Skip to main content

Advertisement

Log in

Review: Microbial biocenoses in pristine aquifers and an assessment of investigative methods

  • Report
  • Published:
Hydrogeology Journal Aims and scope Submit manuscript

Abstract

The current knowledge of microbial biocenoses (communities) in pristine aquifers is presented in a review, which also discusses their relevance for questions of groundwater protection. Aquifers are heterogeneous on all scales and structured in a variety of habitats. The void spaces in many aquifers are small. The biocenoses are thus predominantly composed of microorganisms and, often, microinvertebrates. Larger voids and macroorganisms occur in karst cavities. Due to the absence of light, the biocenoses depend on chemical energy resources, which are, however, scarce in non-contaminated groundwater. The microorganisms thus show small cell sizes, low population densities and reduced activity; they developed specific strategies to survive oligotrophic conditions. The review also discusses the impact of contamination on the biocenoses, and the potential use of the biocenoses or specific organisms as indicators for groundwater quality, and the limits of this approach. Bacteria are either planktonic or attached to aquifer material, which requires both fluid and solid phase sampling. Most groundwater bacteria are viable but non-culturable. Consequently, cultivation techniques give an incomplete picture of the biocenoses, while methods from molecular microbiology provide genetic fingerprints of the entire community. Different analytical methods are available to count microorganisms, identify species, characterise microbial diversity, and measure activity.

Résumé

Cette revue expose l’état actuel des connaissances concernant les biocénoses microbiennes présentes dans les aquifères oligotrophes. L’impact d’une contamination sur les biocénoses est discuté, ainsi que le potentiel que représentent les communautés ou un organisme spécifique, en tant qu’indicateur de qualité des eaux souterraines. En dernier lieu les méthodes à disposition en microbiologie sont examinées.

Les aquifères sont hétérogènes à de nombreuses échelles et sont structurés en une grande variété d’habitats. Les espaces vides sont très souvent de petite taille. De ce fait, les biocénoses sont composées de manière prédominante par des microorganismes et parfois quelques micro-invertébrés. Les espaces plus larges, notamment les cavités karstiques, sont peuplés de macro-organismes également.

En l’absence de toute forme d’énergie lumineuse, les biocénoses dépendent de sources d’énergie chimiques, présentes en faible quantité dans les aquifères non contaminés. Les microorganismes développent ainsi de petites tailles, une densité de population faible et une activité réduite. La physiologie des organismes est adaptée à la survie en conditions oligotrophes.

Les bactéries sont planctoniques ou attachées aux matériaux de l’aquifère, ce qui demande un échantillonnage à la fois de l’eau et du substrat. De nombreuses méthodes sont aujourd’hui disponibles pour le comptage, l’identifi-cation et la caractérisation de la diversité, ainsi que la mesure des activités des organismes des aquifères. Comme la grande majorité des bactéries est viable mais non cultivable, les techniques de cultures actuelles ne donnent qu’une image incomplète des communautés, alors que les méthodes moléculaires développées récemment offrent la possibilité d’obtenir un profil de la communauté plus complet.

Resumen

Se presenta una reseña crítica del conocimiento actual de biocenosis microbiana (comunidades) en acuíferos prístinos la cual también discute su relevancia en términos de protección de aguas subterráneas. Los acuíferos son heterogéneos en todas las escalas y estructurados en una variedad de habitats. Los espacios vacíos en muchos acuíferos son pequeños. La biocenosis está por lo tanto compuesta predominantemente por microorganismos y, frecuentemente, microinvertebrados. Espacios más grandes y macroorganismos ocurren en cavidades kársticas. Debido a la ausencia de luz la biocenosis depende de recursos energéticos químicos los cuales, sin embargo, son escasos en agua subterránea no contaminada. Los microorganismos muestran entonces tamaños de células pequeñas, bajas densidades de población y actividad reducida por lo que desarrollan estrategias específicas para sobrevivir en condiciones oligotróficas. Esta reseña crítica también discute el impacto de la contaminación en la biocenosis y el uso potencial de la biocenosis o de organismos específicos como indicadores de la calidad del agua subterránea, así como los límites de este enfoque. Las bacterias se encuentran ya sea en forma planctónica o ligadas al material acuífero lo cual requiere muestreo de la fase sólida y la fase fluida. La mayoría de bacterias de agua subterránea son viables pero no cultivables. Por lo tanto, las técnicas de cultivo aportan un cuadro incompleto de la biocenosis mientras que los métodos de microbiología molecular aportan señales genéticas de toda la comunidad. Existen diferentes métodos analíticos para contar microorganismos, identificar especies, caracterizar diversidad microbiana, y medir actividad.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ackermann H-W, DuBow MS (1987) Viruses of prokaryotes: General properties of bacteriophages, 1. CRC Press, Boca Raton, Florida, 202 pp

    Google Scholar 

  • Ahn IS, Lee CH (2003) Kinetic studies of attachment and detachment of microbial cells from soil. Environ Technol 24(4):411–418

    PubMed  Google Scholar 

  • Albrechtsen HJ (1994) Distribution of bacteria, estimated by a viable count method, and heterotrophic activity in different size fractions of aquifer sediment. Geomicrobiol J 12(4):253–264

    Google Scholar 

  • Alfreider A, Krossbacher M, Psenner R (1997) Groundwater samples do not reflect bacterial densities and activity in subsurface systems. Water Res 31(4):832–840

    Article  Google Scholar 

  • Amann R, Fuchs BM, Behrens S (2001) The identification of micro-organisms by fluorescence in situ hybridisation. Curr Opin Biotechnol 12(3):231–236

    Article  PubMed  Google Scholar 

  • Amann R, Kühl M (1998) In situ methods for assessment of micro-organisms and their activities. Curr Opin Microbiol 1(3):352–358

