1887

Abstract

Two novel strictly anaerobic bacteria, strains Bs105 and Bs107, were isolated from a deep aquifer-derived hydrocarbonoclastic community. The cells were rod-shaped, not motile and had terminal spores. Phylogenetic affiliation and physiological properties revealed that these isolates belong to two novel species of the genus Desulfotomaculum . Optimal growth temperatures for strains Bs105 and Bs107 were 42 and 45 °C, respectively. The estimated G+C content of the genomic DNA was 42.9 and 48.7 mol%. For both strains, the major cellular fatty acid was palmitate (C16 : 0). Specific carbon fatty acid signatures of Gram-positive bacteria (iso-C17 : 0) and sulfate-reducing bacteria (C17 : 0 cyc) were also detected. An insertion was revealed in one of the two 16S rRNA gene copies harboured by strain Bs107. Similar insertions have previously been highlighted among moderately thermophilic species of the genus Desulfotomaculum . Both strains shared the ability to oxidize aromatic acids (Bs105: hydroquinone, acetophenone, para-toluic acid, 2-phenylethanol, trans-cinnamic acid, 4-hydroxybenzaldehyde, benzyl alcohol, benzoic acid 4-hydroxybutyl ester; Bs107: ortho-toluic acid, benzoic acid 4-hydroxybutyl ester). The names Desulfotomaculum aquiferis sp. nov. and Desulfotomaculum profundi sp. nov. are proposed for the type strains Bs105 (=DSM 24088=JCM 31386) and Bs107 (=DSM 24093=JCM 31387).

Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.001352
2016-11-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/66/11/4329.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.001352&mimeType=html&fmt=ahah

References

  1. Acinas S. G., Marcelino L. A., Klepac-Ceraj V., Polz M. F..( 2004;). Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. . J Bacteriol186:2629–2635. [CrossRef][PubMed]
    [Google Scholar]
  2. Alawi M., Lerm S., Vetter A., Wolfgramm M., Seibt A., Würdemann H..( 2011;). Diversity of sulfate-reducing bacteria in a plant using deep geothermal energy. . Grundwasser16:105–112. [CrossRef]
    [Google Scholar]
  3. Aoki M., Kakiuchi R., Yamaguchi T., Takai K., Inagaki F., Imachi H..( 2015;). Phylogenetic diversity of aprA genes in subseafloor sediments on the northwestern pacific margin off Japan. . Microbes Environ30:276–280. [CrossRef][PubMed]
    [Google Scholar]
  4. Aüllo T., Ranchou-Peyruse A., Ollivier B., Magot M..( 2013;). Desulfotomaculum spp. and related gram-positive sulfate-reducing bacteria in deep subsurface environments. . Front Microbiol4:362. [CrossRef][PubMed]
    [Google Scholar]
  5. Aüllo T., Berlendis S., Lascourrèges J. F., Dessort D., Duclerc D., Saint-Laurent S., Schraauwers B., Mas J., Patriarche D. et al.( 2016;). New bio-indicators for long term natural attenuation of monoaromatic compounds in deep terrestrial aquifers. . Front Microbiol7:122. [CrossRef][PubMed]
    [Google Scholar]
  6. Baker B. J., Moser D. P., MacGregor B. J., Fishbain S., Wagner M., Fry N. K., Jackson B., Speolstra N., Loos S. et al.( 2003;). Related assemblages of sulphate-reducing bacteria associated with ultradeep gold mines of South Africa and deep basalt aquifers of Washington State. . Env Microbiol5:267–277. [CrossRef]
    [Google Scholar]
