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Plant Biol (Stuttg) 2004; 6(4): 447-453
DOI: 10.1055/s-2004-820888
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Phylogenetic Position of Endosymbiotic Green Algae in Paramecium bursaria Ehrenberg from Japan

R. Hoshina1 , S.-i. Kamako1 , N. Imamura1
  • 1Department of Bio Science and Biotechnology, Faculty of Science and Engineering, Ritsumeikan University, Kusatsu Shiga, Japan
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Publikationsverlauf

Publikationsdatum:
12. Juli 2004 (online)

   Lizenzen und Reprints

Abstract

Endosymbiotic green algae of Japanese Paramecium bursaria were phylogenetically analyzed based on DNA sequences from the ribosomal DNA operon (18S rDNA, ITS1, 5.8S rDNA, and ITS2). Phylogenetic trees constructed using 18S rDNA sequences showed that the symbionts belong to the Chlorella sensu stricto (Trebouxiophyceae) group. They are genetically closer to the C. vulgaris Beijerinck group than to C. kessleri Fott et Nováková as proposed previously. Branching order in C. vulgaris group was unresolved in 18S rDNA trees. Compared heterogeneities of 18S rDNA, ITS1, 5.8S r, and ITS2 among symbionts and two Chlorella species, indicated that the ITS2 region (and probably also ITS1) is better able to resolve phylogenetic problems in such closely related taxa. All six symbiotic sequences obtained here (approximately 4000-bp sequences of 18S rDNA, ITS1, 5.8S rDNA, and ITS2) were completely identical in each, strongly suggesting a common origin.