    Article  PubMed  Google Scholar 

  • Anderson RT, Lovley DR (1997) Ecology and biogeochemistry of in situ groundwater bioremediation. Adv Microbial Ecol 15:289–350

    Google Scholar 

  • Auckenthaler A, Huggenberger P (ed) (2003) Pathogene Mikroorganismen im Grund- und Trinkwasser [pathogenic microorganisms in groundwater and drinking water]. Birkhäuser Verlag, Basel, 184 pp

  • Auckenthaler A, Raso G, Huggenberger P (2002) Particle transport in a karst aquifer: natural and artificial tracer experiments with bacteria, bacteriophages and microspheres. Water Sci Technol 46(3):131–138

    Google Scholar 

  • Baker MA, Valett HM, Dahm CN (2000) Organic carbon supply and metabolism in a shallow groundwater ecosystem. Ecology 81(11):3133–3148

    Google Scholar 

  • Balkwill DL, Ghiorse WC (1985) Characterization of subsurface bacteria associated with two shallow aquifers in Oklahoma. Appl Environ Microbiol 50(3):580–588

    PubMed  Google Scholar 

  • Balkwill DL, Murphy EM, Fair DM, Ringelberg DB, White DC (1998) Microbial communities in high and low recharge environments: implications for microbial transport in the vadose zone. Microbial Ecol 35(2):156–171

    Article  Google Scholar 

  • Bast E (2001) Mikrobiologische Methoden [microbiological methods]. Spektrum Akademischer Verlag, Heidelberg, 429 pp

    Google Scholar 

  • Batiot C, Emblanch C, Blavoux B (2003) Total organic carbon (TOC) and magnesium (Mg): two complementary tracers of residence time in karstic systems. Comptes Rendus Geosci 335(2):205–214

    Article  Google Scholar 

  • Baur WH (2003) Gewässergüte bestimmen und beurteilen [determination and evaluation of water quality]. VFG, 209 pp

  • Beloin RM, Sinclair JL, Ghiorse WC (1988) Distribution and activity of micro-organisms in subsurface sediments of a pristine study site in Oklahoma. Microbial Ecol 16(1):85–97

    Article  Google Scholar 

  • Bloom Y, Aravena R, Hunkeler D, Edwards E, Frape SK (2000) Carbon isotope fractionation during microbial dechlorination of trichloroethene, cis-1,2-dichloroethene, and vinyl chloride: implications for assessment of natural attenuation. Environ Sci Technol 34(13):2768–2772

    Article  Google Scholar 

  • Boissier JM, Marmonier P, Claret C, Fontvieille D, Blanc P (1996) Comparison of solutes, nutrients and bacteria inputs from two types of groundwater to the Rhone River during an artificial drought. Hydrobiologia 319(1):65–72

    Article  Google Scholar 

  • Bone TL, Balkwill DL (1988) Morphological and cultural comparison of micro-organisms in surface soil and subsurface sediments at a pristine study site in Oklahoma. Microbial Ecol 16:49–64

    Article  Google Scholar 

  • Boon N, De Windt W, Verstraete W, Top EM (2002) Evaluation of nested PCR-DGGE (denaturing gradient gel electrophoresis) with group-specific 16S rRNA primers for the analysis of bacterial communities from different wastewater treatment plants. FEMS Microbiol Ecol 39(2):101–112

    Google Scholar 

  • Boulton AJ, Findlay S, Marmonier P, Stanley EH, Valett HM (1998) The functional significance of the hyporheic zone in streams and rivers. Ann Rev Ecol Syst 29:59–81

    Article  Google Scholar 

  • Brockman FJ, Li SW, Fredrickson JK, Ringelberg DB, Kieft TL, Spadoni CM, White DC, McKinley JP (1998) Post-sampling changes in microbial community composition and activity in a subsurface paleosol. Microbial Ecol 36(2):152–164

    Article  Google Scholar 

  • Brockman FJ, Murray CJ (1997) Subsurface microbiological heterogeneity: Current knowledge, descriptive approaches and applications. FEMS Microbiol Rev 20(3/4):231–247

    Google Scholar 

  • Brooks T, Osicki RA, Springthorpe VS, Satter SA, Filion L, Abrial D, Riffard S (2004) Detection and infection of Legionella species from groundwaters. J Toxicol Environ Health A 67:1845–1859

    Article  PubMed  Google Scholar 

  • Bruggemann J, Stephen JR, Chang YJ, Macnaughton SJ, Kowalchuk GA, Kline E, White DC (2000) Competitive PCR-DGGE analysis of bacterial mixtures: an internal standard and an appraisal of template enumeration accuracy. J Microbiol Methods 40(2):111–123

    Article  PubMed  Google Scholar 

  • Brunke M, Gonser T (1997) The ecological significance of exchange processes between rivers and groundwater [Review]. Freshwater Biol 37(1):1–33

    Article  Google Scholar 

  • Bruns A, Cypionka H, Overmann J (2002) Cyclic AMP and Acyl Homoserine Lactones Increase the Cultivation Efficiency of Heterotrophic Bacteria from the Central Baltic Sea. Appl Environ Microbiol 68(8):3978–3987

    Article  PubMed  Google Scholar 

  • Byrd JJ, Xu HS, Colwell RR (1991) Viable but nonculturable bacteria in drinking-water. Appl Environ Microbiol 57(3):875–878

    PubMed  Google Scholar 

  • Capuano RM, Siringan MA, Jan RZ, Jurtshuk P (1995) Enhanced activity of oligotrophic endogenous bacteria in clay-rich sediments by nutrient injection. Geomicrobiol J 13(3):165–179

    Google Scholar 

  • Casamayor EO, Pedros-Alio C, Muyzer G, Amann R (2002) Microheterogeneity in 16S ribosomal DNA-defined bacterial populations from a stratified planktonic environment is related to temporal changes and to ecological adaptations. Appl Environ Microbiol 68(4):1706–1714

