1887

Abstract

A fast-growing and cell-fusing hyperthermophilic archaeon was isolated from a hydrothermal vent at Suiyo Seamount, Izu-Bonin Arc, Western Pacific Ocean. Strain TS2 is an irregular, motile coccus that is generally 0.7–1.5 μm in diameter and possesses a polar tuft of flagella. In the mid-exponential phase of growth, cells that appeared black under phase-contrast microscopy fused at room temperature in the presence of a DNA-intercalating dye, as previously observed in . Cell fusion was not observed in later growth phases. Transmission electron microscopy revealed that the cells in the mid-exponential phase had a 5 nm-thick, electron-dense cell envelope that appeared to associate loosely with the cytoplasmic membrane. As the growth stage progressed, a surface layer developed on the membrane under the envelope and the envelope eventually peeled off. These observations suggest that the surface layer prevents the fusion of cells. Cells of strain TS2 grew at 50–85 °C, pH 5.6–8.3 and at NaCl concentrations of 1.0 to 4.5 %, with optimal growth occurring at 80 °C, pH 7.0 and 3.0 % NaCl. Under optimal growth conditions, strain TS2 grew very fast with an apparent doubling time of 20 min. It is suggested that the biosynthesis of the surface layer cannot catch up with cell multiplication in the mid-exponential phase and thus cells without the surface layer are generated. Strain TS2 was an anaerobic chemo-organotroph that grew on either yeast extract or tryptone as the sole growth substrate. The genomic DNA G+C content was 54.6 mol%. Phylogenetic analysis based on 16S rRNA gene sequencing indicated that the isolate belongs to the genus . However, no significant DNA–DNA hybridization was observed between the genomic DNA of strain TS2 and phylogenetically related species. On the basis of this evidence, strain TS2 is proposed to represent a novel species, sp. nov., a name chosen to reflect the fast growth of the strain. The type strain is TS2 (=NBRC 101555=JCM 13640=DSM 17994).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.64597-0
2007-03-01
2019-10-13
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/57/3/437.html?itemId=/content/journal/ijsem/10.1099/ijs.0.64597-0&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. Atomi, H., Fukui, T., Kanai, T., Morikawa, M. & Imanaka, T. ( 2004; ). Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1, 263–267.[CrossRef]
    [Google Scholar]
  3. Balch, W. E., Fox, G. E., Magrum, L. J., Woese, C. R. & Wolfe, R. S. ( 1979; ). Methanogens: reevaluation of a unique biological group. Microbiol Rev 43, 260–296.
    [Google Scholar]
  4. Canganella, F. & Jones, W. J. ( 1994; ). Microbial characterization of thermophilic Archaea isolated from the Guaymas Basin hydrothermal vent. Curr Microbiol 28, 299–306.[CrossRef]
    [Google Scholar]
  5. Canganella, F., Jones, W. J., Gambacorta, A. & Antranikian, G. ( 1998; ). Thermococcus guaymasensis sp. nov. and Thermococcus aggregans sp. nov., two novel thermophilic archaea isolated from the Guaymas Basin hydrothermal vent site. Int J Syst Bacteriol 48, 1181–1185.[CrossRef]
    [Google Scholar]
  6. Chen, E. H. & Olson, E. N. ( 2005; ). Unveiling the mechanisms of cell-cell fusion. Science 308, 369–373.[CrossRef]
    [Google Scholar]
  7. Duffaud, G. D., d'Hennezel, O. B., Peek, A. S., Reysenbach, A.-L. & Kelly, R. M. ( 1998; ). Isolation and characterization of Thermococcus barossii, sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal vent flange formation. Syst Appl Microbiol 21, 40–49.[CrossRef]
