1887

Abstract

The mitochondrial cytochrome- oxidase subunit 1 () gene has been proposed as a DNA barcode to identify animal species. To test the applicability of the gene in identifying ciliates, 75 isolates of the genus and three non- ciliates that are close relatives of , , and , were selected. All tetrahymenines of unproblematic species could be identified to the species level using 689 bp of the sequence, with about 11 % interspecific sequence divergence. Intraspecific isolates of , , and could be identified by their sequences, showing <0.65 % intraspecific sequence divergence. In addition, isolates of these species were clustered together on a neighbour-joining (NJ) tree. However, strains identified as and showed high intraspecific sequence divergence values of 5.01 and 9.07 %, respectively, and did not cluster together on a NJ tree. This may indicate the presence of cryptic species. The mean interspecific sequence divergence of was about 11 times greater than the mean intraspecific sequence divergence, and this increased to 58 times when all isolates of species with high intraspecific sequence divergence were excluded. This result is similar to DNA barcoding studies on animals, indicating that congeneric sequence divergences are an order of magnitude greater than conspecific sequence divergences. Our analysis also demonstrated low sequence divergences of <1.0 % between some isolates of and on the one hand and some isolates of and on the other, suggesting that the latter species in each pair is a junior synonym of the former. Overall, our study demonstrates the feasibility of using the mitochondrial gene as a taxonomic marker for ‘barcoding’ and identifying species and some other ciliated protists.

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.64865-0
2007-10-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/57/10/2412.html?itemId=/content/journal/ijsem/10.1099/ijs.0.64865-0&mimeType=html&fmt=ahah

References

  1. Avise J. C. 2000 Phylogeography: the History and Formation of Species Cambridge, MA: Harvard University Press;
    [Google Scholar]
  2. Ball S. L., Hebert P. D. N., Burian S. K., Webb J. M. 2005; Biological identifications of mayflies (Ephemeroptera) using DNA barcodes. J N Am Benthol Soc 24:508–524 [CrossRef]
    [Google Scholar]
  3. Barrett R. D. H., Hebert P. D. N. 2005; Identifying spiders through DNA barcodes. Can J Zool 83:481–491 [CrossRef]
    [Google Scholar]
  4. Barth D., Krenek S., Fokin S. I., Berendonk T. U. 2006; Intraspecific genetic variation in Paramecium revealed by mitochondrial cytochrome c oxidase I sequences. J Eukaryot Microbiol 53:20–25 [CrossRef]
    [Google Scholar]
  5. Borden D., Whitt G. S., Nanney D. L. 1973a; Electrophoretic characterization of classical Tetrahymena pyriformis strains. J Protozool 20:693–700 [CrossRef]
    [Google Scholar]
  6. Borden D., Whitt G. S., Nanney D. L. 1973b; Isozymic heterogeneity in Tetrahymena strains. Science 181:279–280 [CrossRef]
    [Google Scholar]
  7. Borden D., Miller E. T., Whitt G. S., Nanney D. L. 1977; Electrophoretic analysis of evolutionary relationships in Tetrahymena . Evolution 31:91–102 [CrossRef]
    [Google Scholar]
  8. Brandl M. T., Rosenthal B. M., Haxo A. F., Berk S. G. 2005; Enhanced survival of Salmonella enterica in vesicles released by a soilborne Tetrahymena species. Appl Environ Microbiol 71:1562–1569 [CrossRef]
    [Google Scholar]
  9. Brown J. W., Miller S. E., Horak M. 2003; Studies on New Guinea moths. 2. Description of a new species of Xenothictis Meyrick (Lepidoptera: Tortricidae: Archipini. Proc Entomol Soc Wash 105:1043–1050
