Taxonomic Study of Aromatic-Degrading Bacteria from Deep-Terrestrial-Subsurface Sediments and Description of sp. nov., sp. nov., and sp. nov. Free

Abstract

Abstract

Phylogenetic analyses of 16S rRNA gene sequences by distance matrix and parsimony methods indicated that six strains of bacteria isolated from deep saturated Atlantic coastal plain sediments were closely related to the genus Five of the strains clustered with, but were distinct from, whereas the sixth strain was most closely related to The five strains that clustered with all of which could degrade aromatic compounds, were gram-negative, non-spore-forming, non-motile, rod-shaped organisms that produced small, yellow colonies on complex media. Their G+C contents ranged from 60.0 to 65.4 mol%, and the predominant isoprenoid quinone was ubiquinone Q-10. All of the strains were aerobic and catalase positive. Indole, urease, and arginine dihydrolase were not produced. Gelatin was not liquified, and glucose was not fermented. Sphingolipids were present in all strains; 2OH14:0 was the major hydroxy fatty acid, and 18:1 was a major constituent of cellular lipids. Acid was produced oxidatively from pentoses, hexoses, and disaccharides, but not from polyalcohols and indole. All of these characteristics indicate that the five aromatic-degrading strains should be placed in the genus as currently denned. Phylogenetic analysis of 16S rRNA gene sequences, DNA-DNA reassociation values, BOX-PCR genomic fingerprinting, differences in cellular lipid composition, and differences in physiological traits all indicated that the five strains represent three previously undescribed species. Therefore, we propose the following new species: (type strain, SMCC F199), (type strain, SMCC B0478), and (type strain, SMCC B0712).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/00207713-47-1-191
1997-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/47/1/ijs-47-1-191.html?itemId=/content/journal/ijsem/10.1099/00207713-47-1-191&mimeType=html&fmt=ahah

References

  1. Applied Biosystems, Inc. 1992 Taq DyeDeoxy terminator cycle sequencing kit user bulletin no. 901497, revision E Applied Biosystems, Inc.; Foster City, Calif.:
    [Google Scholar]
  2. Balkwill D. L. 1989; Numbers, diversity, and morphological characteristics of aerobic, chemoheterotrophic bacteria in deep subsurface sediments from a site in South Carolina. Geomicrobiol. J. 7:33–51
    [Google Scholar]
  3. Balkwill D. L. 1993; DOE makes subsurface cultures available. ASM News 59:504–506
    [Google Scholar]
  4. Balkwill D. L., Fredrickson J. K., Thomas J. M. 1989; Vertical and horizontal variations in the physiological diversity of the aerobic chemoheterotrophic bacterial microflora in deep Southeast Coastal Plain subsurface sediments. Appl. Environ. Microbiol. 55:1058–1065
    [Google Scholar]
  5. Balkwill D. L., Ghiorse W. C. 1985; Characterization of subsurface bacteria associated with two shallow aquifers in Oklahoma. Appl. Environ. Microbiol. 50:580–588
    [Google Scholar]
  6. Bligh E. C., Dyer W. J. 1959; A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:910–917
    [Google Scholar]
  7. Boone D. R., Liu Y., Zhao Z.-J., Balkwill D. L., Drake G. R., Stevens T. O., Aldrich H. C. 1995; Bacillus infernus sp. nov., an Fe(III)- and Mn(IV)-reducing anaerobe from the deep terrestrial subsurface. Int. J. Syst. Bacteriol. 45:441–448
    [Google Scholar]