    [Google Scholar]
  8. Ezaki, T., Hashimoto, Y. & Yabuuchi, E. ( 1989; ). Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int J Syst Bacteriol 39, 224–229.[CrossRef]
    [Google Scholar]
  9. Godfroy, A., Meunier, J.-R., Guezennec, J., Lesongeur, F., Raguénès, G., Rimbault, A. & Barbier, G. ( 1996; ). Thermococcus fumicolans sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent in the North Fiji Basin. Int J Syst Bacteriol 46, 1113–1119.[CrossRef]
    [Google Scholar]
  10. Godfroy, A., Lesongeur, F., Raguénès, G., Quérellou, J., Antoine, E., Meunier, J.-R., Guezennec, J. & Barbier, G. ( 1997; ). Thermococcus hydrothermalis sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Int J Syst Bacteriol 47, 622–626.[CrossRef]
    [Google Scholar]
  11. González, J. M., Kato, C. & Horikoshi, K. ( 1995; ). Thermococcus peptonophilus sp. nov., a fast-growing, extremely thermophilic archaebacterium isolated from deep-sea hydrothermal vents. Arch Microbiol 164, 159–164.[CrossRef]
    [Google Scholar]
  12. Goris, J., Suzuki, K., De Vos, P., Nakase, T. & Kersters, K. ( 1998; ). Evaluation of a microplate DNA-DNA hybridization method compared with the initial renaturation method. Can J Microbiol 44, 1148–1153.[CrossRef]
    [Google Scholar]
  13. Grote, R., Li, L., Tamaoka, J., Kato, C., Horikoshi, K. & Antranikian, G. ( 1999; ). Thermococcus siculi sp. nov., a novel hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent at the Mid-Okinawa Trough. Extremophiles 3, 55–62.[CrossRef]
    [Google Scholar]
  14. Gupta, R. S. & Golding, G. B. ( 1996; ). The origin of the eukaryotic cell. Trends Biochem Sci 21, 166–171.[CrossRef]
    [Google Scholar]
  15. Honda, D. & Inouye, I. ( 2002; ). Ultrastructure and taxonomy of a marine photosynthetic stramenopile Phaeomonas parva gen. et sp. nov. (Pinguiophyceae) with emphasis on the flagellar apparatus architecture. Phycol Res 50, 75–89.[CrossRef]
    [Google Scholar]
  16. Horiike, T., Hamada, K., Miyata, D. & Shinozawa, T. ( 2004; ). The origin of eukaryotes is suggested as the symbiosis of Pyrococcus into γ-Proteobacteria by phylogenetic tree based on gene content. J Mol Evol 59, 606–619.[CrossRef]
    [Google Scholar]
  17. Inagaki, Y., Susko, E. & Roger, A. J. ( 2006; ). Recombination between elongation factor 1α genes from distantly related archaeal lineages. Proc Natl Acad Sci USA 103, 4528–4533.[CrossRef]
    [Google Scholar]
  18. Jolivet, E., L'Haridon, S., Corre, E., Forterre, P. & Prieur, D. ( 2003; ). Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol 53, 847–851.[CrossRef]
    [Google Scholar]
  19. Katayama-Fujimura, Y., Komatsu, Y., Kuraishi, H. & Kaneko, T. ( 1984; ). Estimation of DNA base composition by high performance liquid chromatography of its nuclease P1 hydrolysate. Agric Biol Chem 48, 3169–3172.[CrossRef]
    [Google Scholar]
  20. Kobayashi, T., Kwak, Y. S., Akiba, T., Kudo, T. & Horikoshi, K. ( 1994; ). Thermococcus profundus sp. nov., a new hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Syst Appl Microbiol 17, 232–236.[CrossRef]
    [Google Scholar]
  21. Kuwabara, T., Minaba, M., Iwayama, Y., Inouye, I., Nakashima, M., Marumo, K., Maruyama, A., Sugai, A., Itoh, T. & other authors ( 2005; ). Thermococcus coalescens sp. nov., a cell-fusing hyperthermophilic archaeon from Suiyo Seamount. Int J Syst Evol Microbiol 55, 2507–2514.[CrossRef]
    [Google Scholar]