    Article  PubMed  Google Scholar 

  • Cassidy MB, Leung KT, Lee H, Trevors JT (2000) A comparison of enumeration methods for culturable Pseudomonas fluorescens cells marked with green fluorescent protein. J Microbiol Methods 40(2):135–145

    Article  PubMed  Google Scholar 

  • Chandler DP, Brockman FJ, Fredrickson JK (1997) Use of 16S rDNA clone libraries to study changes in a microbial community resulting from ex situ perturbation of a subsurface sediment. FEMS Microbiol Rev 20(3/4):217–230

    Google Scholar 

  • Chapelle FH (2001) Ground-water microbiology and geochemistry. Wiley , New York, 477 pp

    Google Scholar 

  • Cho JC, Kim SJ (1999) Viable, but non-culturable, state of a green fluorescence protein-tagged environmental isolate of Salmonella typhi in groundwater and pond water. FEMS Microbiol Lett 170(1):257–264

    PubMed  Google Scholar 

  • Cho JC, Kim SJ (2000) Increase in bacterial community diversity in subsurface aquifers receiving livestock wastewater input. Appl Environ Microbiol 66(3):956–965

    Article  PubMed  Google Scholar 

  • Church PE, Granato GE (1996) Bias in ground-water data caused by well-bore flow in long-screen wells. Ground Water 34(2):262–273

    Article  Google Scholar 

  • Colwell FS, Stormberg GJ, Phelps TJ, Birnbaum SA, McKinley J, Rawson SA, Veverka C, Goodwin S, Long PE, Russell BF, Garland T, Thompson D, Skinner P, Grover S (1992) Innovative techniques for collection of saturated and unsaturated subsurface basalts and sediments for microbiological characterization. J Microbiol Methods 15(4):279–292

    Article  Google Scholar 

  • Covich AP, Austen MC, Barlocher F, Chauvet E, Cardinale BJ, Biles CL, Inchausti P, Dangles O, Solan M, Gessner MO, Statzner B, Moss B (2004) The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54(8):767–775

    Google Scholar 

  • Craun GF, Nwachuku N, Calderon RL, Craun MF (2002) Outbreaks in drinking-water systems, 1991–1998. J Environ Health 65(1):16–23

    Google Scholar 

  • Culver DC, Christman MC, Sket B, Trontelj P (2004) Sampling adequacy in an extreme environment: species richness patterns in Slovenian caves. Biodivers Conserv 13(6):1209–1229

    Article  Google Scholar 

  • Damgaard LR, Revsbech NP (1997) A microscale biosensor for methane containing methanotrophic bacteria and an internal oxygen reservoir. Anal Chem 69(13):2262–2267

    Article  Google Scholar 

  • Damgaard LR, Revsbech NP, Reichardt W (1998) Use of an oxygen-insensitive microscale biosensor for methane to measure methane concentration profiles in a rice paddy. Appl Environ Microbiol 64(3):864–870

    PubMed  Google Scholar 

  • Danielopol DL, Griebler C, Gunatilaka A, Notenboom J (2003) Present state and future prospects for groundwater ecosystems. Environ Conserv 30(2):104–130

    Article  Google Scholar 

  • Danielopol DL, Pospisil P (2001) Hidden biodiversity in the groundwater of the Danube Flood Plain National Park (Austria). Biodivers Conserv 10(10):1711–1721

    Article  Google Scholar 

  • de Beer D, Glud A, Epping E, Kühl M (1997) A fast-responding CO2 microelectrode for profiling sediments, microbial mats, and biofilms. Limnol Oceanogr 42(7):1590–1600

    Google Scholar 

  • de Lipthay JR, Johnsen K, Albrechtsen HJ, Rosenberg P, Aamand J (2004) Bacterial density and community structure of a sub-surface aquifer exposed to realistic low herbicide concentrations. FEMS Microbiol Ecol 49:59–69

    Article  Google Scholar 

  • DeBorde DC, Woessner WW, Lauerman B, Ball PN (1998) Virus occurrence and transport in a school septic system and unconfined aquifer. Ground Water 36(5):825–834

    Article  Google Scholar 

  • DeLeo PC, Baveye P (1997) Factors affecting protozoan predation of bacteria clogging laboratory aquifer microcosms. Geomicrobiol J 14(2):127–149

    Google Scholar 

  • Dewettinck T, Hulsbosch W, Van Hege K, Top EM, Verstraete W (2001) Molecular fingerprinting of bacterial populations in groundwater and bottled mineral water. Appl Microbiol Biotechnol 57(3):412–418

    Article  PubMed  Google Scholar 

  • Doig F, Lollar BS, Ferris FG (1995) Microbial communities in deep Canadian Shield groundwaters—an in-situ biofilm experiment. Geomicrobiol J 13(2):91–102

    Google Scholar 

  • Dollhopf SL, Hashsham SA, Tiedje JM (2001) Interpreting 16S rDNA T-RFLP Data: Application of self-organizing maps and principal component analysis to describe community dynamics and convergence. Microbial Ecol 42:495–505

    Article  Google Scholar 

  • Drever JI (ed) (1997) The geochemistry of natural waters—surface and groundwater environments. Prentice Hall, Upper Saddle River, NJ, 436 pp

    Google Scholar 

  • Dröge M, Pühler A, Selbitschka W (1999) Horizontal gene transfer among bacteria in terrestrial and aquatic habitats as assessed by microcosm and field studies. Biol Fertil Soils 29:221–245

    Article  Google Scholar 

  • Dumas P, Bou C, Gibert J (2001) Groundwater macrocrustaceans as natural indicators of the Ariege alluvial aquifer. Int Rev Hydrobiol 86(6):619–633

    Article  Google Scholar 

  • Dumont MG, Murrell JC (2005) Stable isotope probing linking microbial identity to function. Nat Rev Microbiol 3(6):499–504

