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FISH Shows That Desulfotomaculum spp. Are the Dominating Sulfate-Reducing Bacteria in a Pristine Aquifer

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Abstract

The hydrochemistry and the microbial diversity of a pristine aquifer system near Garzweiler, Germany, were characterized. Hydrogeochemical and isotopic data indicate a recent activity of sulfate-reducing bacteria in the Tertiary marine sands. The community structure in the aquifer was studied by fluorescence in situ hybridization (FISH). Up to 7.3 × 105 cells/mL were detected by DAPI-staining. Bacteria (identified by the probe EUB338) were dominant, representing 51.9% of the total cell number (DAPI). Another 25.7% of total cell were affiliated with the domain Archaea as identified by the probe ARCH915. Within the domain Bacteria, the β-Proteobacteria were most abundant (21.0% of total cell counts). Using genus-specific probes for sulfate-reducing bacteria (SRB), 2.5% of the total cells were identified as members of the genus Desulfotomaculum. This reflects the predominant role these microorganisms have been found to play in sulfate-reducing zones of aquifers at other sites. Previously, all SRB cultured from this site were from the spore-forming genera Desulfotomaculum and Desulfosporosinus.

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References

  1. C Achtnich A Schuhmann T Wind R Conrad (1995) ArticleTitleRole of interspecies H2 transfer to sulfate and ferric iron-reducing bacteria in acetate consumption in anoxic paddy soil. FEMS Microbiol Ecol 16 61–70 Occurrence Handle10.1016/0168-6496(94)00070-D Occurrence Handle1:CAS:528:DyaK2MXjt1Smu70%3D

    Article  CAS  Google Scholar 

  2. R Amann F-O Glöckner A Neef (1997) ArticleTitleModern methods in subsurface microbiology: in situ identification of microorganisms with nucleic acid probes. FEMS Microbiol Rev 20 191–200 Occurrence Handle10.1016/S0168-6445(97)00007-7 Occurrence Handle1:CAS:528:DyaK2sXltl2msL0%3D

    Article  CAS  Google Scholar 

  3. R Amann W Ludwig K Schleifer (1995) ArticleTitlePhylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59 143–169 Occurrence Handle1:CAS:528:DyaK2MXkvVGmurk%3D Occurrence Handle7535888

    CAS  PubMed  Google Scholar 

  4. R Amann J Snaidr M Wagner W Ludwig K-H Schleifer (1996) ArticleTitleIn situ visualization of high genetic diversity in a natural bacterial community. J Bacteriol 178 3496–3500 Occurrence Handle1:CAS:528:DyaK28XjsFGls7Y%3D Occurrence Handle8655546

    CAS  PubMed  Google Scholar 

  5. RI Amann BJ Binder RJ Olson SW Chisholm R Devereux DA Stahl (1990) ArticleTitleCombination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56 1919–1925 Occurrence Handle1:CAS:528:DyaK3cXkvFCgsrs%3D Occurrence Handle2200342

    CAS  PubMed  Google Scholar 

  6. P Amy (1997) Microbial dormancy and survival in the subsurface. P Amy D Haldeman (Eds) The Microbiology of the Terrestrial Deep Subsurface Lewis Boca Raton, FL 185–203

    Google Scholar 

  7. D Balkwill R Reeves G Drake J Reeves F Crocker M King D Boone (1997) ArticleTitlePhylogenetic characterization of bacteria in the subsurface microbial culture collection. FEMS Microbiol Rev 20 201–216 Occurrence Handle10.1016/S0168-6445(97)00008-9 Occurrence Handle1:CAS:528:DyaK2sXltl2msbo%3D Occurrence Handle9299704

    Article  CAS  PubMed  Google Scholar 

  8. Bergmann, A (1999) Hydrogeochemische Untersuchungen anoxischer Redoxprozesse in tiefen Porengrundwasserleitern der Niederrheinischen Bucht im Umfeld des Tagebaus Ph.D. thesis. Garzweiler I, Ruhr-Universität, Bochum

  9. V Boivin-Jahns R Ruimy A Bianchi S Daumas R Christen (1996) ArticleTitleBacterial diversity in a deep-subsurface clay environment. Appl Environ Microbiol 62 3405–3412 Occurrence Handle1:CAS:528:DyaK28XlsFeqtr8%3D Occurrence Handle8795233

