1887

Abstract

Environmental molecular surveys of microbial diversity have uncovered a vast number of novel taxonomic units in the eukaryotic tree of life that are exclusively known by their small-subunit (SSU) rRNA gene signatures. In this study, we reveal the cellular and taxonomic identity of a novel eukaryote SSU rRNA gene sequence clade within the Kinetoplastea. Kinetoplastea are ubiquitously distributed flagellated protists of high ecological and medical importance. We isolated an organism from the oxic–anoxic interface of the anoxic Framvaren Fjord (Norway), which branches within an unidentified kinetoplastean sequence clade. Ultrastructural studies revealed a typical cellular organization that characterized the flagellated isolate as a member of the order Neobodonida Vickerman 2004, which contains five genera. The isolate differed in several distinctive characters from , , and . The arrangement of the microtubular rod that supports the apical cytostome and the cytopharynx differed from the diagnosis of the fifth described genus ( Vickerman 2004) within the order Neobodonida. On the basis of both molecular and microscopical data, a novel genus within the order Neobodonida, gen. nov., is proposed. Here, we characterize its type species, sp. nov., and provide an tool to access the organism in nature and study its ecology.

Keyword(s): SSU, small-subunit
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.63769-0
2005-11-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/55/6/2623.html?itemId=/content/journal/ijsem/10.1099/ijs.0.63769-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Amaral Zettler L. A., Gomez F., Zettler E., Keenan B. G., Amils R., Sogin M. L. 2002; Eukaryotic diversity in Spain's River of Fire. Nature 417:137 [CrossRef]
    [Google Scholar]
  3. Arndt H., Dietrich D., Auer B., Cleven E., Grafenham T., Weitere M., Mylnikov A. P. 2000; Functional diversity of heterotrophic flagellates in aquatic ecosystems. In The Flagellates: Unity , Diversity and Evolution pp  240–268 Edited by Leadbeater B. S. C., Green J. C. London: Taylor & Francis;
    [Google Scholar]
  4. Bernard C., Simpson A. G. B., Patterson D. J. 2000; Some free-living flagellates (Protista) from anoxic habitats. Ophelia 52:113–142 [CrossRef]
    [Google Scholar]
  5. Berney C., Fahrni J., Pawlowski J. 2004; How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of environmental DNA surveys. BMC Biol 2:13 http://www.biomedcentral.com/1741-7007/2/13 [CrossRef]
    [Google Scholar]
  6. Blom D., de Haan A., van den Berg M., Sloof P., Jirků M., Lukeš J., Benne R. 1998; RNA editing in the free-living bodonid Bodo saltans . Nucleic Acids Res 26:1205–1213 [CrossRef]
    [Google Scholar]
  7. Boenigk J., Arndt H. 2000; Comparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta . Aquat Microb Ecol 22:243–249 [CrossRef]
    [Google Scholar]
  8. Boenigk J., Pfandl K., Stadler P., Chatzinotas A. 2005; High diversity of the ‘ Spumella -like’ flagellates: an investigation based on the SSU rRNA gene sequences of isolates from habitats located in six different geographic regions. Environ Microbiol 7:685–697 [CrossRef]
    [Google Scholar]
  9. Breunig A., Köning H., Brugerolle G., Vickerman K., Hertel H. 1993; Isolation and ultrastructural features of a new strain of Dimastigella trypaniformis Sandon 1928 (Bodonina, Kinetoplastida) and comparison with a previously isolated strain. Eur J Protistol 29:416–424 [CrossRef]
    [Google Scholar]
  10. Brugerolle G. 1985; Des trichocystes chez les bodonides, un caractère phylogénétique supplémentaire entre Kinetoplastida et Euglenida. Protistologica 21:339–348 (in French
    [Google Scholar]
  11. Callahan H. A., Litaker R. W., Noga E. J. 2002; Molecular taxonomy of the suborder Bodonina (Order Kinetoplastida), including the important fish parasite, Ichthyobodo necator . J Eukaryot Microbiol 49:119–128 [CrossRef]
    [Google Scholar]