  7. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S..( 1979;). Methanogens: reevaluation of a unique biological group. . Microbiol Rev43:260–296.[PubMed]
    [Google Scholar]
  8. Basso O., Lascourrèges J. F., Jarry M., Magot M..( 2005;). The effect of cleaning and disinfecting the sampling well on the microbial communities of deep subsurface water samples. . Environ Microbiol7:13–21. [CrossRef][PubMed]
    [Google Scholar]
  9. Basso O., Lascourreges J. F., Le Borgne F., Le Goff C., Magot M..( 2009;). Characterization by culture and molecular analysis of the microbial diversity of a deep subsurface gas storage aquifer. . Res Microbiol160:107–116. [CrossRef][PubMed]
    [Google Scholar]
  10. Berlendis S., Lascourreges J. F., Schraauwers B., Sivadon P., Magot M..( 2010;). Anaerobic biodegradation of BTEX by original bacterial communities from an underground gas storage aquifer. . Environ Sci Technol44:3621–3628. [CrossRef][PubMed]
    [Google Scholar]
  11. Case R. J., Boucher Y., Dahllöf I., Holmström C., Doolittle W. F., Kjelleberg S..( 2007;). Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. . Appl Environ Microbiol73:278–288. [CrossRef][PubMed]
    [Google Scholar]
  12. Cashion P., Holder-Franklin M. A., McCully J., Franklin M..( 1977;). A rapid method for the base ratio determination of bacterial DNA. . Anal Biochem81:461–466. [CrossRef][PubMed]
    [Google Scholar]
  13. Cha I. T., Roh S. W., Kim S. J., Hong H. J., Lee H. W., Lim W. T., Rhee S. K..( 2013;). Desulfotomaculum tongense sp. nov., a moderately thermophilic sulfate-reducing bacterium isolated from a hydrothermal vent sediment collected from the Tofua Arc in the Tonga Trench. . Antonie Van Leeuwenhoek104:1185–1192. [CrossRef][PubMed]
    [Google Scholar]
  14. Cord-Ruwisch R..( 1985;). A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria. . J Microbiol Methods4:33–36. [CrossRef]
    [Google Scholar]
  15. Daumas S., Cord-Ruwisch R., Garcia J. L..( 1988;). Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water. . Antonie Van Leeuwenhoek54:165–178. [CrossRef][PubMed]
    [Google Scholar]
  16. de Rezende J. R., Kjeldsen K. U., Hubert C. R., Finster K., Loy A., Jørgensen B. B..( 2013;). Dispersal of thermophilic Desulfotomaculum endospores into baltic sea sediments over thousands of years. . ISME J7:72–84. [CrossRef][PubMed]
    [Google Scholar]
  17. Detmers J., Strauss H., Schulte U., Bergmann A., Knittel K., Kuever J..( 2004;). FISH shows that Desulfotomaculum spp. are the dominating sulfate-reducing bacteria in a pristine aquifer. . Microb Ecol47:236–242. [CrossRef][PubMed]
    [Google Scholar]
  18. Eichler B., Pfennig N..( 1986;). Characterization of a new platelet-forming purple sulfur bacterium, Amoebobacter pedioformis sp. nov. . Arch Microbiol146:295–300. [CrossRef]
    [Google Scholar]
  19. Giese R., Henninges J., Lüth S., Morozova D., Schmidt-Hattenberger C., Würdemann H., Zimmer M., Cosma C., Juhlin C..( 2009;). Monitoring at the CO2 SINK site: a concept integrating geophysics, geochemistry and microbiology. . Energy Procedia1:2251–2259. [CrossRef]
    [Google Scholar]
  20. Gruber A. R., Lorenz R., Bernhart S. H., Neuböck R., Hofacker I. L..( 2008;). The Vienna RNA websuite. . Nucleic Acids Res36:W70–W74. [CrossRef][PubMed]