    Article  PubMed  Google Scholar 

  • EC (2000) Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy

  • Edberg SC, LeClerc H, Robertson J (1997) Natural protection of spring and well drinking water against surface microbial contamination: II. Indicators and monitoring parameters for parasites. Crit Rev Microbiol 23(2):179–206

    PubMed  Google Scholar 

  • Ekendahl S, Arlinger J, Stahl F, Pedersen K (1994) Characterization of attached bacterial-populations in deep granitic groundwater from the stripa research mine by 16s ribosomal-RNA gene sequencing and scanning electron-microscopy. Microbiol UK 140:1575–1583

    Google Scholar 

  • Farnleitner AH, Wilhartitz I, Ryzinska G, Kirschner AKT, Stadler H, Burtscher MM, Hornek R, Szewzyk U, Herndl G, Mach RL (2005) Bacterial dynamics in spring water of alpine karst aquifers indicates the presence of stable autochthonous microbial endokarst communities. Environ Microbiol 7(8):1248–1259

    Article  PubMed  Google Scholar 

  • Fernandez A, Huang SY, Seston S, Xing J, Hickey R, Criddle C, Tiedje J (1999) How stable is stable? Function versus community composition. Appl Environ Microbiol 65(8):3697–3704

    PubMed  Google Scholar 

  • Flanigan D, Rodgers M (2003) A method to detect viable Helicobacter pylori bacteria in groundwater. Acta Hydrochim Et Hydrobiol 31(1):45–48

    Article  Google Scholar 

  • Flynn R (2003) Virus transport and attenuation in perialpine gravel aquifers. PhD Thesis, University of Neuchâtel, Switzerland, 178 pp

  • Franklin RB, Taylor DR, Mills AL (2000) The distribution of microbial communities in anaerobic and aerobic zones of a shallow coastal plain aquifer. Microbial Ecol 38(4):377–386

    Article  Google Scholar 

  • Fredrickson JK, Li SW, Brockman FJ, Haldeman DL, Amy PS, Balkwill DL (1995) Time-dependent changes in viable numbers and activities of aerobic heterotrophic bacteria in subsurface samples. J Microbiol Methods 21(3):253–265

    Article  Google Scholar 

  • Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4(11):634–643

    PubMed  Google Scholar 

  • Gabrovsek F, Menne B, Dreybrodt W (2000) A model of early evolution of karst conduits affected by subterranean CO2 sources. Environ Geol 39(6):531–543

    Article  Google Scholar 

  • Galassi DMP (2001) Groundwater copepods: diversity patterns over ecological and evolutionary scales. Hydrobiologia 453(1–3):227–253

    Article  Google Scholar 

  • Gavrieli I, Burg A, Guttman J (2002) Transition from confined to phreatic conditions as the factor controlling salinization and change in redox state, Upper subaquifer of the Judea Group, Israel. Hydrogeol J 10(4):483–494

    Article  Google Scholar 

  • Gayraud S, Herouin E, Philippe M (2002) The clogging of stream beds: A review of mechanisms and consequences on habitats and macroinvertebrate communities. Bulletin francais de la peche et de la pisciculture (365/366):339–355

    Google Scholar 

  • Ghiorse WC, Miller DN, Sandoli RL, Siering PL (1996) Applications of laser scanning microscopy for analysis of aquatic microhabitats. Microsc Res Tech 33(1):73–86

    Article  PubMed  Google Scholar 

  • Gillham RW, Starr RC, Millar D (1990) A device for in situ determination of geochemical transport parameters, 2. Biochemical reactions. Ground Water 28(6):858–862

    Article  Google Scholar 

  • Gobat JM, Aragno M, Matthey W (2004) The Living Soil. Fundamentals of Soil Science and Soil Biology. Science Publishers, 602 pp

  • Golas I, Filipkowska Z, Lewandowska D, Zmyslowska I (2002) Potentially pathogenic bacteria from the family Enterobacteriaceae, Pseudomonas sp. and Aeromonas sp. in waters designated for drinking and household purposes. Pol J Environ Stud 11(4):325–330

    Google Scholar 

  • Griebler C, Mindl B, Slezak D, Geiger-Kaiser M (2002) Distribution patterns of attached and suspended bacteria in pristine and contaminated shallow aquifers studied with an in situ sediment exposure microcosm. Aquat Microbial Ecol 28(2):117–129

    Google Scholar 

  • Griebler C, Mösslacher F (2003) Grundwasser-Ökologie [ground-water ecology]. Facultas UTB, Vienna, 495 pp

    Google Scholar 

  • GSchV (1998) Water Protection Ordinance, SR 814.201, Swiss Federal Law, Bern

  • Haack SK, Bekins B (2000) Microbial populations in contaminant plumes. Hydrogeol J 8:63–76

    Article  Google Scholar 

  • Hahn HJ, Friedrich E (1999) Brauchen wir ein faunistisch begründetes Grundwassermonitoring und was kann es leisten? [Do we need a fauna-based groundwater monitoring, and what is its potential?] Grundwasser 4:147–154

    Article  Google Scholar 

  • Hakenkamp CC, Palmer MA, James BR (1994) Metazoans from a sandy aquifer - dynamics across a physically and chemically heterogeneous groundwater system. Hydrobiologia 287(2):195–206

    Google Scholar 

  • Haldeman DL, Amy PS, White DC, Ringelberg DB (1994) Changes in bacteria recoverable from subsurface volcanic rock samples during storage at 4°C. Appl Environ Microbiol 60(8):2697–2703

    PubMed  Google Scholar 

  • Hancock PJ, Boulton AJ, Humphreys WF (2005) Aquifers and hyporheic zones: Towards an ecological understanding of groundwater. Hydrogeol J 13(1):98–111

    Article  Google Scholar 

  • Harvey RW, Smith RL, George L (1984) Effect of organic contamination upon microbial distributions and heterotrophic uptake in a Cape Cod, Mass., Aquifer. Appl Environ Microbiol 48(6):1197–1202