  12. Caron D. A. 1987; Grazing of attached bacteria by heterotrophic microflagellates. Microb Ecol 13:203–218 [CrossRef]
    [Google Scholar]
  13. Cavalier-Smith T. 1981; Eukaryote kingdoms: seven or nine?. Biosystems 14:461–481 [CrossRef]
    [Google Scholar]
  14. Cavalier-Smith T. 1997; Cell and genome coevolution: facultative anaerobiosis, glycosomes and kinetoplastan RNA editing. Trends Genet 13:6–9 [CrossRef]
    [Google Scholar]
  15. Cavalier-Smith T. 2004; Only six kingdoms of life. Proc Biol Sci 271:1251–1262 [CrossRef]
    [Google Scholar]
  16. Dawson S. C., Pace N. R. 2002; Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad Sci U S A 99:8324–8329 [CrossRef]
    [Google Scholar]
  17. de Faria J. G., Cunha A. M., Pinto C. 1922; Estudos sobre protozoairos do mar. Mem Inst Oswaldo Cruz 15:186–208 (in Spanish [CrossRef]
    [Google Scholar]
  18. Del Giorgio P. A., Gasol J. M., Vaque D., Mura P., Agusti S., Duarte C. M. 1996; Bacterioplankton community structure: protists control net production and the proportion of active bacteria in a coastal marine community. Limnol Oceanogr 41:1169–1179 [CrossRef]
    [Google Scholar]
  19. Doležel D., Jirků M., Maslov D. A., Lukeš J. 2000; Phylogeny of the bodonid flagellates (Kinetoplastida) based on small-subunit rRNA gene sequences. Int J Syst Evol Microbiol 50:1943–1951
    [Google Scholar]
  20. Dyková I., Fiala I., Lom J., Lukeš J. 2003; Perkinsiella amoebae -like endosymbionts of Neoparamoeba spp., relatives of the kinetoplastid Ichthyobodo . Eur J Protistol 39:37–52 [CrossRef]
    [Google Scholar]
  21. Elbrächter M., Schnepf E., Balzer I. 1996; Haemistasia phaeocysticola (Scherffel) comb. nov., redescription of a free-living, marine, kinetoplastid flagellate. Arch Protistenkd 147:125–136 (in German [CrossRef]
    [Google Scholar]
  22. Eyden B. P. 1977; Morphology and ultrastructure of Bodo designis Skuja 1948. Protistologica 13:169–179
    [Google Scholar]
  23. Fenchel T., Finlay B. J. 1995 Ecology and Evolution in Anoxic Worlds Oxford: Oxford University Press;
    [Google Scholar]
  24. Foissner W. 1991; Diversity and ecology of soil flagellates. In The Biology of Free-Living Heterotrophic Flagellates pp  93–112 Edited by Patterson D. J., Larsen J. New York: Clarendon Press;
    [Google Scholar]
  25. Frolov A. O., Malysheva M. N. 2002; Ultrastructure of the flagellate Cruzella marina (Kinetoplastidea. Tsitologiia 44:447–484 (in Russian
    [Google Scholar]
  26. Hannaert V., Bringaud F., Opperdoes F. R., Michels P. A. M. 2003; Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid Biol Dis 2:11 [CrossRef]
    [Google Scholar]
  27. Hahn M. M., Lünsdorf H., Wu Q., Schauer M., Höfle M. G., Boenigk J., Stadler P. 2003; Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microbiol 69:1442–1451 [CrossRef]
    [Google Scholar]
  28. Hollande A. 1952; Ordre des Bodonides (Bodonidea ord. nov.). In Traité de Zoologie pp  669–693 Edited by Grassé P. P. Paris: Masson & Cie (in French
    [Google Scholar]
  29. Larsen J., Patterson D. J. 1990; Some flagellates (Protista) from tropical marine sediments. J Nat Hist 24:801–937 [CrossRef]
    [Google Scholar]
  30. López-García P., Rodriguez-Valera F., Pedros-Alio C., Moreira D. 2001; Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607 [CrossRef]
    [Google Scholar]
  31. López-García P., Philippe H., Gail F., Moreira D. 2003; Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci U S A 100:697–702 [CrossRef]
    [Google Scholar]
  32. Ludwig W., Strunk O., Westram R. 29 other authors 2004; arb: a software environment for sequence data. Nucleic Acids Res 32:1363–1371 [CrossRef]
    [Google Scholar]
  33. Lukeš J., Guilbride D. L., Votypka J., Zíkova J., Benne R., Englund P. T. 2002; Kinetoplast DNA network: evolution of an improbable structure. Eukaryot Cell 1:495–502 [CrossRef]
    [Google Scholar]