    CAS  PubMed  Google Scholar 

  10. S Burggraf T Mayer A Amann S Schadhauser C Woese K Stetter (1994) ArticleTitleIdentifying members of the domain Archaea with rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 60 3112–3119 Occurrence Handle1:CAS:528:DyaK2cXlslWmu7c%3D Occurrence Handle7524440

    CAS  PubMed  Google Scholar 

  11. D Chandler S Li C Spadoni G Drake D Balkwill J Fredrickson F Brockman (1997) ArticleTitleA molecular comparison of culturable aerobic heterotrophic bacteria and 16S rDNA clones derived from a deep subsurface sediment. FEMS Microbiol Ecol 23 131–144 Occurrence Handle10.1016/S0168-6496(97)00021-4 Occurrence Handle1:CAS:528:DyaK2sXkvFaksLc%3D

    Article  CAS  Google Scholar 

  12. F Colwell T Onstott M Delwiche D Chandler J Fredrickson Q Yao J McKinley D Boone R Griffiths T Phelps D Ringelberg D White L LaFreniere D Balkwill R Lehman J Konisky P Long (1997) ArticleTitleMicroorganisms from deep, high temperature sandstones: constraints on microbial colonization. FEMS Microbiol. Rev. 20 425–435 Occurrence Handle10.1016/S0168-6445(97)00024-7 Occurrence Handle1:CAS:528:DyaK2sXltl2msLs%3D

    Article  CAS  Google Scholar 

  13. B Crump V Virginia Armbrust J Baross (1999) ArticleTitlePhylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol 65 3192–3204 Occurrence Handle1:CAS:528:DyaK1MXktlemu78%3D Occurrence Handle10388721

    CAS  PubMed  Google Scholar 

  14. J Detmers U Schulte H Strauss J Kuever (2001) ArticleTitleSulfate reduction at a lignite seam: microbial abundance and activity. Microb Ecol 42 238–247 Occurrence Handle10.1007/s00248-001-1014-8 Occurrence Handle1:CAS:528:DC%2BD38XksFc%3D Occurrence Handle12024249

    Article  CAS  PubMed  Google Scholar 

  15. R Devereux MD Kane J Winfrey DA Stahl (1992) ArticleTitleGenus- and group-specific hybridization probes for determinative and environmental studies of sulfate-reducing bacteria. System Appl Microbiol 15 601–609 Occurrence Handle1:CAS:528:DyaK3sXksVGisL4%3D

    CAS  Google Scholar 

  16. DVWK (1992) “Entnahme und Untersuchungsumfang von Grundwasserproben. DVWK-Regeln zur Wasserwirtschaft.” DVWK, Hamburg, Berlin

  17. F Glöckner B Fuchs R Amann (1999) ArticleTitleBacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65 3721–3726 Occurrence Handle10427073

    PubMed  Google Scholar 

  18. FO Glöckner R Amann A Alfreider J Pernthaler R Psenner K Trebesius K-H Schleifer (1996) ArticleTitleAn in situ hybridization protocol for detection and identification of planktonic bacteria. Syst Appl Microbiol 19 403–406

    Google Scholar 

  19. K Hristova M Mau D Zheng R Aminov R Mackie H Gaskins L Raskin (2000) ArticleTitleDesulfotomaculum genus and sub-genus-specific 16S rRNA hybridization probes for environmental studies. Environ Microbiol 2 143–160 Occurrence Handle10.1046/j.1462-2920.2000.00085.x Occurrence Handle1:CAS:528:DC%2BD3cXjslSnsbw%3D Occurrence Handle11220301

    Article  CAS  PubMed  Google Scholar 

  20. P Hugenholtz C Pitulle KL Hershberger NR Pace (1998) ArticleTitleNovel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180 366–376 Occurrence Handle1:CAS:528:DyaK1cXlsVaqsA%3D%3D Occurrence Handle9440526

