1887

Abstract

Strain CSC1, a Gram-negative, aerobic, methane-oxidizing bacterium, was isolated from an uncontaminated aquifer nearly 20 years ago. Based on 16S rRNA gene sequence similarity, this strain was identified as a member of the , most closely related to an uncultured member of the as well as two cultured organisms, sp. L32 and sp. SC2. This strain differed from extant species in cell shape, size, expression of soluble methane monooxygenase and its unique spiny surface layers, composed of polysaccharide. DNA–DNA hybridization results showed only 3.8 % relatedness with NCIMB 13100 and 41.1 % relatedness with SV97. Based on these genotypic and physiological differences, this isolate is proposed as a member of a novel species of the genus , sp. nov. (type strain CSC1 =ATCC BAA-1344 =DSM 18500).

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2007-08-01
2019-10-21
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References

  1. Adriaens, P. ( 1994; ). Evidence for chlorine migration during oxidation of 2-chlorobiphenyl by a type II methanotroph. Appl Environ Microbiol 60, 1658–1662.
    [Google Scholar]
  2. Adriaens, P. & Grbić-Galić, D. ( 1994; ). Cometabolic transformation of mono- and dichlorobiphenyls and chlorohydroxybiphenyls by methanotrophic groundwater isolates. Environ Sci Technol 28, 1325–1330.[CrossRef]
    [Google Scholar]
  3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. ( 1990; ). Basic local alignment search tool. J Mol Biol 215, 403–410.[CrossRef]
    [Google Scholar]
  4. Auman, A. J., Stolyar, S., Costello, A. M. & Lidstrom, M. E. ( 2000; ). Molecular characterization of methanotrophic isolates from freshwater lake sediment. Appl Environ Microbiol 66, 5259–5266.[CrossRef]
    [Google Scholar]
  5. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Smith, J. A., Seidman, J. G. & Struhl, K. (editors) ( 1989; ). Current Protocols in Molecular Biology. New York: Wiley.
  6. Bowman, J. P., Sly, L. I., Nichols, P. D. & Hayward, A. C. ( 1993; ). Revised taxonomy of the methanotrophs: description of Methylobacter gen. nov., emendation of Methylococcus, validation of Methylosinus and Methylocystis species and a proposal that the family Methylococcaceae includes only the group I methanotrophs. Int J Syst Bacteriol 43, 735–753.[CrossRef]
    [Google Scholar]
  7. Brusseau, G. A., Tsien, H. C., Hanson, R. S. & Wackett, L. P. ( 1990; ). Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1, 19–29.[CrossRef]
    [Google Scholar]
  8. Calhoun, A. & King, G. M. ( 1998; ). Characterization of root-associated methanotrophs from three freshwater macrophytes: Pontederia cordata, Sparganium eurycarpum, and Sagittaria latifolia. Appl Environ Microbiol 64, 1099–1105.
    [Google Scholar]
  9. Choi, D.-W., Kunz, R. C., Boyd, E. S., Semrau, J. D., Antholine, W. A., Han, J.-I., Zahn, J. A., Boyd, J. M., de la Mora, A. M. & DiSpirito, A. A. ( 2003; ). The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH : quinone oxidoreductase complex from Methylococcus capsulatus Bath. J Bacteriol 185, 5755–5764.[CrossRef]
    [Google Scholar]
  10. Costello, A. M. & Lidstrom, M. E. ( 1999; ). Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65, 5066–5074.
    [Google Scholar]
  11. Dedysh, S. N., Liesack, W., Khmelenina, V. N., Suzina, N. E., Trotsenko, Y. A., Semrau, J. D., Bares, A. M., Panikov, N. S. & Tiedje, J. M. ( 2000; ). Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Int J Syst Evol Microbiol 50, 955–969.[CrossRef]
    [Google Scholar]
  12. Dedysh, S. N., Khmelenina, V. N., Suzina, N. E., Trotsenko, Y. A., Semrau, J. D., Liesack, W. & Tiedje, J. M. ( 2002; ). Methylocapsa acidiphila gen. nov., sp. nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol 52, 251–261.