    [Google Scholar]
  21. Hagenauer A., Hippe H., Rainey F. A..( 1997;). Desulfotomaculum aeronauticum sp. nov., a sporeforming, thiosulfate-reducing bacterium from corroded aluminium alloy in an aircraft. . Syst Appl Microbiol20:65–71. [CrossRef]
    [Google Scholar]
  22. Haouari O., Fardeau M. L., Cayol J. L., Casiot C., Elbaz-Poulichet F., Hamdi M., Joseph M., Ollivier B..( 2008;). Desulfotomaculum hydrothermale sp. nov., a thermophilic sulfate-reducing bacterium isolated from a terrestrial Tunisian hot spring. . Int J Syst Evol Microbiol58:2529–2535. [CrossRef][PubMed]
    [Google Scholar]
  23. Hofacker I. L., Fontana W., Stadler P. F., Bonhoeffer L. S., Tacker M., Schuster P..( 1994;). Fast folding and comparison of RNA secondary structures. . Monatsh Chem125:167–188. [CrossRef]
    [Google Scholar]
  24. Hubert C., Loy A., Nickel M., Arnosti C., Baranyi C., Brüchert V., Ferdelman T., Finster K., Christensen F. M. et al.( 2009;). A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. . Science325:1541–1544. [CrossRef][PubMed]
    [Google Scholar]
  25. Hubert C., Arnosti C., Brüchert V., Loy A., Vandieken V., Jørgensen B. B..( 2010;). Thermophilic anaerobes in Arctic marine sediments induced to mineralize complex organic matter at high temperature. . Environ Microbiol12:1089–1104. [CrossRef][PubMed]
    [Google Scholar]
  26. Hungate R. E..( 1969;). A roll-tube method for the cultivation of strict anaerobes. . Methods Microbiol3:117–132.[CrossRef]
    [Google Scholar]
  27. Imachi H., Sekiguchi Y., Kamagata Y., Loy A., Qiu Y. L., Hugenholtz P., Kimura N., Wagner M., Ohashi A., Harada H..( 2006;). Non-sulfate-reducing, syntrophic bacteria affiliated with desulfotomaculum cluster I are widely distributed in methanogenic environments. . Appl Environ Microbiol72:2080–2091. [CrossRef][PubMed]
    [Google Scholar]
  28. Jukes T. H., Cantor C. R..( 1969;). Evolution of protein molecules. . In Mammalian Prot Metabolism,vol. 3 , pp. 21–132. Edited by Munro H. N.. New York, NY:: Academic Press;.[CrossRef]
    [Google Scholar]
  29. Junier P., Frutschi M., Wigginton N. S., Schofield E. J., Bargar J. R., Bernier-Latmani R..( 2009;). Metal reduction by spores of Desulfotomaculum reducens. . Environ Microbiol11:3007–3017. [CrossRef][PubMed]
    [Google Scholar]
  30. Kaksonen A. H., Spring S., Schumann P., Kroppenstedt R. M., Puhakka J. A..( 2006;). Desulfotomaculum thermosubterraneum sp. nov., a thermophilic sulfate-reducer isolated from an underground mine located in a geothermally active area. . Int J Syst Evol Microbiol56:2603–2608. [CrossRef][PubMed]
    [Google Scholar]
  31. Kaur A., Chaudhary A., Choudhary R., Kaushik R..( 2005;). Phospholipid fatty acid–a bioindicator of environment monitoring and assessment in soil ecosystem. . Curr Sci89:1103–1112.
    [Google Scholar]
  32. Kuykendall L. D., Roy M. A., O’Neill J. J., Devine T. E..( 1988;). Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. . Int J Syst Bacteriol38:358–361. [CrossRef]
    [Google Scholar]
  33. Lane D. J..( 1991;). 16S/23S rRNA sequencing. . In Nucleic Acid Techniques in Bacterial Systematics , pp. 115–175. Edited by Stackebrandt E., Goodfellow M.. New York:: Wiley;.