    CAS  PubMed  Google Scholar 

  21. K Ishi S Takii S Fukunaga K Aoki (2000) ArticleTitleCharacterization by denaturating gardient gel electrophoresis of bacterial communities in deep groundwater at the Kamaishi Mine, Japan. J Gen Appl Microbiol 46 85–93 Occurrence Handle12483595

    PubMed  Google Scholar 

  22. L Jimenez (1990) ArticleTitleMolecular analysis of deep-subsurface bacteria. Appl Environ Microbiol 56 2108–2113 Occurrence Handle1:CAS:528:DyaK3cXltFahtbo%3D Occurrence Handle2389933

    CAS  PubMed  Google Scholar 

  23. S Kotelnikova K Pedersen (1997) ArticleTitleEvidence for methanogenic archaea and homoacetogenic bacteria in deep granitic rock aquifers. FEMS Microbiol Rev 20 339–349 Occurrence Handle10.1016/S0168-6445(97)00016-8 Occurrence Handle1:CAS:528:DyaK2sXltl2ms7g%3D

    Article  CAS  Google Scholar 

  24. J Kuever F Rainey H Hippe (1999) ArticleTitleDescription of Desulfotomaculum sp. Groll as Desulfotomaculum gibsoniae, sp. nov. Int J Syst Bacteriol 49 1801–1808 Occurrence Handle1:CAS:528:DyaK1MXnsFGiur0%3D Occurrence Handle10555363

    CAS  PubMed  Google Scholar 

  25. W Liesack E Stackebrandt (1992) ArticleTitleOccurrence of novel groups of the domain Bacteria as revealed by analysis of genetic material isolated from an Australian terrestrial environment. J Bacteriol 174 5072–5078 Occurrence Handle1:CAS:528:DyaK38XlsVKqu7k%3D Occurrence Handle1629164

    CAS  PubMed  Google Scholar 

  26. E Madsen (2000) ArticleTitleNucleic-acid characterization of the identity and activity of subsurface microorganisms. Hydrogeol J 8 112–125 Occurrence Handle10.1007/s100400050012 Occurrence Handle1:CAS:528:DC%2BD38Xkt1GrtL8%3D

    Article  CAS  Google Scholar 

  27. W Manz R Amann W Ludwig M Vancanneyt K-H Schleifer (1996) ArticleTitleApplication of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum CytophagaFlavobacterBacteroides in the natural environment. Microbiology 142 1097–1106 Occurrence Handle1:CAS:528:DyaK28XjtFyju7c%3D Occurrence Handle8704951

    CAS  PubMed  Google Scholar 

  28. W Manz R Amann W Ludwig M Wagner K-H Schleifer (1992) ArticleTitlePhylogentic oligodeoxynucelotide probes for the major subclasses of proteobacteria: problems and solutions. Syst Appl Microbiol 15 593–600

    Google Scholar 

  29. W Manz M Eisenbrecher TR Neu U Szewzyk (1998) ArticleTitleAbundance and spatial organization of Gram-negative sulfate-reducing bacteria in activated sludge investigated by in situ probing with specific 16S rRNA targeted oligonucleotides. FEMS Microbiol Ecol 25 43–61 Occurrence Handle10.1016/S0168-6496(97)00082-2 Occurrence Handle1:CAS:528:DyaK1cXislymtA%3D%3D

    Article  CAS  Google Scholar 

  30. D Martino E Grossman G Ulrich K Burger J Schlichenmeyer J Suflita J Ammerman (1998) ArticleTitleMicrobial abundance and activity in a low-conductivity aquifer system in East-Central Texas. Microb Ecol 35 224–234 Occurrence Handle10.1007/s002489900078 Occurrence Handle1:CAS:528:DyaK1cXivFCntbs%3D Occurrence Handle9569280

    Article  CAS  PubMed  Google Scholar 

  31. H Meier R Amann W Ludwig K-H Schleifer (1999) ArticleTitleSpecific oligonucleotide probes for in situ detection of a major group of Gram-positive bacteria with low DNA G+C content. Syst Appl Microbiol 22 186–196 Occurrence Handle1:CAS:528:DyaK1MXks1Smtbs%3D Occurrence Handle10390869