Key words

18S rDNA - Chlorella - endosymbiont - ITS - Paramecium bursaria - phylogeny

References

  • 1 Bhattacharya D., Friedl T., Damberger S.. Nuclear-encoded rDNA group I introns, origin and phylogenetic relationships of insertion site lineages in the green algae.  Mol. Biol. Evol.. (1996);  13 978-989
    PubMedSuche in Google Scholar
  • 2 Cozzolino S., Campo I., Moretti M. A., Pollio A.. The use of nuclear ribosomal ITS1 DNA sequences for the identification of Chlorella strains.  Algological Studies. (1999);  95 31-42
    PubMedSuche in Google Scholar
  • 3 Douglas A. E., Huss V. A. R.. On the characteristics and taxonomic position of symbiotic Chlorella. .  Arch. Microbiol.. (1986);  145 80-84
    CrossrefPubMedSuche in Google Scholar
  • 4 Dahlkild Å., Källersjö M., Lohtander K., Tehler A.. Photobiont diversity in the Physciaceae (Lecanorales).  Bryologist. (2001);  104 527-536
    PubMedSuche in Google Scholar
  • 5 Felsenstein J.. Evolutionary trees from DNA sequences: a maximum-likelihood approach.  J. Mol. Evol.. (1981);  17 368-376
    CrossrefPubMedSuche in Google Scholar
  • 6 Felsenstein J.. Confidence intervals on phylogenies: an approach using the bootstrap.  Evolution. (1985);  39 783-791
    PubMedSuche in Google Scholar
  • 7 Friedl T., Zeltner C.. Assessing the relationships of some coccoid green lichen algae and the Microthamniales (Chlorophyta) with 18S ribosomal RNA gene sequence comparisons.  J. Phycol.. (1994);  30 500-506
    CrossrefPubMedSuche in Google Scholar
  • 8 Friedl T., Rokitta C.. Species relationships in the lichen alga Trebouxia (Chlorophyta, Trebouxiophyceae): molecular phylogenetic analyses of nuclear-encoded large subunit rRNA gene sequences.  Symbiosis. (1997);  23 125-148
    PubMedSuche in Google Scholar
  • 9 Hasegawa M., Kishino H., Yano T. A.. Dating of human-ape splitting by a molecular clock of mitochondrial DNA.  J. Mol. Evol.. (1985);  22 160-174
    PubMedSuche in Google Scholar
  • 10 Helms G., Friedl T., Rambold G., Mayrhofer H.. Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing.  Lichenologist. (2001);  33 73-86
    PubMedSuche in Google Scholar
  • 11 Hershkovitz M. A., Lewis L. A.. Deep-level diagnostic value of the rDNA-ITS region.  Mol. Biol. Evol.. (1996);  13 1276-1295
    PubMedSuche in Google Scholar
  • 12 Hoshina R., Hasegawa K., Tanaka J., Hara Y.. Molecular phylogeny of the Dictyotaceae (Phaeophyceae) with emphasis on their morphology and its taxonomic implication.  Jpn. J. Phycol.. (2004);  52 (Suppl.) 189-194
    PubMedSuche in Google Scholar
  • 13 Huss V. A. R., Sogin M. L.. Primary structure of the Chlorella vulgaris small subunit ribosomal RNA coding region.  Nucl. Acids Res.. (1989);  17 1255
    PubMedSuche in Google Scholar
  • 14 Huss V. A. R., Sogin M. L.. Phylogenetic position of some Chlorella species within the chlorococcales based upon complete small-subunit ribosomal RNA sequences.  J. Mol. Evol.. (1990);  31 432-442
    PubMedSuche in Google Scholar
  • 15 Huss V. A. R., Holweg C., Seidel B., Reich V., Rahat M., Kessler E.. There is an ecological basis for host/symbiont specificity in Chlorella/Hydra symbioses.  Endocyt. Cell Res.. 1993/94;  10 35-46
    PubMedSuche in Google Scholar
  • 16 Huss V. A. R., Frank C., Hartmann E. C., Hirmer M., Kloboucek A., Seidel B. M., Wenzeler P., Kessler E.. Biochemical taxonomy and molecular phylogeny of the genus Chlorella sensu lato (Chlorophyta).  J. Phycol.. (1999);  35 587-598
    CrossrefPubMedSuche in Google Scholar
  • 17 Huss V. A. R., Ciniglia C., Cennamo P., Cozzolino S., Pinto G., Pollio A.. Phylogenetic relationships and taxonomic position of Chlorella-like isolates from low pH environments (pH < 3.0).  BMC Evol Biol.. (2002);  2 13
    CrossrefPubMedSuche in Google Scholar
  • 18 Ichimura T.. Sexual cell division and conjugation-papilla formation in sexual reproduction of Closterium strigosum. .  Proc. Int. Seaweed Symp.. (1971);  7 208-214
    PubMedSuche in Google Scholar
  • 19 Jukes T. H., Cantor C. H.. Evolution of protein molecules. Munro, H. M., ed. Mammalian Protein Metabolism. New York; Academic Press (1969): 21-123
    Suche in Google Scholar
  • 20 Kessler E., Huss V. A. R.. Biochemical taxonomy of symbiotic Chlorella strains from Paramecium and Acanthocystis. .  Bot. Acta. (1990);  103 140-142
    PubMedSuche in Google Scholar
  • 21 Kessler E., Schäfer M., Hümmer C., Kloboucek A., Huss V. A. R.. Physiological, biochemical, and molecular characters for the taxonomy of the subgenera of Scenedesmus (Chlorococcales, Chlorophyta).  Bot. Acta. (1997);  110 244-250
    PubMedSuche in Google Scholar
  • 22 Kimura M.. A simple method for estimating rate of base substitutions through comparative studies of nucleotide sequences.  J. Mol. Evol.. (1980);  16 111-120
    CrossrefPubMedSuche in Google Scholar
  • 23 Kroken S., Taylor J. W.. Phylogenetic species, reproductive mode, and specificity of the green alga Trebouxia forming lichens with the fungal genus Letharia. .  Bryologist. (2000);  103 645-660
    PubMedSuche in Google Scholar
  • 24 Kvitko K. V., Migunova A. V., Karelov D. V., Prokosheva M.  Ju.. Molecular taxonomy of virus-sensitive Chlorella sp. - symbionts of Paramecium bursaria. .  Protistology. (2001);  2 96-104
    PubMedSuche in Google Scholar
  • 25 Lanave C., Preparata G., Saccone C., Serio G.. A new method for calculating evolutionary substitution rates.  J. Mol. Evol.. (1984);  20 86-93
    PubMedSuche in Google Scholar