    PubMed  Google Scholar 

  • Haveman SA, Pedersen K (2002) Distribution of culturable micro-organisms in Fennoscandian Shield groundwater. FEMS Microbiol Ecol 39(2):129–137

    Google Scholar 

  • Hazen TC, Jimenez L, Devictoria GL, Fliermans CB (1991) Comparison of bacteria from deep subsurface sediment and adjacent groundwater. Microbial Ecol 22(3):293–304

    Google Scholar 

  • Herwaldt BL, Craun GF, Stokes SL, Juranek DD (1992) Outbreaks of waterborne disease in the United-States - 1989–90. J Am Water Works Assoc 84(4):129–135

    Google Scholar 

  • Hohener P, Hunkeler D, Hess A, Bregnard T, Zeyer J (1998) Methodology for the evaluation of engineered in situ bioremediation: lessons from a case study. J Microbiol Methods 32(2):179–192

    Article  Google Scholar 

  • Hollibaugh JT (1994) Relationship between thymidine metabolism, bacterioplankton community metabolic capabilities, and sources of organic-matter. Microbial Ecol 28(2):117–131

    Article  Google Scholar 

  • Holliger C, Gaspard S, Glod G, Heijman C, Schumacher W, Schwarzenbach R, Vazquez F (1995) Contaminated environments in the subsurface and bioremediation: organic contaminants. Curr Opin Biotechnol 6(3):347–351

    Article  Google Scholar 

  • Holm PE, Nielsen PH, Albrechtsen HJ, Christensen TH (1992) Importance of unattached bacteria and attached bacteria to sediment in determining potentials for degradation of xenobiotic organic contaminants in an aerobic aquifer. Appl Environ Microbiol 58:3020–3026

    PubMed  Google Scholar 

  • Hunkeler D, Anderson N, Aravena R, Bernasconi SM, Butler BJ (2001) Hydrogen and carbon isotope fractionation during aerobic biodegradation of benzene. Environ Sci Technol 35(17):3462–3467

    Article  PubMed  Google Scholar 

  • Hunkeler D, Aravena R, Parker BL, Cherry JA, Diao X (2003) Monitoring oxidation of chlorinated ethenes by permanganate in groundwater using stable isotopes: Laboratory and field studies. Environ Sci Technol 37(4):798–804

    Article  PubMed  Google Scholar 

  • Hunkeler D, Goldscheider N, Rossi P, Burn C (2006) Biozönosen im Grundwasser - Grundlagen und Methoden der Charakterisierung von mikrobiellen Gemeinschaften [Biocenoses in groundwater - basics and methods to characterise microbial communities]. Umwelt-Wissen, Swiss Federal Office for the Environment (FOEN), Berne

  • Hunkeler D, Hohener P, Bernasconi S, Zeyer J (1999) Engineered in situ bioremediation of a petroleum hydrocarbon-contaminated aquifer: assessment of mineralization based on alkalinity, inorganic carbon and stable carbon isotope balances. J Contam Hydrol 37(3/4):201–223

    Article  Google Scholar 

  • Hurst CJ, Crawford RL, Knudsen GR, McInerney MJ, Stetzenbach LD (2002) Manual of environmental microbiology, 2nd edn. ASM Press, 1158 pp

  • Istok JD, Humphrey MD, Schroth MH, Hyman MR, Oreilly KT (1997) Single-well, “push-pull” test for in situ determination of microbial activities. Ground Water 35(4):619–631

    Article  Google Scholar 

  • Jean JS, Tsai CL, Ju SH, Tsao CW, Wang SM (2002) Biodegradation and transport of benzene, toluene, and xylenes in a simulated aquifer: comparison of modelled and experimental results. Hydrol Process 16(16):3151–3168

    Article  Google Scholar 

  • Kell DB, Kaprelyants AS, Weichart DH, Harwood CR, Barer MR (1998) Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 73(2):169–187

    Article  Google Scholar 

  • Kent AD, Triplett EW (2002) Microbial communities and their interactions in soil and rhizosphere ecosystems. Annu Rev Microbiol 56:211–236

    Article  PubMed  Google Scholar 

  • Kirchman D, Knees E, Hodson R (1985) Leucine incorporation and its potential as a measure of protein-synthesis by bacteria in natural aquatic systems. Appl Environ Microbiol 49(3):599–607

    PubMed  Google Scholar 

  • Klimant I, Holst G, Kühl M (1997) A simple fiberoptic sensor to detect the penetration of microsensors into sediments and other biogeochemical systems. Limnol Oceanogr 42(7):1638–1643

    Google Scholar 

  • Konopka A, Turco R (1991) Biodegradation of organic-compounds in vadose zone and aquifer sediments. Appl Environ Microbiol 57(8):2260–2268

    PubMed  Google Scholar 

  • Kota S, Borden RC, Barlaz MA (1999) Influence of protozoan grazing on contaminant biodegradation. FEMS Microbiol Ecol 29(2):179–189

    Google Scholar 

  • Krumholz LR, McKinley JP, Ulrich FA, Suflita JM (1997) Confined subsurface microbial communities in Cretaceous rock. Nature 386(6620):64–66

    Article  Google Scholar 

  • Lawrence JG (2002) Gene transfer in bacteria: speciation without species? Theor Popul Biol 61(4):449–460

    Article  PubMed  Google Scholar 

  • Lebaron P, Servais P, Baudoux AC, Bourrain M, Courties C, Parthuisot N (2002) Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aquat Microbial Ecol 28(2):131–140

    Google Scholar 

  • Lee N, Nielsen PH, Andreasen KH, Juretschko S, Nielsen JL, Schleifer KH, Wagner M (1999) Combination of fluorescent in situ hybridization and microautoradiography–-a new tool for structure-function analyses in microbial ecology. Appl Environ Microbiol 65(3):1289–1297