    CAS  PubMed  Google Scholar 

  32. Neef, A (1997) Anwendung der in situ-Einzelzell-Identifizierung von Bakterien zur Populations-Analyse in komplexen mikrobiellen Biozönosen. Ph.D. thesis, Technische Universität München

  33. A Neef R Amann H Schlesner K-H Schleifer (1998) ArticleTitleMonitoring a widespread bacterial group: In situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology 144 3257–3266 Occurrence Handle1:CAS:528:DyaK1MXisVOrtg%3D%3D Occurrence Handle9884217

    CAS  PubMed  Google Scholar 

  34. V Orphan L Taylor D Hafenbradl E Delong (2000) ArticleTitleCulture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66 700–711 Occurrence Handle10.1128/AEM.66.2.700-711.2000 Occurrence Handle1:CAS:528:DC%2BD3cXhtFeqs7w%3D Occurrence Handle10653739

    Article  CAS  PubMed  Google Scholar 

  35. K Pedersen (1997) ArticleTitleMicrobial life in deep granitic rock. FEMS Microbiol Rev 20 399–414 Occurrence Handle10.1016/S0168-6445(97)00022-3 Occurrence Handle1:CAS:528:DyaK2sXltl2msLw%3D

    Article  CAS  Google Scholar 

  36. K Pedersen J Arlinger S Ekendahl L Hallbeck (1996a) ArticleTitle16S rRNA gene diversity of attached and unattached bacteria in boreholes along the access tunnel to the Äspö hard rock laboratory, Sweden. FEMS Microbiol Ecol 19 249–262 Occurrence Handle10.1016/0168-6496(96)00017-7 Occurrence Handle1:CAS:528:DyaK28XjsVOktb8%3D

    Article  CAS  Google Scholar 

  37. K Pedersen J Arlinger L Hallbeck C Petterson (1996b) ArticleTitleDiversity and distribution of subterranean bacteria in groundwater at Oklo in Gabon, Africa, as determined by 16S rRNA gene sequencing. Mol Ecol 5 427–436 Occurrence Handle10.1046/j.1365-294X.1996.d01-320.x Occurrence Handle1:CAS:528:DyaK28Xktlynt78%3D

    Article  CAS  Google Scholar 

  38. K Ravenschlag K Sahm C Knoblauch BB Jørgensen R Amann (2000) ArticleTitleCommunity structure, cellular rRNA content and activity of sulfate-reducing bacteria in marine arctic sediments. Appl Environ Microbiol 66 3592–3602 Occurrence Handle10.1128/AEM.66.8.3592-3602.2000 Occurrence Handle1:CAS:528:DC%2BD3cXlsFarsbc%3D Occurrence Handle10919825

    Article  CAS  PubMed  Google Scholar 

  39. K Ravenschlag K Sahm J Pernthaler R Amann (1999) ArticleTitleHigh bacterial diversity in permanently cold marine sediments. Appl Environ Microbiol 65 3982–3989 Occurrence Handle1:CAS:528:DyaK1MXlvFeqtbs%3D Occurrence Handle10473405

    CAS  PubMed  Google Scholar 

  40. C Roller M Wagner R Amann W Ludwig K-H Schleifer (1994) ArticleTitleIn situ probing of gram-positive bacteria with high DNA G+C content using 23S rRNA-targeted oligonucleotides. Microbiology 140 2849–2858 Occurrence Handle1:CAS:528:DyaK2MXhslGlu7Y%3D Occurrence Handle8000548

    CAS  PubMed  Google Scholar 

  41. K Sahm B MacGregor BB Jørgensen D Stahl (1999) ArticleTitleSulphate reduction and vertical distribution of sulphate-reducing bacteria quantified by rRNA slot-blot hybridization in a coastal marine sediment. Environ Microbiol 1 65–74 Occurrence Handle10.1046/j.1462-2920.1999.00007.x Occurrence Handle1:CAS:528:DyaK1MXit1Wks7Y%3D Occurrence Handle11207719

    Article  CAS  PubMed  Google Scholar 

  42. Schulte, U (1998) Isotopengeochemische Untersuchungen zur Charakterisierung biologisch gesteuerter Redoxprozesse in Aquiferen der Niederrheinischen Bucht. Ph.D. thesis, Ruhr-Universität, Bochum