  • 26 Linz B., Linz A., Migunova A. V., Kvitko K. V.. Correlation between virus-sensitivity and isoenzyme spectrum in symbiotic Chlorella-like algae.  Protistology. (1999);  1 76-81
    PubMedSuche in Google Scholar
  • 27 Litaker R. W., Tester P. A., Colorni A., Levy M. G., Noga E. J.. The phylogenetic relationship of Pfiesteria piscicida, Cryptoperidiniopsoid sp., Amyloodinium ocellatum and a Pfiesteria-like dinoflagellate to other dinoflagellates and apicomplexans.  J. Phycol.. (1999);  35 1379-1389
    CrossrefPubMedSuche in Google Scholar
  • 28 Marin B., Melkonian M.. Mesostigmatophyceae, a new class of Streptophyte green algae revealed by SSU rRNA sequence comparisons.  Protist. (1999);  150 399-417
    PubMedSuche in Google Scholar
  • 29 Moncalvo J. M., Lutzoni F. M., Rehner L. S., Johnson J., Vilgalys R.. Phylogenetic relationships of agaric fungi based on nuclear large subunit ribosomal DNA sequences.  Syst. Biol.. (2000);  49 278-305
    PubMedSuche in Google Scholar
  • 30 Nakayama T., Watanabe S., Mitsui K., Uchida H., Inouye I.. The phylogenetic relationship between the Chlamydomonadales and Chlorococcales inferred from 18S rDNA sequence data.  Phycol. Res.. (1996);  44 47-55
    PubMedSuche in Google Scholar
  • 31 Nishihara N., Horiike S., Takahashi T., Kosaka T., Shigenaka Y., Hosoya H.. Cloning and characterization of endosymbiotic algae isolated from Paramecium bursaria. .  Protoplasma. (1998);  203 91-99
    CrossrefPubMedSuche in Google Scholar
  • 32 Pearson W. R., Lipman D. J.. Improved tools for biological sequence analysis.  PNAS. (1988);  85 2444-2448
    PubMedSuche in Google Scholar
  • 33 Reisser W.. The taxonomy of green algae endosymbiotic in Ciliates and Sponge.  Br. Phycol. J.. (1984);  19 309-318
    PubMedSuche in Google Scholar
  • 34 Reisser W.. Naturally occurring and artificially established associations of ciliates and algae. Models for different steps in the evolution of stable endosymbioses.  Ann. N.Y. Acad. Sci.. (1987);  503 316-329
    PubMedSuche in Google Scholar
  • 35 Reisser W., Vietze S., Widowski M.. Taxonomic studies on endocytobiotic Chlorophycean algae isolated from different American and European strains of Paramecium bursaria. .  Symbiosis. (1988);  6 253-270
    PubMedSuche in Google Scholar
  • 36 Romeike J., Friedl T., Helms G., Ott S.. Genetic diversity of algal and fungal partners in four species of Umbilicaria (Lichenized A scomycetes) along a transect of the Antarctic peninsula.  Mol. Biol. Evol.. (2002);  19 1209-1217
    PubMedSuche in Google Scholar
  • 37 Saitou N., Nei M.. The neighbor-joining method: A new method for reconstructing phylogenetics trees.  Mol. Biol. Evol.. (1987);  4 406-425
    PubMedSuche in Google Scholar
  • 38 Sonneborn T. M.. Breeding systems, reproductive methods and species problems in Protozoa. Mayr, E., ed. The Species Problem. Washington DC; American Assoc. Adv. Science (1957): 155-324
    Suche in Google Scholar
  • 39 Swofford D. L.. PAUP. Phylogenetic Analysis Using Parsimony (and other methods), Version 4. Sunderland, Massachusetts; Sinauer Associates (2000)
    Suche in Google Scholar
  • 40 Takeda H.. Cell wall composition and taxonomy of symbiotic Chlorella from Paramecium and Acanthocystis. .  Phytochemistry. (1995);  40 457-459
    CrossrefPubMedSuche in Google Scholar
  • 41 Takeda H., Sekiguchi T., Nunokawa S., Usuki I.. Species-specificity of Chlorella for establishment of symbiotic association with Paramecium bursaria - Does infectivity depend upon sugar components of the cell wall?.  Europ. J. Protistol.. (1998);  34 133-137
    PubMedSuche in Google Scholar
  • 42 Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.  Nucleic Acids Res.. (1997);  24 4876-4882
    PubMedSuche in Google Scholar
  • 43 Ustinova I., Krienitz L., Huss V. A. R.. Closteriopsis acicularis (G. M. Smith) Belcher et Swale is a fusiform alga closely related to Chlorella kessleri Fott et Nováková (Chlorophyta, Trebouxiophyceae).  Eur. J. Phycol.. (2001);  36 341-351
    CrossrefPubMedSuche in Google Scholar
  • 44 Van de Peer Y., De Wacher R.. Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA.  J. Mol. Evol.. (1997);  45 619-630
    PubMedSuche in Google Scholar
  • 45 Waddle J. A., Schuster A. M., Lee K. W., Meints R. H.. The mitochondrial genome of an exsymbiotic Chlorella-like green alga.  Plant Mol. Biol.. (1990);  14 187-195
    CrossrefPubMedSuche in Google Scholar
  • 46 White T. J., Bruns T., Lee S., Taylor J.. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis, M., Gelfand, D., Sninsky, J., and White, T., eds. PCR Protocols: A Guide to Methods and Application. San Diego; Academic Press (1990): 315-322
    Suche in Google Scholar
  • 47 Wolf M., Krienitz L., Hepperle D.. Phylogenetic Position of Actinastrum hantzschii Lagerheim 1882 (Chlorophyta, Trebouxiophyceae).  Arch. Hydrobiol. Suppl. Algol. Stud.. (2002);  104 59-67
    PubMedSuche in Google Scholar
  • 48 Yang Z.. Estimating the pattern of nucleotide substitution.  J. Mol. Evol.. (1994);  39 105-111
    PubMedSuche in Google Scholar
  • 49 Zuker M.. Mfold web server for nucleic acid folding and hybridization prediction.  Nucleic Acids Res.. (2003);  31 1-10
    CrossrefPubMedSuche in Google Scholar

N. Imamura

Department of Bio Science and Biotechnology
Faculty of Science and Engineering
Ritsumeikan University

Noji Higashi 1-1-1

Kusatsu Shiga 525-8577

Japan

eMail: imamura@se.ritsumei.ac.jp

Section Editor: F. Salamini