  8. Brosius J., Palmer M. L., Kennedy P. J., Noller H. R. 1979; Complete nucleotide sequence of a 16S ribosomal gene from Escherichia coli. Proc. Natl. Acad. Sci. USA 75:4801–4805
    [Google Scholar]
  9. Chapelle F. H. 1993 Ground-water microbiology and geochemistry John Wiley & Sons, Inc.; New York, N.Y.:
    [Google Scholar]
  10. Denhardt D. T. 1966; A membrane-filter technique for the detection of complementary DNA. Biochem. Biophys. Res. Commun. 23:641–646
    [Google Scholar]
  11. Devereux R., He S. H., Orkland S., Stahl D. A., LeGall J., Whitman W. B. 1990; Diversity and origin of Desulfovibrio species: phylogenetic definition of a family. J. Bacteriol. 172:3609–3613
    [Google Scholar]
  12. Doetsch R. N. 1981; Determinative methods in light microscopy. 21–33 Gerhardt P., Murray R. G. E., Costilow R. N., Nester E. W., Wood W. A., Krieg N. R., Phillips G. B. Manual of methods for general bacteriology American Society for Microbiology; Washington, D.C.:
    [Google Scholar]
  13. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
    [Google Scholar]
  14. Felsenstein J. 1993 PHYLIP (phylogeny inference package) version 3.5c J. Felsenstein, University of Washington; Seattle:
    [Google Scholar]
  15. Fitch W. M., Margoliash E. 1967; Construction of phylogenetic trees. Science 155:279–284
    [Google Scholar]
  16. Fredrickson J. K., Balkwill D. L., Drake G. R., Romine M. F., Ringelberg D. B., White D. C. 1995; Aromatic-degrading Sphingomonas from the deep subsurface. Appl. Environ. Microbiol. 61:1917–1922
    [Google Scholar]
  17. Fredrickson J. K., Balkwill D. L., Zachara J. M., Li S. W., Brockman F. J., Simmons M. A. 1991; Physiological diversity and distributions of heterotrophic bacteria in deep Cretaceous sediments of the Atlantic Coastal Plain. Appl. Environ. Microbiol. 57:402–411
    [Google Scholar]
  18. Fredrickson J. K., Brockman F. J., Workman D. J., Li S. W., Stevens T. O. 1991; Isolation and characterization of a subsurface bacterium capable of growth on toluene, naphthalene, and other aromatic compounds. Appl. Environ. Microbiol. 57:796–803
    [Google Scholar]
  19. Fredrickson J. K., Garland T. R., Hicks R. J., Thomas J. M., Li S. W., McFadden K. M. 1989; Autotrophic and heterotrophic bacteria in deep subsurface sediments and their relationship to sediment properties. Geomicrobiol. J. 7:53–56
    [Google Scholar]
  20. Fuerst J. A., Hawkins J. A., Holmes A. J., Sly L. T., Moore C. J., Stackebrandt E. 1993; Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from freshwater. Int. J. Syst. Bacteriol. 43:125–134
    [Google Scholar]
  21. Govindaswami M., Schmidt T. M., White D. C., Loper J. C. 1993; Phylogenetic analysis of a bacterial aerobic degrader of azo dyes. J. Bacteriol. 175:6062–6066
    [Google Scholar]
  22. Guckert J. B., Ringelberg D. B., White D. C., Hanson R. S., Bratina B. J. 1991; Membrane fatty acids as phenotypic markers in the polyphasic taxonomy of methylotrophs within the proteobacteria. J. Gen. Microbiol. 137:2631–2641
    [Google Scholar]
  23. Haldeman D. L., Amy P. S., Ringelberg D., White D. C. 1993; Char acterization of the microbiology within a 21 m3 section of rock from the deep subsurface. Microb. Ecol. 26:145–159
    [Google Scholar]
  24. Hugenholtz P., Stackebrandt E., Fuerst J. A. 1994; A phylogenetic analysis of the genus Blastobacter with a view to its future reclassification. Syst. Appl. Microbiol. 17:51–57
    [Google Scholar]