    [Google Scholar]
  34. Liu Y., Karnauchow T. M., Jarrell K. F., Balkwill D. L., Drake G. R., Ringelberg D., Clarno R., Boone D. R..( 1997;). Description of two new thermophilic Desulfotomaculum spp., Desulfotomaculum putei sp. nov., from a deep terrestrial subsurface, and Desulfotomaculum luciae sp. nov., from a hot spring. . Int J Syst Bacteriol47:615–621.[CrossRef]
    [Google Scholar]
  35. López-López A., Benlloch S., Bonfá M., Rodríguez-Valera F., Mira A..( 2007;). Intragenomic 16S rDNA divergence in Haloarcula marismortui is an adaptation to different temperatures. . J Mol Evol65:687–696. [CrossRef][PubMed]
    [Google Scholar]
  36. Mesbah M., Premachandran U., Whitman W. B..( 1989;). Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. . Int J Syst Bacteriol39:159–167. [CrossRef]
    [Google Scholar]
  37. Miller L. T..( 1982;). Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. . J Clin Microbiol16:584–586.[PubMed]
    [Google Scholar]
  38. Morasch B., Schink B., Tebbe C. C., Meckenstock R. U..( 2004;). Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum. . Arch Microbiol181:407–417. [CrossRef][PubMed]
    [Google Scholar]
  39. Morgenstern B..( 2004;). DIALIGN: multiple DNA and protein sequence alignment at BiBiServ. . Nucleic Acids Res32:W33–W36. [CrossRef][PubMed]
    [Google Scholar]
  40. Nazina T. N., Rozanova E. P..( 1978;). Thermophilic sulfate-reducing bacteria from oil strata. . Microbiology47:113–118.
    [Google Scholar]
  41. Newman D. K., Kennedy E. K., Coates J. D., Ahmann D., Ellis D. J., Lovley D. R., Morel F. M..( 1997;). Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. . Arch Microbiol168:380–388. [CrossRef][PubMed]
    [Google Scholar]
  42. O'Sullivan L. A., Roussel E. G., Weightman A. J., Webster G., Hubert C. R., Bell E., Head I., Sass H., Parkes R. J..( 2015;). Survival of Desulfotomaculum spores from estuarine sediments after serial autoclaving and high-temperature exposure. . ISME J9:922–933. [CrossRef][PubMed]
    [Google Scholar]
  43. Ogg C. D., Patel B. K. C..( 2011;). Desulfotomaculum varum sp. nov., a moderately thermophilic sulfate-reducing bacterium isolated from a microbial mat colonizing a great Artesian basin bore well runoff channel. . Biotech1:139–149. [CrossRef]
    [Google Scholar]
  44. Otwell A. E., Sherwood R. W., Zhang S., Nelson O. D., Li Z., Lin H., Callister S. J., Richardson R. E..( 2015;). Identification of proteins capable of metal reduction from the proteome of the gram-positive bacterium Desulfotomaculum reducens MI-1 using an NADH-based activity assay. . Environ Microbiol17:1977–1990. [CrossRef][PubMed]
    [Google Scholar]
  45. Patel B. K. C., Love C. A., Stackebrandt E..( 1992;). Helix 6 of the 16S rRNA of the bacterium Desulfotomaculum australicum exhibits an unusual structural idiosyncrasy. . Nucleic Acid Res20:5483. [CrossRef][PubMed]
    [Google Scholar]
  46. Pfennig N., Widdel F., Trüper H..( 1981;). The dissmilatory sulfate-reducing bacteria. . In The Prokaryotes, pp. 926–940. Edited by Starr M. P., Stolp H., Trüpper H. G., Balows A., Schlegel H. G.. Berlin:: Springer Verlag;.[CrossRef]
    [Google Scholar]
  47. Postgate J..( 1959;). A diagnostic reaction of Desulphovibrio desulphuricans. . Nature183:481–482. [CrossRef][PubMed]
    [Google Scholar]
  48. Rainey F. A., Ward-Rainey N. L., Janssen P. H., Hippe H., Stackebrandt E..( 1996;). DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences. . Microbiology142:2087–2095. [CrossRef][PubMed]
    [Google Scholar]
  49. Ray A. E., Connon S. A., Sheridan P. P., Gilbreath J., Shields M., Newby D. T., Fujita Y., Magnuson T. S..( 2010;). Intragenomic heterogeneity of the 16S rRNA gene in strain UFO1 caused by a 100-bp insertion in helix 6. . FEMS Microbiol Ecol72:343–353. [CrossRef][PubMed]
    [Google Scholar]
  50. Saitou N., Nei M..( 1987;). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol4:406–425.
    [Google Scholar]
  51. Sasser M..( 1990;). Technical Note 101: Identification of Bacteria by Gas Chromatography of Cellular Fatty Acids. Newark:: MIDI;.