    [Google Scholar]
  10. Brunk C. F., Lee C. L., Tran A. B., Li J. 2003; Complete sequence of the mitochondrial genome of Tetrahymena thermophila and comparative methods for identifying highly divergent genes. Nucleic Acids Res 31:1673–1682 [CrossRef]
    [Google Scholar]
  11. Burger G., Zhu Y., Littlejohn T. G., Greenwood S. J., Schnare M. N., Lang B. F., Gray M. W. 2000; Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J Mol Biol 297:365–380 [CrossRef]
    [Google Scholar]
  12. Corliss J. O. 1952; Le cycle autogamique de Tetrahymena rostrata . C R Acad Sci 235:399–402 (in French
    [Google Scholar]
  13. Corliss J. O. 1953; Silver impregnation of ciliated protozoa by the Chatton-Lwoff technic. Stain Technol 28:97–100
    [Google Scholar]
  14. Corliss J. O. 1972; Tetrahymena and some thoughts on the evolutionary origin of endoparasitism. Trans Am Microsc Soc 91:566–573 [CrossRef]
    [Google Scholar]
  15. Corliss J. O. 1973; History, taxonomy, ecology, and evolution of species of Tetrahymena . In Biology of Tetrahymena pp 1–55 Edited by Elliott A. M. Stroudsburg, PA: Dowden, Hutchinson & Ross;
    [Google Scholar]
  16. Corliss J. O., Daggett P.-M. 1983; Paramecium aurelia ” and “ Tetrahymena pyriformis ”: current status of the taxonomy and nomenclature of these popularly known and widely used ciliates. Protistologica 19:307–322
    [Google Scholar]
  17. Cummings D. J. 1992; Mitochondrial genomes of the ciliates. Int Rev Cytol 141:1–64
    [Google Scholar]
  18. Czapik A. 1968; La famille Tetrahymenidae et son importance dans la systématique et l'évolution des ciliés. Acta Protozool 5:315–357 (in French
    [Google Scholar]
  19. Dawkins R. 1998 Unweaving the Rainbow: Science, Delusion and the Appetite for Wonder Boston: Houghton Mifflin;
    [Google Scholar]
  20. Elliott A. M. 1970; The distribution of Tetrahymena pyriformis . J Protozool 17:162–168 [CrossRef]
    [Google Scholar]
  21. Elwood H. J., Olsen G. J., Sogin M. L. 1985; The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata . Mol Biol Evol 2:399–410
    [Google Scholar]
  22. Felsenstein J. 2004 phylip (phylogeny inference package), version 3.6. Distributed by the author. Department of Genome Sciences University of Washington; Seattle, USA:
    [Google Scholar]
  23. Fenchel T., Finlay B. J. 2004; The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784 [CrossRef]
    [Google Scholar]
  24. Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. 1994; DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–297
    [Google Scholar]
  25. Gruchy D. F. 1955; The breeding system and distribution of Tetrahymena pyriformis . J Protozool 2:178–185 [CrossRef]
    [Google Scholar]
  26. Hajibabaei M., Janzen D. H., Burns J. M., Hallwachs W., Hebert P. D. N. 2006; DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci U S A 103:968–971 [CrossRef]
    [Google Scholar]
  27. Hebert P. D. N., Ratnasingham S., deWaard J. R. 2003a; Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc Biol Sci 270 (Suppl. 1):S96–S99 [CrossRef]
    [Google Scholar]
  28. Hebert P. D. N., Cywinska A., Ball S. L., deWaard J. R. 2003b; Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321 [CrossRef]
    [Google Scholar]
  29. Hebert P. D. N., Penton E. H., Burns J. M., Janzen D. H., Hallwachs W. 2004a; Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator . Proc Natl Acad Sci U S A 101:14812–14817 [CrossRef]
    [Google Scholar]
  30. Hebert P. D. N., Stoeckle M. Y., Zemlak T. S., Francis C. M. 2004b; Identification of birds through DNA barcodes. PLoS Biol 2: e312 [CrossRef]