    [Google Scholar]
  13. Dedysh, S. N., Knief, C. & Dunfield, P. F. ( 2005; ). Methylocella species are facultatively methanotrophic. J Bacteriol 187, 4665–4670.[CrossRef]
    [Google Scholar]
  14. Dykstra, M. J. ( 1993; ). Manual of Applied Techniques for Biological Electron Microscopy. New York: Plenum.
  15. Easterbrook, K. B. ( 1989; ). Spinate bacteria. In Bergey's Manual of Systematic Bacteriology, vol. 3, pp. 1991–1993. Edited by J. T. Staley, M. P. Bryant, N. Pfennig & J. G. Holt. Baltimore: Williams & Wilkins.
  16. Easterbrook, K. B. & Alexander, S. A. ( 1983; ). The initiation and growth of bacterial spinae. Can J Microbiol 29, 476–487.[CrossRef]
    [Google Scholar]
  17. Easterbrook, K. B. & Sperker, S. ( 1982; ). Physiological controls of bacterial spinae production in complex medium and their value as indicators of spina function. Can J Microbiol 28, 130–136.[CrossRef]
    [Google Scholar]
  18. Fang, J., Barcelona, M. & Semrau, J. ( 2000; ). Characterization of methanotrophic bacteria on the basis of intact phospholipid profiles. FEMS Microbiol Lett 189, 67–72.[CrossRef]
    [Google Scholar]
  19. Fassel, T. A., Schaller, M. J., Lidstrom, M. E. & Remsen, C. C. ( 1990; ). Effect of fixation-resin combinations and ruthenium red on elucidating outer envelope structure and surface morphology of two methanotrophic bacteria. J Electron Microsc Tech 14, 52–62.[CrossRef]
    [Google Scholar]
  20. Fassel, T. A., Schaller, M. J. & Remsen, C. C. ( 1992; ). Comparison of Alcian blue and ruthenium red effects on preservation of outer envelope ultrastructure in methanotrophic bacteria. Microsc Res Tech 20, 87–94.[CrossRef]
    [Google Scholar]
  21. Gal'chenko, V. F., Shishkina, V. N., Suzina, N. E. & Trotsenko, Y. A. ( 1977; ). Isolation and properties of new strains of obligate methanotrophs. Mikrobiologiia 46, 723–728 (in Russian).
    [Google Scholar]
  22. Graham, D., Kim, H. Y. & Lindner, A. S. ( 2002; ). Methanotrophic bacteria. In Encyclopedia of Environmental Microbiology, pp. 1923–1936. Edited by G. Bitton. New York: Wiley.
  23. Hanson, R. S. & Hanson, T. E. ( 1996; ). Methanotrophic bacteria. Microbiol Rev 60, 439–471.
    [Google Scholar]
  24. Haubold, R. ( 1977; ). Two different types of surface structures of methane utilizing bacteria. Z Allg Mikrobiol 18, 511–515.
    [Google Scholar]
  25. Henry, S. M. & Grbić-Galić, D. ( 1990; ). Effect of mineral media on trichloroethylene oxidation by aquifer methanotrophs. Microb Ecol 20, 151–169.[CrossRef]
    [Google Scholar]
  26. Henry, S. M. & Grbić-Galić, D. ( 1991; ). Influence of endogenous and exogenous electron donors and trichloroethylene oxidation toxicity on trichloroethylene oxidation by methanotrophic cultures from a groundwater aquifer. Appl Environ Microbiol 57, 236–244.
    [Google Scholar]
  27. Heyer, J., Gal'chenko, V. & Dunfield, P. F. ( 2002; ). Molecular phylogeny of type II methane-oxidizing bacteria isolated from various environments. Microbiology 148, 2831–2846.