    [Google Scholar]
  52. Selesi D., Meckenstock R. U..( 2009;). Anaerobic degradation of the aromatic hydrocarbon biphenyl by a sulfate-reducing enrichment culture. . FEMS Microbiol Ecol68:86–93. [CrossRef][PubMed]
    [Google Scholar]
  53. Stackebrandt E., Sproer C., Rainey F. A., Burghardt J., Pauker O., Hippe H..( 1997;). Phylogenetic analysis of the genus Desulfotomaculum: evidence for the misclassification of Desulfotomaculum guttoideum and description of Desulfotomaculum orientis as Desulfosporosinus orientis gen. nov., comb. nov. . Int J Syst Evol Microbiol47:1134–1139. [CrossRef][PubMed]
    [Google Scholar]
  54. Takai K., Komatsu T., Horikoshi K..( 2001;). Hydrogenobacter subterraneus sp. nov., an extremely thermophilic, heterotrophic bacterium unable to grow on hydrogen gas, from deep subsurface geothermal water. . Int J Syst Evol Microbiol51:1425–1435. [CrossRef][PubMed]
    [Google Scholar]
  55. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S..( 2013;). mega6: molecular evolutionary genetics analysis version 6.0. . Mol Biol Evol30:2725–2729. [CrossRef][PubMed]
    [Google Scholar]
  56. Taubert M., Vogt C., Wubet T., Kleinsteuber S., Tarkka M. T., Harms H., Buscot F., Richnow H. H., von Bergen M., Seifert J..( 2012;). Protein-SIP enables time-resolved analysis of the carbon flux in a sulfate-reducing, benzene-degrading microbial consortium. . ISME J6:2291–2301. [CrossRef][PubMed]
    [Google Scholar]
  57. Tebo B. M., Obraztsova A. Y..( 1998;). Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. . FEMS Microbiol Lett162:193–198. [CrossRef]
    [Google Scholar]
  58. Tourova T. P., Kuznetzov B. B., Novikova E. V, Poltaraus A. B., Nazina T. N..( 2001;). Heterogeneity of the nucleotide sequences of the 16S rRNA genes of the type strain of Desulfotomaculum kuznetsovii. . Microbiology70:678–684.[CrossRef]
    [Google Scholar]
  59. Trimarco E., Balkwill D., Davidson M., Onstott T. C..( 2006;). In situ enrichment of a diverse community of bacteria from a 4–5 km deep fault zone in South Africa. . Geomicrobiol J23:463–473. [CrossRef]
    [Google Scholar]
  60. Villemur R., Constant P., Gauthier A., Shareck M., Beaudet R..( 2007;). Heterogeneity between 16S ribosomal RNA gene copies borne by one Desulfitobacterium strain is caused by different 100–200 bp insertions in the 5′ region. . Can J Microbiol53:116–128. [CrossRef][PubMed]
    [Google Scholar]
  61. Visser M., Frutschi M., Stams A. J. M., Bernier-Latmani R..( 2016;). Phylogenetic comparison of Desulfotomaculum species of subgroup 1a and description of Desulfotomaculum reducens sp. nov. . Int J Syst Evol Microbiol66:762–767. [CrossRef]
    [Google Scholar]
  62. Weisburg W. G., Barns S. M., Pelletier D. A., Lane D. J..( 1991;). 16S ribosomal DNA amplification for phylogenetic study. . J Bacteriol173:697–703.[PubMed][CrossRef]
    [Google Scholar]
  63. Widdel F., Pfennig N..( 1981;). Sporulation and further nutritional characteristics of Desulfotomaculum acetoxidans. . Arch Microbiol129:401–402. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.001352
Loading
/content/journal/ijsem/10.1099/ijsem.0.001352
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

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