ragan,et al.  Are rRNA sequence comparisons the Rosetta stone of phylogenetics? , 1986, Cell.

[51]  M. Sogin,et al.  Sequence of the small subunit ribosomal RNA gene from the hypotrichous ciliate Euplotes aediculatus. , 1986, The Journal of protozoology.

[52]  E. B. Meyer,et al.  Shifting ditypic site analysis: Heuristics for expanding the phylogenetic range of nucleotide sequences in Sankoff analyses , 1989, Journal of Molecular Evolution.

[53]  Joseph Felsenstein,et al.  A likelihood approach to character weighting and what it tells us about parsimony and compatibility , 1981 .

[54]  K. Skryabin,et al.  The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene from Saccharomyces cerevisiae. , 1980, Nucleic acids research.

[55]  J. Mignot,et al.  Précis de protistologie , 1987 .

[56]  M. Sogin,et al.  Primary structure of the Neurospora crassa small subunit ribosomal RNA coding region. , 1986, Nucleic acids research.

[57]  H. E. Finley.  The Peritrichs, Now and Then: 1676 to 1973 , 1974 .

[58]  Joseph Felsenstein,et al.  DISTANCE METHODS FOR INFERRING PHYLOGENIES: A JUSTIFICATION , 1984, Evolution; international journal of organic evolution.

[59]  G. Moore,et al.  A method for constructing maximum parsimony ancestral amino acid sequences on a given network. , 1973, Journal of theoretical biology.

[60]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[61]  J. Bachellerie,et al.  Partial phylogeny of the unicellular eukaryotes based on rapid sequencing of a portion of 28S ribosomal RNA. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[62]  J. Corliss.  The Changing World of Ciliate Systematics: Historical Analysis of Past Efforts and a Newly Proposed Phylogenetic Scheme of Classification for the Protistan Phylum Ciliophora , 1974 .

[63]  M. Sogin,et al.  Phylogenetic evidence for the acquisition of ribosomal RNA introns subsequent to the divergence of some of the major Tetrahymena groups. , 1986, The EMBO journal.

[64]  E. B. Meyer,et al.  Comparison of ribosomal and isozymic phylogenies of tetrahymenine ciliates. , 1989, The Journal of protozoology.

[65]  L. Sadler,et al.  Phylogenetic relationships amongTetrahymena species determined using the polymerase chain reaction , 1990, Journal of Molecular Evolution.

[66]  M. Sogin,et al.  Phylogenetic relationships between chlorophytes, chrysophytes, and oomycetes. , 1987, Proceedings of the National Academy of Sciences of the United States of America.