  22. Lake, J. A., Moore, J. E., Simonson, A. B. & Rivera, M. C. ( 2005; ). Fulfilling Darwin's Dream. In Microbial Phylogeny and Evolution: Concepts and Controversies, pp. 184–206. Edited by J. Sapp. New York: Oxford University Press.
  23. Margulis, L. ( 1996; ). Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proc Natl Acad Sci U S A 93, 1071–1076.[CrossRef]
    [Google Scholar]
  24. Marmur, J. & Doty, P. ( 1962; ). Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5, 109–118.[CrossRef]
    [Google Scholar]
  25. Martin, W. & Müller, M. ( 1998; ). The hydrogen hypothesis for the first eukaryote. Nature 392, 37–41.[CrossRef]
    [Google Scholar]
  26. Miroshnichenko, M. L., Bonch-Osmolovskaya, E. A., Neuner, A., Kostrikina, N. A., Chernych, N. A. & Alekseev, V. A. ( 1989; ). Thermococcus stetteri sp. nov., a new extremely thermophilic marine sulfur-metabolizing archaebacterium. Syst Appl Microbiol 12, 257–262.[CrossRef]
    [Google Scholar]
  27. Miroshnichenko, M. L., Gongadze, G. M., Rainey, F. A., Kostyukova, A. S., Lysenko, A. M., Chernyh, N. A. & Bonch-Osmolovskaya, E. A. ( 1998; ). Thermococcus gorgonarius sp. nov. and Thermococcus pacificus sp. nov.: heterotrophic extremely thermophilic archaea from New Zealand submarine hot vents. Int J Syst Bacteriol 48, 23–29.[CrossRef]
    [Google Scholar]
  28. Moreira, D. & López-García, P. ( 1998; ). Symbiosis between methanogenic Archaea and δ-Proteobacteria as the origin of Eukaryotes: the syntrophic hypothesis. J Mol Evol 47, 517–530.[CrossRef]
    [Google Scholar]
  29. Nelson, K. E., Clayton, R. A., Gill, S. R., Gwinn, M. L., Dodson, R. J., Haft, D. H., Hickey, E. K., Peterson, J. D., Nelson, W. C. & other authors ( 1999; ). Evidence for lateral gene transfer between Archaea and Bacteria from genome sequence of Thermotoga maritima. Nature 399, 323–329.[CrossRef]
    [Google Scholar]
  30. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  31. Sugai, A., Masuchi, Y., Uda, I., Itoh, T. & Itoh, Y. H. ( 2000; ). Core lipids of hyperthermophilic archaeon, Pyrococcus horikoshii OT3. J Jpn Oil Chem Soc 49, 695–700.[CrossRef]
    [Google Scholar]
  32. Sugai, A., Uda, I., Itoh, Y. H. & Itoh, T. ( 2004; ). The core lipid composition of the 17 strains of hyperthermophilic Archaea, Thermococcales. J Oleo Sci 53, 41–44.[CrossRef]
    [Google Scholar]
  33. 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]
  34. Wächtershäuser, G. ( 2003; ). From pre-cells to Eukarya - a tale of two lipids. Mol Microbiol 47, 13–22.
    [Google Scholar]
  35. Wayne, L. G., Brenner, D. J., Colwell, R. R., Grimont, P. A. D., Kandler, O., Krichevsky, M. I., Moore, L. H., Moore, W. E. C., Murray, R. G. E. & other authors ( 1987; ). International Committee on Systematic Bacteriology. Report of the ad hoc committee on reconstitution of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]
    [Google Scholar]
  36. Woese, C. ( 1998; ). The universal ancestor. Proc Natl Acad Sci U S A 95, 6854–6859.[CrossRef]
    [Google Scholar]
  37. Zillig, W., Holz, I., Janekovic, D., Schäfer, W. & Reiter, W. D. ( 1983; ). The archaebacterium Thermococcus celer represents a novel genus within the thermophilic branch of the archaebacteria. Syst Appl Microbiol 4, 88–94.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.64597-0
Loading
/content/journal/ijsem/10.1099/ijs.0.64597-0
Loading

Data & Media loading...

[PDF] 

PDF

A movie showing cell fusion in strain TS2 . [mpg](opens with Windows Media Player, may not open with QuickTime) (7.5 MB)

MOVIE

Most Cited This Month

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