  25. Imai R., Nagata Y., Fukada M., Takagi M., Yano K. 1991; Molecular cloning of a Pseudomonas paucimobilis gene encoding for a 17-kilodalton polypeptide that eliminates HCl molecules from γ-hexachlorocyclohexane. J. Bacteriol. 173:6811–6819
    [Google Scholar]
  26. Johnson J. L. 1981; Genetic characterization. 450–472 Gerhardt P., Murray R. G. E., Costilow R. N., Nester E. W., Wood W. A., Krieg N. R., Phillips G. B. Manual of methods for general bacteriology American Society for Microbiology; Washington, D.C.:
    [Google Scholar]
  27. Johnson J. L. 1991; DNA reassociation experiments. 21–44 Stackebrandt E., Goodfellow M. Nucleic acid techniques in bacterial systematics John Wiley and Sons Ltd.; London, United Kingdom:
    [Google Scholar]
  28. Jukes T. H., Cantor C. R. 1969; Evolution of protein molecules. 21–132 Munro H. N. Mammalian protein metabolism Academic Press; New York, N.Y.:
    [Google Scholar]
  29. Karlson U., Rojo F., van Elsas J. D., Moore E. R. B. 1996; Genetic and serological evidence for the recognition of 4 pentachlorophenol-degrading bacterial strains as a species of the genus Sphingomonas. Appl. Syst. Microbiol. 18:539–548
    [Google Scholar]
  30. Kazuyoshi K., Seydel U., Matsuura M., Danbara H., Rietschel E. T., Zahringer U. 1991; Chemical structure of glycosphingolipids isolated from Sphingomonas paucimobilis. Fed. Eur. Biochem. Soc. Lett. 292:107–110
    [Google Scholar]
  31. Khan A. A., Wang R.-F., Cao W.-W., Franklin W., Cerniglia C. E. 1996; Reclassification of a polycyclic aromatic hydrocarbon-metabolizing bacterium, Beijerinckia sp. strain B1, as Sphingomonas yanoikuyae by fatty acid analysis, protein pattern analysis, DNA-DNA hybridization, and 16S ribosomal DNA sequencing. Int. J. Syst. Bacteriol. 46:466–469
    [Google Scholar]
  32. Kim E., Aversano P. J., Romine M. F., Schneider R. P., Zylstra G. J. 1996; Homology between genes for aromatic hydrocarbon degradation in surface and deep-subsurface Sphingomonas strains. Appl. Environ. Microbiol. 62:1467–1470
    [Google Scholar]
  33. Kuhm A. E., Stolz A., Ngai K.-L., Knackmuss H.-J. 1991; Purification and characterization of a 1,2-dihydroxynaphthalene dioxygenase from a bacterium that degrades naphthalenesulfonic acids. J. Bacteriol. 173:3795–3802
    [Google Scholar]
  34. Lane D. J., Pace G., Olsen G. E., Stahl D. A., Sogin M. L., Pace N. R. 1985; Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. USA 82:6955–6959
    [Google Scholar]
  35. Louws F. J., Fulbright D. W., Stephens C. T., de Bruijn F. J. 1994; Specific genomic fingerprints of phytopathogenic Xanthomonas and Pseudomonas pathovars and strains generated with repetitive sequences and PCR. Appl. Environ. Microbiol. 60:2286–2295
    [Google Scholar]
  36. Maidak B. L., Larsen N., McCaughey M. J., Overbeek R., Olsen G. J., Fogel K., Blandy J., Woese C. R. 1994; The Ribosomal Database Project. Nucleic Acids Res. 22:3485–3487
    [Google Scholar]
  37. Martin B., Humbert O., Camara M., Guenzi E., Walker J., Mitchell T., Andrew P., Prudhomme M., Alloing G., Hakenback R., Morrison D. A., Boulnois G. J., Claverys J. 1992; A highly conserved repetitive element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res. 20:3479–3483
    [Google Scholar]
  38. Mayberry W. R., Lane J. R. 1993; Sequential saponification/acid hydrolysis/esterification in a one-tube method with enhanced recovery of both cyclopropane and hydroxylated fatty acids. J. Microbiol. Methods 18:21–32