    [Google Scholar]
  31. Hogg I. D., Hebert P. D. N. 2004; Biological identification of springtails (Hexapoda: Collembola) from the Canadian Arctic, using mitochondrial DNA barcodes. Can J Zool 82:749–754 [CrossRef]
    [Google Scholar]
  32. Holz G. G., Corliss J. O. 1956; Tetrahymena setifera n. sp., a member of the genus Tetrahymena with a caudal cilium. J Protozool 3:112–118 [CrossRef]
    [Google Scholar]
  33. Janczewski D. N., Modi W. S., Stephens J. C., O'Brien S. J. 1995; Molecular evolution of mitochondrial 12S RNA and cytochrome b sequences in the pantherine lineage of Felidae. Mol Biol Evol 12:690–707
    [Google Scholar]
  34. Jerome C. A., Lynn D. H. 1996; Identifying and distinguishing sibling species in the Tetrahymena pyriformis complex (Ciliophora, Oligohymenophorea) using PCR/RFLP analysis of nuclear ribosomal DNA. J Eukaryot Microbiol 43:492–497 [CrossRef]
    [Google Scholar]
  35. Kahl A. 1926; Neue und wenig bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch Protistenkd 55:197–438 (in German
    [Google Scholar]
  36. Kimura M. 1980; A simple method of estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [CrossRef]
    [Google Scholar]
  37. Kumar S., Tamura K., Nei M. 2004; mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163 [CrossRef]
    [Google Scholar]
  38. Kumazawa Y., Nishida M. 1993; Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol 37:380–398
    [Google Scholar]
  39. Lynn D. H., Strüder-Kypke M. C. 2006; Species of Tetrahymena identical by small subunit rRNA gene sequences are discriminated by mitochondrial cytochrome c oxidase I gene sequences. J Eukaryot Microbiol 53:385–387 [CrossRef]
    [Google Scholar]
  40. Mardulyn P., Whitfield J. B. 1999; Phylogenetic signal in the COI, 16S, and 28S genes for inferring relationships among genera of Microgastrinae (Hymenoptera; Braconidae): evidence of a high diversification rate in this group of parasitoids. Mol Phylogenet Evol 12:282–294 [CrossRef]
    [Google Scholar]
  41. Medlin L., Elwood H. J., Stickel S., Sogin M. L. 1988; The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491–499 [CrossRef]
    [Google Scholar]
  42. Meyer E. B., Nanney D. L. 1987; Isozymes in the ciliated protozoa. In Isozymes ( Current Topics in Biological and Medical Research, vol. 13) pp 61–101 Edited by Rattazzi M. C. New York: Alan R. Liss;
    [Google Scholar]
  43. Monaghan M. T., Balke M., Gregory T. R., Vogler A. P. 2005; DNA-based species delineation in tropical beetles using mitochondrial and nuclear markers. Philos Trans R Soc Lond B Biol Sci 360:1925–1933 [CrossRef]
    [Google Scholar]
  44. Nanney D. L., McCoy J. W. 1976; Characterization of the species of the Tetrahymena pyriformis complex. Trans Am Microsc Soc 95:664–682 [CrossRef]
    [Google Scholar]
  45. Nanney D. L., Meyer E. B., Simon E. M., Preparata R.-M. 1989; Comparison of ribosomal and isozymic phylogenies of tetrahymenine ciliates. J Protozool 36:1–8 [CrossRef]
    [Google Scholar]
  46. Nanney D. L., Park C., Preparata R., Simon E. M. 1998; Comparison of sequence differences in a variable 23S rRNA domain among sets of cryptic species of ciliated protozoa. J Eukaryot Microbiol 45:91–100 [CrossRef]
    [Google Scholar]
  47. Nelsen E. M., Debault L. E. 1978; Transformation in Tetrahymena pyriformis : description of an inducible phenotype. J Protozool 25:113–119 [CrossRef]
    [Google Scholar]
  48. Nyberg D. 1981; Three new “biological” species of Tetrahymena ( T. hegewischi n. sp., T. sonneborni n. sp., T. nipissingi n. sp.) and temperature tolerance of members of the “ pyriformis ” complex. J Protozool 28:65–69 [CrossRef]