  43. U Schulte H Strauss A Bergmann P Obermann (1997) ArticleTitleIsotopenverhältnisse der Schwefel-und Kohlenstoffspezies aus Sedimenten und tiefen Grundwässern der Niederrheinischen Bucht. Grundwasser 3 103–110 Occurrence Handle10.1007/s767-1997-8531-4

    Article  Google Scholar 

  44. U Schulte H Strauss J Detmers J Kuever (1999) ArticleTitleCharacterization of an aquifer system—stable isotopes and microbiology. J Conf Abstr 4 578

    Google Scholar 

  45. J Snaidr R Amann I Huber W Ludwig K-H Schleifer (1997) ArticleTitlePhylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63 2884–2896 Occurrence Handle1:CAS:528:DyaK2sXktlekt7Y%3D Occurrence Handle9212435

    CAS  PubMed  Google Scholar 

  46. D Stahl R Amann (1991) Development and application of nucleic acid probes in bacterial systematics. ESaM Goodfellow (Eds) Nucleic Acid Techniques in Bacterial Systematics John Wiley & Sons Chichester, UK 205–248

    Google Scholar 

  47. O Strunk O Gross B Reichel M May S Hermann N Stuckmann M Nonhoff M Lenke A Ginhart A Vilbig T Ludwig A Bode K-H Schleifer W Ludwig (1999) ARB: a software environment for sequence data Department of Microbiology, Technische Universität München Munich, Germany

    Google Scholar 

  48. G Ulrich D Martino K Burger J Routh E Grossman J Ammerman J Suflita (1998) ArticleTitleSulfur cycling in the terrestrial subsurface: commensal interactions, spatial scales, and microbial heterogeneity. Microb Ecol 36 141–151 Occurrence Handle10.1007/s002489900101 Occurrence Handle1:CAS:528:DyaK1cXlsVOnurY%3D Occurrence Handle9688776

    Article  CAS  PubMed  Google Scholar 

  49. H Urukawa K Kita-Tsukamoto K Ohwada (1999) ArticleTitleMicrobial diversity in marine sediments from Sagami Bay and Tokyo Bay, Japan, as determined by 16S rRNA gene analysis. Microbiology 145 3305–3315 Occurrence Handle10589740

    PubMed  Google Scholar 

  50. G Wallner R Amann W Beisker (1993) ArticleTitleOptimizing fluorescent in situ hybridization with rRNA-targeted oligonucleotide probes for flow cytometric identification of microorganisms. Cytometry 14 136–143 Occurrence Handle1:CAS:528:DyaK3sXisVylsrs%3D Occurrence Handle7679962

    CAS  PubMed  Google Scholar 

  51. B Zarda G Mattison A Hess D Hahn P Höhener J Zeyer (1998) ArticleTitleAnalysis of bacterial and protozoan communities in an aquifer contaminated with monoaromatic hydrocarbons. FEMS Microbiol Ecol 27 141–152 Occurrence Handle10.1016/S0168-6496(98)00061-0 Occurrence Handle1:CAS:528:DyaK1cXmtl2ntr8%3D

    Article  CAS  Google Scholar 

  52. I Zlatkin M Schneider F de Bruijn L Forney (1996) ArticleTitleDiversity among bacteria isolated from the deep subsurface. J Industr Microbiol 17 219–227 Occurrence Handle1:CAS:528:DyaK2sXltF2hsQ%3D%3D

    CAS  Google Scholar 

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Acknowledgements

This paper represents a publication of the Priority Program 546, “Geochemical processes with long-term effects in anthropogenically-affected seepage- and groundwater.” Financial support provided by the Deutsche Forschungsgemeinschaft is gratefully acknowledged. Jan Detmers, Katrin Knittel, and Jan Kuever were supported by the Max-Planck-Society. R. Amann is acknowledged for critical reading of the manuscript.

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Detmers, J., Strauss, H., Schulte, U. et al. FISH Shows That Desulfotomaculum spp. Are the Dominating Sulfate-Reducing Bacteria in a Pristine Aquifer . Microb Ecol 47, 236–242 (2004). https://doi.org/10.1007/s00248-004-9952-6

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