    [Google Scholar]
  39. McBride L. J., Koepf S. M., Gibbs R. A., Salser W., Mayrand P. E., Hunkapiller M. W., Kronick M. N. 1989; Automated DNA sequencing methods involving polymerase chain reaction. Clin. Chem. 35:2196–2201
    [Google Scholar]
  40. Mesbah M., Whitman W. B. 1989; Measurement of deoxyguanosine/thymidine ratios in complex mixtures by high-performance liquid chromatography for determination of the mole percentage guanine + cytosine of DNA. J. Chromatogr. 479:297–306
    [Google Scholar]
  41. Moore E. R. B., Wittich R.-M., Fortnagel P., Timmis K. N. 1993; 16S ribosomal RNA gene sequence characterization and phylogenetic analysis of a dibenzo-p-dioxin-degrading isolate within the new genus Sphingomonas. Lett. Appl. Microbiol. 17:115–118
    [Google Scholar]
  42. Mueller J. G., Chapman P. J., Blattman B. O., Pritchard P. H. 1990; Isolation of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl. Environ. Microbiol. 56:1079–1086
    [Google Scholar]
  43. Murphy E. M., Schramke J. A., Fredrickson J. K., Bledsoe H. W., Francis A. J., Sklarew D. S., Linehan J. C. 1992; The influence of microbial activity and sedimentary organic carbon on the isotope geochemistry of the Middendorf Aquifer. Water Resour. Res. 28:723–740
    [Google Scholar]
  44. Nichols P. D., Volkman J. K., Johns R. B. 1983; Sterols and fatty acids of the marine unicellular alga, FCRG51. Phytochemistry 22:1447–1452
    [Google Scholar]
  45. Nohynek L. J., Nurmiaho-Lassila E.-L., Suhonen E. I., Busse H.-J., Mohammadi M., Hantula J., Rainey F., Salkinoja-Salonen M. S. 1996; Description of chlorophenol-degrading Pseudomonas sp. strains KF1T, KF3, and NKF1 as a new species of the genus Sphingomonas, Sphingomonas subarctica sp. nov.. Int. J. Syst. Bacteriol. 46:1042–1055
    [Google Scholar]
  46. Pedersen K., Ekendahl S. 1990; Distribution and activity of bacteria in deep granitic groundwaters of southeastern Sweden. Microb. Ecol. 20:37–52
    [Google Scholar]
  47. Reeves R. H., Reeves J. Y., Balkwill D. L. 1995; Strategies for phylogenetic characterization of subsurface bacteria. J. Microbiol. Methods 21:235–251
    [Google Scholar]
  48. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular cloning: a laboratory manual, 2nd ed.. Cold Spring Harbor Laboratory; Cold Spring Harbor, N.Y.:
    [Google Scholar]
  49. Schmidt S., Wittich R.-M., Erdmann D., Wilkes H., Francke W., Fortnagel P. 1992; Biodegradation of diphenyl ether and its monohalogenated derivatives by Sphingomonas sp. strain SS3. Appl. Environ. Microbiol. 58:2744–2750
    [Google Scholar]
  50. Stackebrandt E., Goebel B. M. 1994; Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int. J. Syst. Bacteriol. 44:846–849
    [Google Scholar]
  51. Stahl D. A., Key R., Flesher B., Smit J. 1992; The phylogeny of marine and freshwater caulobacters. J. Bacteriol. 174:2193–2198
    [Google Scholar]
  52. Stevens T. O., McKinley J. P., Fredrickson J. K. 1993; Bacteria associated with deep, alkaline, anaerobic groundwaters in southeast Washington. Microb. Ecol. 25:35–50
    [Google Scholar]
  53. Stillwell L. C., Thurston S. J., Schneider R. P., Romine M. F., Fredrickson J. K., Salter J. D. 1995; Physical mapping and characterization of a catabolic plasmid from the deep-subsurface bacterium Sphingomonas sp. strain F199. J. Bacteriol. 177:4537–4539
    [Google Scholar]