    [Google Scholar]
  28. Holmes, A. J., Costello, A., Lidstrom, M. E. & Murrell, J. C. ( 1995; ). Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132, 203–208.[CrossRef]
    [Google Scholar]
  29. Hršak, D. ( 1996; ). Cometabolic transformation of linear alkylbenzenesulphonates by methanotrophs. Water Res 30, 3092–3098.[CrossRef]
    [Google Scholar]
  30. Hršak, D. & Begonja, A. ( 1998; ). Growth characteristics and metabolic activities of the methanotrophic-heterotrophic groundwater community. J Appl Microbiol 85, 448–456.[CrossRef]
    [Google Scholar]
  31. Lane, D. J. ( 1991; ). 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics, pp. 115–175. Edited by E. Stackebrandt & M. Goodfellow. New York: Wiley.
  32. Lewis, P. R. & Knight, D. P. ( 1977; ). Staining Methods for Sectioned Material. Amsterdam: North-Holland.
  33. Lloyd, J. S., DeMarco, P., Dalton, H. & Murrell, J. C. ( 1999; ). Heterologous expression of soluble methane monooxygenase genes in methanotrophs containing only particulate methane monooxygenase. Arch Microbiol 171, 364–370.[CrossRef]
    [Google Scholar]
  34. Lontoh, S. & Semrau, J. D. ( 1998; ). Methane and trichloroethylene degradation by Methylosinus trichosporium OB3b expressing particulate methane monooxygenase. Appl Environ Microbiol 64, 1106–1114.
    [Google Scholar]
  35. McDonald, I. R. & Murrell, J. C. ( 1997; ). The methanol dehydrogenase structural gene mxaF and its use as a functional gene probe for methanotrophs and methylotrophs. Appl Environ Microbiol 63, 3218–3224.
    [Google Scholar]
  36. McDonald, I. R., Uchiyama, H., Kame, S., Yagi, O. & Murrell, J. C. ( 1997; ). The soluble methane monooxygenase gene cluster of the trichloroethylene-degrading methanotroph Methylocystis sp. strain M. Appl Environ Microbiol 63, 1898–1904.
    [Google Scholar]
  37. Meyer, J., Haubold, J., Heyer, J. & Bökel, W. ( 1986; ). Contribution to the taxonomy of methanotrophic bacteria: correlation between membrane type and GC-value. J Basic Microbiol 26, 155–160.[CrossRef]
    [Google Scholar]
  38. Mignot, T., Denis, B., Couture-Tosi, E., Kolsto, A.-B., Mock, M. & Fouet, A. ( 2001; ). Distribution of S-layers on the surface of Bacillus cereus strains: phylogenetic origin and ecological pressure. Environ Microbiol 3, 493–501.[CrossRef]
    [Google Scholar]
  39. Minsky, A., Shimoni, E. & Frenkiel-Krispin, D. ( 2002; ). Stress, order and survival. Nat Rev Mol Cell Biol 3, 50–60.[CrossRef]
    [Google Scholar]
  40. Monneron, A. & Bernhard, W. ( 1966; ). Action de certaines enzymes sur des tissus inclus en Epon. J Microsc 5, 697–714 (in French).
    [Google Scholar]
  41. Murrell, J. C. & Radejewski, S. ( 2000; ). Cultivation-independent techniques for studying methanotroph ecology. Res Microbiol 151, 807–814.[CrossRef]
    [Google Scholar]
  42. Norris, J. R. & Ribbons, D. W. (editors) ( 1971; ). Methods in Microbiology, vol. 6A. London: Academic Press.
  43. Page, R. D. M. ( 1996; ). TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358.
    [Google Scholar]
  44. Prior, S. D. & Dalton, H. ( 1985; ). Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath). FEMS Microbiol Lett 29, 105–109.[CrossRef]
    [Google Scholar]
  45. Sára, M. & Sleytr, U. B. ( 1987; ). Molecular sieving through S-layers of Bacillus stearothermophilus strains. J Bacteriol 169, 4092–4098.