    PubMed  Google Scholar 

  • Lehloesa LJ, Muyima NYO (2000) Evaluation of the impact of household treatment procedures on the quality of groundwater supplies in the rural community of the Victoria district, Eastern Cape. Water SA 26(2):285–290

    Google Scholar 

  • Lehman RM (2001) Attached and unattached microbial communities in a simulated basalt aquifer under fracture- and porous-flow conditions. Appl Environ Microbiol 67(6)

  • Lehman RM, Roberto FF, Earley D, Bruhn DF, Brink SE, O’Connell SP, Delwiche ME, Colwell FS (2001) Attached and unattached bacterial communities in a 120-meter corehole in an acidic, crystalline rock aquifer. Appl Environ Microbiol 67(5):2095–2106

    Article  PubMed  Google Scholar 

  • Lerner DN, Teutsch G (1995) Recommendations for level-determined sampling in wells. J Hydrol 171(3/4):355–377

    Article  Google Scholar 

  • Li BL, Loehle C, Malon D (1996) Microbial transport through heterogeneous porous media: random walk, fractal, and percolation approaches. Ecol Model 85(2/3):285–302

    Article  Google Scholar 

  • Lillis TO, Bissonnette GK (2001) Detection and characterization of filterable heterotrophic bacteria from rural groundwater supplies. Lett Appl Microbiol 32(4):268–272

    Article  PubMed  Google Scholar 

  • Lisle JT, Rose JB (1995) Cryptosporidium contamination of water in the USA and UK—a minireview. J Water Supply: Res Technol - AQUA 44(3):103–117

    Google Scholar 

  • Loaiciga HA, Charbeneau RJ, Everett LG, Fogg GE, Hobbs BF, Rouhani S (1992) Review of groundwater quality monitoring network design. J Hydraulic Eng - Asce 118(1):11–37

    Google Scholar 

  • Madigan MT, Martinko JM, Parker J (2000) Brock - biology of micro-organisms, 9th edn. Prentice-Hall, New York, 991 pp

  • Mahler BJ, Personne JC, Lods GF, Drogue C (2000) Transport of free and particulate-associated bacteria in karst. J Hydrol 238(3/4):179–193

    Article  Google Scholar 

  • Maier RM, Pepper IL, Gerba CP (2000) Environmental microbiology. Academic: 585 pp

  • Malard F, Gibert J, Laurent R, Reygrobellet JL (1994) A new method for sampling the fauna of deep karstic aquifers. C R Acad Sci 317(10):955–966

    Google Scholar 

  • Malard F, Hervant F (1999) Oxygen supply and the adaptations of animals in groundwater. Freshwater Biol 41(1):1–30

    Article  Google Scholar 

  • Malard F, Mathieu J, Reygrobellet JL, Lafont M (1996a) Biomotoring groundwater contamination: application to a karst area in Southern France. Aquat Sci 58(2):158–187

    Article  Google Scholar 

  • Malard F, Plenet S, Gibert J (1996b) The use of invertebrates in ground water monitoring: a rising research field. Ground Water Monit Remediation 16(2):103–113

    Google Scholar 

  • Malard F, Tockner K, Dole-Olivier MJ, Ward JV (2002) A landscape perspective of surface-subsurface hydrological exchanges in river corridors. Freshwater Biol 47(4):621–640

    Article  Google Scholar 

  • Marmonier P, Vervier P, Gibert J, Doleolivier MJ (1993) Biodiversity in ground waters. Trends Ecol Evol 8(11):392–395

    Article  Google Scholar 

  • Martin K (2002) Ökologie der Biozönosen [ecology of biocenoses]. Springer-Lehrbuch

  • Marxsen J (1988) Investigations into the number of respiring bacteria in groundwater from sandy and gravelly deposits. Microbial Ecol 16(1):65–72

    Article  Google Scholar 

  • Marxsen J (1996) Measurement of bacterial production in stream-bed sediments via leucine incorporation. FEMS Microbiol Ecol 21(4):313–325

    Google Scholar 

  • Mathieu J, Essafichergui K, Culver DC (1992) Variations in the structure of stygobiont crustacean populations (Niphargus-Rhenorhodanensis and Proasellus Valdensis) within the sediments of a karst outflow. Hydrobiologia 231(1):41–49

    Article  Google Scholar 

  • Mauclaire L, Pelz O, Thullner M, Abraham WR, Zeyer J (2003) Assimilation of toluene carbon along a bacteria-protist food chain determined by C-13-enrichment of biomarker fatty acids. J Microbiol Methods 55(3):635–649

    Article  PubMed  Google Scholar 

  • McMahon PB, Chapelle FH (1991) Geochemistry of dissolved inorganic carbon in a coastal plain aquifer. 2. Modeling carbon sources, sinks, and δ13C evolution. J Hydrol 127:109–135

    Article  Google Scholar 

  • Moeseneder MM, Arrieta JM, Muyzer G, Winter C, Herndl GJ (1999) Optimization of terminal-restriction fragment length polymorphism analysis for complex marine bacterioplankton communities and comparison with denaturing gradient gel electrophoresis. Appl Environ Microbiol 65(8):3518–3525

    PubMed  Google Scholar 

  • Murphy EM, Ginn TR, Chilakapati A, Resch CT, Phillips JL, Wietsma TW, Spadoni CM (1997) The influence of physical heterogeneity on microbial degradation and distribution in porous media. Water Resour Res 33(5):1087–1103

    Article  Google Scholar 

  • Muyzer G (1999) DGGE/TGGE a method for identifying genes from natural ecosystems. Curr Opin Microbiol 2(3):317–322

    Article  PubMed  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 73(1):127–141