  34. Maddison D., Maddison W. 2000 MacClade 4: Analysis of Phylogeny and Character Evolution CD-ROM; Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  35. Moreira D., López-García P., Vickerman K. 2004; An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. Int J Syst Evol Microbiol 54:1861–1875 [CrossRef]
    [Google Scholar]
  36. Novarino G. 1996; Notes on flagellate nomenclature. I. Cryptaulaxoides nom. n.,a zoological substitute for Cryptaulax Skuja, 1948 (Protista incertae sedis) non Cryptaulax Tate, 1869 (Mollusca, Gastropoda) non Cryptaulax Cameron (Insecta, Hymenoptera), with remarks on botanical nomenclature. Acta Protozool 35:235–238
    [Google Scholar]
  37. Pernthaler J., Gloeckner F. O., Schoenhuber W., Amann R. 2001; Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol 30:207–226
    [Google Scholar]
  38. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [CrossRef]
    [Google Scholar]
  39. Reize I. B., Melkonian M. 1989; A new way to investigate living flagellated/ciliated cells in the light microscope: immobilization of cells in agarose. Bot Acta 102:145–151 [CrossRef]
    [Google Scholar]
  40. Reynolds E. S. 1963; The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212 [CrossRef]
    [Google Scholar]
  41. Simpson A. G., Lukeš J., Roger A. J. 2002; The evolutionary history of kinetoplastids and their kinetoplasts. Mol Biol Evol 19:2071–2083 [CrossRef]
    [Google Scholar]
  42. Skei J. M. 1988; Framvaren – environmental settings. Mar Chem 23:209–218 [CrossRef]
    [Google Scholar]
  43. Spurr A. R. 1969; A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43 [CrossRef]
    [Google Scholar]
  44. Stoeck T., Taylor G. T., Epstein S. S. 2003a; Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea. Appl Environ Microbiol 69:5656–5663 [CrossRef]
    [Google Scholar]
  45. Stoeck T., Fowle W. H., Epstein S. S. 2003b; Methodology of protistan discovery: from rRNA detection to quality scanning electron microscope images. Appl Environ Microbiol 69:6856–6863 [CrossRef]
    [Google Scholar]
  46. Swale E. M. F. 1973; A study of the colourless flagellate Rhynchomonas nasuta (Stokes) Klebs. Biol J Linn Soc 5:255–264 [CrossRef]
    [Google Scholar]
  47. Swofford D. L. 2001 paup* – Phylogenetic Analysis Using Parsimony (*and other methods) v. 4.0b6 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  48. 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]
  49. Tong S. 1997; Heterotrophic flagellates and other protists from Southampton water, UK. Ophelia 47:71–131 [CrossRef]
    [Google Scholar]
  50. Vickerman K. 1976; The diversity of the kinetoplastid flagellates. In Biology of the Kinetoplastida pp  1–34 Edited by Lumsden W. H. R., Evans D. A. London: Academic Press;
    [Google Scholar]
  51. Vickerman K. 2000a Order Kinetoplastea. In The Illustrated Guide to the Protozoa , pp. 1159–1185 Edited by Lee J. J., Leedale G. F., Bradbury P. Lawrence, KS: Allen Press;
    [Google Scholar]
  52. Vickerman K. 2000b; Adaptations to parasitism. In The Flagellates: Unity , Diversity and Evolution . pp  190–216 Edited by Leadbeater B. S. C., Green J. C. London: Taylor & Francis;
  53. von der Heyden S. 2004; Testing ubiquitous dispersal and freshwater/marine divergence in free-living protist groups . PhD thesis University of Oxford;
  54. von der Heyden S., Chao E. E., Vickerman K., Cavalier-Smith T. 2004; Ribosomal RNA phylogeny of bodonid and diplonemid flagellates and the evolution of Euglenozoa. J Eukaryot Microbiol 51:402–416 [CrossRef]
    [Google Scholar]
  55. Vørs N. 1992; Heterotrophic amoebae, flagellates and heliozoa from the Tvärminne area, Gulf of Finland, in 1988–1990. Ophelia 36:1–109 [CrossRef]
    [Google Scholar]
  56. Willerslev E., Hansen A. J., Christensen B., Steffensen J. P., Arctander P. 1999; Diversity of Holocene life forms in fossil glacier ice. Proc Natl Acad Sci U S A 96:8017–8021 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.63769-0
Loading
/content/journal/ijsem/10.1099/ijs.0.63769-0
Loading

Data & Media loading...

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