    [Google Scholar]
  46. Sára, M., Pum, D. & Sleytr, U. B. ( 1992; ). Permeability and charge-dependent adsorption properties of the S-layer lattice from Bacillus coagulans E36-66. J Bacteriol 174, 3487–3493.
    [Google Scholar]
  47. Sidhu, M. S. & Olsen, I. ( 1997; ). S-layers of Bacillus species. Microbiology 143, 1039–1052.[CrossRef]
    [Google Scholar]
  48. Sleytr, U. B. & Messner, P. ( 1988; ). Crystalline surface layers in prokaryotes. J Bacteriol 170, 2891–2897.
    [Google Scholar]
  49. Sleytr, U. B., Messner, P., Pum, D. & Sara, M. ( 1993; ). Crystalline bacterial cell surface layers: general principles and application potential. J Appl Bacteriol 74, S21–S32.[CrossRef]
    [Google Scholar]
  50. Smibert, R. M. & Krieg, N. R. ( 1981; ). General characterization. In Manual of Methods for General Bacteriology, pp. 409–443. Edited by G. B. Phillips. Washington, DC: American Society for Microbiology.
  51. Sorokin, D. Y., Jones, B. E. & Kuenen, J. G. ( 2000; ). An obligate methylotrophic, methane-oxidizing Methylomicrobium species from a highly alkaline environment. Extremophiles 4, 145–155.[CrossRef]
    [Google Scholar]
  52. Stanley, S. H., Prior, S. D., Leak, D. J. & Dalton, H. ( 1983; ). Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. Biotechnol Lett 5, 487–492.[CrossRef]
    [Google Scholar]
  53. Theisen, A. R. & Murrell, J. C. ( 2005; ). Facultative methanotrophs revisited. J Bacteriol 187, 4303–4305.[CrossRef]
    [Google Scholar]
  54. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  55. Trotsenko, Y. A. & Khmelenina, V. N. ( 2002; ). The biology and osmoadaptation of haloalkaliphilic methanotrophs. Microbiology (English translation of Mikrobiologiia) 71, 123–132.
    [Google Scholar]
  56. Tsien, H. C. & Hanson, R. S. ( 1992; ). Soluble methane monooxygenase component B gene probe for identification of methanotrophs that rapidly degrade trichloroethylene. Appl Environ Microbiol 58, 953–960.
    [Google Scholar]
  57. Wartiainen, I., Grethe Hestnes, A., McDonald, I. R. & Svenning, M. M. ( 2006; ). Methylocystis rosea sp. nov., a novel methanotrophic bacterium from Arctic wetland soil, Svalbard, Norway (7 ° N). Int J Syst Evol Microbiol 56, 541–547.[CrossRef]
    [Google Scholar]
  58. Wayne, L. G., Brenner, D. J., Colwell, R. R., Grimont, P. A. D., Kandler, O., Krichevskey, 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 reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37, 463–464.[CrossRef]
    [Google Scholar]
  59. Whittenbury, R., Phillips, K. C. & Wilkinson, J. F. ( 1970; ). Enrichment, isolation, and some properties of methane-utilizing bacteria. J Gen Microbiol 61, 205–218.[CrossRef]
    [Google Scholar]
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Phylogenetic relationships of the partial and gene sequences of strain CSC1 and members of related genera. [PDF](19 KB)

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Electron microscope cytochemistry of the S-layer of strain CSC1 . (a) Surface of a cell fixed initially with glutaraldehyde alone. The spiny layer is indistinct and lightly stained. (b) Surface of a cell fixed initially with a glutaraldehyde/Alcian blue mixture to stain polysaccharide selectively. Compared with (a), the spiny layer stains darker and is thicker and is more distinct. (c, d) Cells after Pronase digestion. In (c), a cross-section, a light layer around the cell has been left where the Pronase has removed the protein in the S-layer. In (d), a grazing section of the spines at the cell surface, numerous light spots in the plastic show where the Pronase has removed the spikes. Bars, 0.2 µm.

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