  54. Swofford D. L. 1993 PAUP: phylogenetic analysis using parsimony, 3.0rd ed.. Illinois Natural History Survey; Champaign:
    [Google Scholar]
  55. Taira K., Hayase N., Arimura N., Yamashita S., Miyazaki T., Furukawa K. 1988; Cloning and nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene from the PCB-degrading strain of Pseudomonas paucimobilis Q1. Biochemistry 27:3990–3996
    [Google Scholar]
  56. Takeuchi M., Kawai F., Shimada Y., Yokota A. 1993; Taxonomic study of polyethylene glycol-utilizing bacteria: emended description of the genus Sphingomonas and new descriptions of Sphingomonas macrogoltabidus sp. nov., Sphingomonas sanguis sp. nov. and Sphingomonas terrae sp. nov.. Syst. Appl. Microbiol. 16:227–238
    [Google Scholar]
  57. Takeuchi M., Sakane T., Yanagi M., Yamasato K., Hamana K., Yokota A. 1995; Taxonomic study of bacteria isolated from plants: proposal of Sphingomonas rosa sp. nov., Sphingomonas pruni sp. nov., Sphingomonas asaccharolytica sp. nov., and Sphingomonas mali sp. nov.. Int. J. Syst. Bacteriol. 45:334–341
    [Google Scholar]
  58. Takeuchi M., Sawada H., Oyaizu H., Yokota A. 1994; Phylogenetic evidence for Sphingomonas and Rhizomonas as nonphotosynthetic members of the alpha-4 subclass of the Proteobacteria. Int. J. Syst. Bacteriol. 44:308–314
    [Google Scholar]
  59. van Bruggen A. H. C., Jochimsen K. N., Steinberger E. M., Segers P., Gillis M. 1993; Classification of Rhizomonas suberifaciens, unnamed Rhizomonas species, and Sphingomonas spp. in rRNA superfamily IV. Int. J. Syst. Bacteriol. 43:1–7
    [Google Scholar]
  60. Versalovic J., Schneider M., de Bruijn F. J., Lupski J. R. 1994; Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 5:23–40
    [Google Scholar]
  61. Wang Y., Lau P. C. K. 1996; Sequence and expression of an isocitrate dehydrogenase-encoding gene from a polycyclic aromatic hydrocarbon oxidizer, Sphingomonas yanoikuyae Bl. Gene 168:15–21
    [Google Scholar]
  62. Wayne L. G., Brenner D. J., Colwell R. R., Grimont P. A. D., Kandier O., Krichevsky M. L., Moore L. H., Moore W. E. C., Murray R. G. E., Stackebrandt E., Starr M. P., Trüper H. G. 1987; Report of the Ad Hoc Committee on Reconciliation of Approaches to Bacterial Systematics. Int. J. Syst. Bacteriol. 37:463–464
    [Google Scholar]
  63. Weisberg W. G., Barns S. M., Pelletier D. A., Lane D. J. 1991; 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697–703
    [Google Scholar]
  64. Wittich R.-M., Wilkes H., Sinnwell V., Francke W., Fortnagel P. 1992; Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl. Environ. Microbiol. 58:1005–1010
    [Google Scholar]
  65. Yabuuchi E., Yano I., Oyaizu H., Hashimoto Y., Ezaki T., Yamamoto H. 1990; Proposals of Sphingomonas paucimobilis gen. nov. and comb, nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb, nov., and two genospecies of the genus Sphingomonas. Microbiol. Immunol. 34:99–119
    [Google Scholar]
  66. Yurkov V., Stackebrandt E., Holmes A., Fuerst J. A., Hugenholtz P., Golecki J., Gad’on N., Gorlenko V. M., Kompantseva E. I., Drews G. 1994; Phylogenetic positions of novel aerobic bacteriochlorophyll a -containing bacteria and descriptions of Roseococcus thiosolfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov.. Int. J. Syst. Bacteriol. 44:427–434
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/00207713-47-1-191
Loading
/content/journal/ijsem/10.1099/00207713-47-1-191
Loading

Data & Media loading...

Most cited Most Cited RSS feed