    Article  Google Scholar 

  • Nasser AM, Tchorch Y, Fattal B (1993) Comparative survival of Escherichia coli, F+bacteriophages, HAV and poliovirus-1 in waste-water and groundwater. Water Sci Technol 27(3/4):401–407

    Google Scholar 

  • Nebbache S, Loquet M, Vinceslas-Akpa M, Feeny V (1997) Turbidity and micro-organisms in a karst spring. Eur J Soil Biol 33(2):89–103

    Google Scholar 

  • Neff JC, Asner GP (2001) Dissolved organic carbon in terrestrial ecosystems: synthesis and a model. Ecosystems 4(1):29–48

    Article  Google Scholar 

  • Nielsen JL, Nielsen PH (2002) Quantification of functional groups in activated sludge by microautoradiography. Water Sci Technol 46(1–2):389–395

    Google Scholar 

  • Niemi RM, Niemi JS (1991) Bacterial pollution of waters in pristine and agricultural lands. J Environ Qual 20(3):620–627

    Article  Google Scholar 

  • Northup DE, Lavoie KH (2001) Geomicrobiology of caves: a review. Geomicrobiol J 18(3):199–222

    Article  Google Scholar 

  • Olson GJ, Dockins WS, McFeters GA, Iverson WP (1981) Sulfate-reducing and methanogenic bacteria from deep aquifers in Montana. Geomicrobiol J 2(4):327–340

    Google Scholar 

  • Overmann J (2003) Principles of enrichment, isolation, cultivation, and preservation of prokaryotes, Release 3.12. In: Dworkin M (ed) The Prokaryotes: an evolving electronic resource for the microbiological community, http://141.150.157.117:8080/ prokPUB/index.htm (cited September 2005), Springer, Berlin Heidelberg New York

  • Pabich WJ, Valiela I, Hemond HF (2001) Relationship between DOC concentration and vadose zone thickness and depth below water table in groundwater of Cape Cod, USA. Biogeochemistry 55(3):247–268

    Article  Google Scholar 

  • Pedersen K, Arlinger J, Ekendahl S, Hallbeck L (1996) 16S rRNA gene diversity of attached and unattached bacteria in boreholes along the access tunnel to the Aspo hard rock laboratory, Sweden. FEMS Microbiol Ecol 19(4):249–262

    Google Scholar 

  • Pickup RW, Rhodes G, Alamillo ML, Mallinson HEH, Thornton SF, Lerner DN (2001) Microbiological analysis of multi-level borehole samples from a contaminated groundwater system. J Contam Hydrol 53(3/4):269–284

    Article  PubMed  Google Scholar 

  • Pipan T, Brancelj A (2004) Distribution patterns of copepods (Crustacea: Copepoda) in percolation water of the Postojnska Jama Cave system (Slovenia). Zool Stud 43(2):206–210

    Google Scholar 

  • Plenet S, Gibert J (1995) Comparison of surface-water groundwater interface zones in fluvial and karstic systems. Comptes Rendus De L Academie Des Sciences Serie Iii-Sciences De La Vie-Life Sciences 318(4):499–509

    Google Scholar 

  • Plenet S, Hugueny H, Gibert J (1996) Invertebrate community responses to physical and chemical factors at the river aquifer interaction zone. 2. Downstream from the city of Lyon. Archiv für Hydrobiologie 136(1):65–88

    Google Scholar 

  • Pombo SA, Pelz O, Schroth MH, Zeyer J (2002) Field-scale C-13-labeling of phospholipid fatty acids (PLFA) and dissolved inorganic carbon: tracing acetate assimilation and mineralization in a petroleum hydrocarbon-contaminated aquifer. FEMS Microbiol Ecol 41(3):259–267

    Google Scholar 

  • Preuss G, Schminke HK (2004) A global ecosystem–-groundwater is alive! Chemie in unserer Zeit 38(5):340–347

    Article  Google Scholar 

  • Pronk M, Goldscheider N, Zopfi J (in press) Dynamics and interaction of organic carbon, turbidity and bacteria in a karst aquifer system. Hydrogeol J, published online. DOI: 10.1007/s10040-005-0454-5

  • Puhakka JA, Jarvinen KT, Langwaldt JH, Melin ES, Mannisto MK, Salminen JM, Sjolund MT (2000) On-site and in situ bioremediation of wood-preservative contaminated groundwater. Water Sci Technol 42(5/6):371–376

    Google Scholar 

  • Rapp MC, Fulda C, Schafer W, Kinzelbach W (1998) The Dual Pumping Technique (DPT) for level-determined sampling in fully screened groundwater wells. J Hydrol 207(3/4):220–235

    Article  Google Scholar 

  • Richardson JS, Kiffney PM (2000) Responses of a macroinvertebrate community from a pristine, southern British Columbia, Canada, stream to metals in experimental mesocosms. Environ Toxicol Chem 19(3):736–743

    Article  Google Scholar 

  • Rogers JR, Bennett PC (2004) Mineral stimulation of subsurface micro-organisms: release of limiting nutrients from silicates. Chem Geol 203(1/2):91–108

    Article  Google Scholar 

  • Röling WFM, van Verseveld HW (2002) Natural attenuation: What does the subsurface have in store? Biodegradation 13(1):53–64

    Article  PubMed  Google Scholar 

  • Ross N, Villemur R, Marcandella E, Deschenes L (2001) Assessment of changes in biodiversity when a community of ultramicrobacteria isolated from groundwater is stimulated to form a biofilm. Microbial Ecol 42(1):56–68

    Google Scholar 

  • Rosselló-Mora R, Amann R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  Google Scholar 

  • Rossi P, Dorfliger N, Kennedy K, Muller I, Aragno M (1998) Bacteriophages as surface and ground water tracers. Hydrol Earth Syst Sci 2(1):101–110

    Article  Google Scholar 

  • Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51(3):365–379

    PubMed  Google Scholar 

  • Rouch R, Danielopol DL (1997) Species richness of microcrustacea in subterranean freshwater habitats. Comparative analysis and approximate evaluation. Internationale Revue der gesamten Hydrobiologie 82(2):121–145