    [Google Scholar]
  49. Preparata R. M., Meyer E. B., Preparata F. P., Simon E. M., Vossbrinck C. R., Nanney D. L. 1989; Ciliate evolution: the ribosomal phylogenies of the tetrahymenine ciliates. J Mol Evol 28:427–441 [CrossRef]
    [Google Scholar]
  50. Remigio E. A., Hebert P. D. N. 2003; Testing the utility of partial COI sequences for phylogenetic estimates of gastropod relationships. Mol Phylogenet Evol 29:641–647 [CrossRef]
    [Google Scholar]
  51. Sadler L. A., Brunk C. F. 1992; Phylogenetic relationships and unusual diversity in histone H4 proteins within the Tetrahymena pyriformis complex. Mol Biol Evol 9:70–84
    [Google Scholar]
  52. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
    [Google Scholar]
  53. Saunders G. W. 2005; Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc Lond B Biol Sci 360:1879–1888 [CrossRef]
    [Google Scholar]
  54. Scheffer S. J., Lewis M. L., Joshi R. C. 2006; DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in the Philippines. Ann Entomol Soc Am 99:204–210 [CrossRef]
    [Google Scholar]
  55. Schlegel M., Elwood H. J., Sogin M. L. 1991; Molecular evolution in hypotrichous ciliates: sequence of the small subunit RNA genes from Onychodromus quadricornutus and Oxytricha granulifera (Oxytrichidae, Hypotrichida, Ciliophora). J Mol Evol 32:64–69 [CrossRef]
    [Google Scholar]
  56. Simon E. M., Meyer E. B., Preparata R. M. 1985; New wild Tetrahymena from Southeast Asia, China, and North America, including Tetrahymena malaccensis , Tetrahymena asiatica , Tetrahymena nanneyi , Tetrahymena caudata , and Tetrahymena silvana n. spp. J Protozool 32:183–189 [CrossRef]
    [Google Scholar]
  57. Smith M. A., Fisher B. L., Hebert P. D. N. 2005; DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philos Trans R Soc Lond B Biol Sci 360:1825–1834 [CrossRef]
    [Google Scholar]
  58. Sogin M. L., Elwood H. J. 1986; Primary structure of the Paramecium tetraurelia small-subunit rRNA coding region: phylogenetic relationships within the Ciliophora. J Mol Evol 23:53–60 [CrossRef]
    [Google Scholar]
  59. Strüder-Kypke M. C., Wright A.-D. G., Jerome C. A., Lynn D. H. 2001; Parallel evolution of histophagy in ciliates of the genus Tetrahymena . BMC Evol Biol 1:5 [CrossRef]
    [Google Scholar]
  60. Tautz D., Arctander P., Minelli A., Thomas R. H., Vogler A. P. 2002; DNA points the way ahead in taxonomy. Nature 418:479
    [Google Scholar]
  61. Tautz D., Arctander P., Minelli A., Thomas R. H., Vogler A. P. 2003; A plea for DNA taxonomy. Trends Ecol Evol 18:70–74 [CrossRef]
    [Google Scholar]
  62. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  63. Walsh P. S., Metzger D. A., Higuchi R. 1991; Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
    [Google Scholar]
  64. Ward R. D., Zemlak T. S., Innes B. H., Last P. R., Hebert P. D. N. 2005; DNA barcoding Australia's fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857 [CrossRef]
    [Google Scholar]
  65. Williams N. E., Buhse H. E. Jr, Smith M. G. 1984; Protein similarities in the genus Tetrahymena and a description of Tetrahymena leucophrys n. sp. J Protozool 31:313–321 [CrossRef]
    [Google Scholar]
  66. Ziaie Z., Suyama Y. 1987; The cytochrome oxidase subunit I gene of Tetrahymena : a 57 amino acid NH2-terminal extension and a 108 amino acid insert. Curr Genet 12:357–368 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.64865-0
Loading
/content/journal/ijsem/10.1099/ijs.0.64865-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error