    Google Scholar 

  • Ruiz-Aguilar GML, Fernandez-Sanchez JM, Kane SR, Kim D, Alvarez PJJ (2002) Effect of ethanol and methyl-tert-butyl ether on monoaromatic hydrocarbon biodegradation: Response variability for different aquifer materials under various electron-accepting conditions. Environ Toxicol Chem 21(12):2631–2639

    Article  PubMed  Google Scholar 

  • Russell CE, Jacobson R, Haldeman DL, Amy PS (1994) Heterogeneity of deep subsurface micro-organisms and correlations to hydrogeological and geochemical parameters. Geomicrobiol J 12(1):37–51

    Google Scholar 

  • Rusterholtz KJ, Mallory LM (1994) Density, activity, and diversity of bacteria indigenous to a karstic aquifer. Microbial Ecol 28(1):79–99

    Article  Google Scholar 

  • Ryan M, Meiman J (1996) An examination of short-term variations in water quality at a karst spring in Kentucky. Ground Water 34(1):23–30

    Article  Google Scholar 

  • Santegoeds CM, Damgaard LR, Hesselink C, Zopfi J, Lens P, Muyzer G, De Beer D (1999) Distribution of sulfate-reducing and methanogenic bacteria in anaerobic aggregates determined by microsensor and molecular analyses. Appl Environ Microbiol 65(10):4618–4629

    PubMed  Google Scholar 

  • Santegoeds CM, Muyzer G, de Beer D (1998) Biofilm dynamics studied with microsensors and molecular techniques. Water Sci Technol 37(4/5):125–129

    Article  Google Scholar 

  • Schaffter N, Parriaux A (2002) Pathogenic-bacterial water contamination in mountainous catchments. Water Res 36(1):131–139

    Article  PubMed  Google Scholar 

  • Schaffter N, Zumstein J, Parriaux A (2004): Factors influencing the bacteriological water quality in mountainous surface and groundwaters. Acta Hydrochim Hydrobiol 32:225–234

    Article  Google Scholar 

  • Schlegel HG (1993) General Microbiology, 7th ed. Cambridge University Press, 673 pp

  • Schmitter-Soto JJ, Comin FA, Escobar-Briones E, Herrera-Silveira J, Alcocer J, Suarez-Morales E, Elias-Gutierrez M, Diaz-Arce V, Marin LE, Steinich B (2002) Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula (SE Mexico). Hydrobiologia 467(1–3):215–228

    Article  Google Scholar 

  • Schubert R (1991) Lehrbuch der Ökologie [Introduction to ecology]. Spektrum Akademischer Verlag: 657 pp

  • Schulze-Makuch D, Kennedy JF (2000) Microbiological and chemical characterization of hydrothermal fluids at Tortugas Mountain Geothermal Area, southern New Mexico, USA. Hydrogeol J 8(3):295–309

    Article  Google Scholar 

  • Sekar R, Fuchs BM, Amann R, Pernthaler J (2004) Flow sorting of marine bacterioplankton after fluorescence in situ hybridization. Appl Environ Microbiol 70(10):6210–6219

    Article  PubMed  Google Scholar 

  • Severson KJ, Johnstone DL, Keller CK, Wood BD (1991) Hydrogeologic parameters affecting vadose-zone microbial distributions. Geomicrobiol J 9(4):197–216

    Google Scholar 

  • Sievert SM, Brinkhoff T, Muyzer G, Ziebis V, Kuever J (1999) Spatial heterogeneity of bacterial populations along an environmental gradient at a shallow submarine hydrothermal vent near Milos Island (Greece). Appl Environ Microbiol 65(9):3834–3842

    PubMed  Google Scholar 

  • Sinclair JL, Alexander M (1989) Effect of protozoan predation on relative abundance of fast- growing and slow-growing bacteria. Can J Microbiol 35(5):578–582

    Article  Google Scholar 

  • Sinclair JL, Randtke SJ, Denne JE, Hathaway LR, Ghiorse WC (1990) Survey of microbial-populations in buried-valley aquifer sediments from Northeastern Kansas. Ground Water 28(3):369–377

    Article  Google Scholar 

  • Sket B (1999) High biodiversity in hypogean waters and its endangerment - the situation in Slovenia, the Dinaric Karst, and Europe. Crustaceana 72:767–779

    Article  Google Scholar 

  • Smets BF, Siciliano SD, Verstraete W (2002) Natural attenuation: extant microbial activity forever and ever? Environ Microbiol 4(6):315–317

    Article  PubMed  Google Scholar 

  • Smith H, Wood PJ (2002) Flow permanence and macroinvertebrate community variability in limestone spring systems. Hydrobiologia 487(1):45–58

    Article  Google Scholar 

  • Swiger RR, Tucker JD (1996) Fluorescence in situ hybridization: A brief review. Environ Mol Mutagen 27: 245–254

    Google Scholar 

  • Szewzyk U, Szewzyk R, Manz W, Schleifer KH (2000) Microbiological safety of drinking water. Annu Rev Microbiol 54:81–127

    Article  PubMed  Google Scholar 

  • Thomas JM, Ward CH (1992) Subsurface microbial ecology and bioremediation. J Hazard Mater 32(2/3):179–194

    Article  Google Scholar 

  • Ultee A, Souvatzi N, Maniadi K, König H (2004) Identification of the culturable and nonculturable bacterial population in ground water of a municipal water supply in Germany. J Appl Microbiol 96:560–568

    Article  PubMed  Google Scholar 

  • Vachee A, Vincent P, Struijk CB, Mossel DAA, Leclerc H (1997) A study of the fate of the autochtonous bacterial flora of still mineral waters by analysis of restriction fragment length polymorphism of genes coding for rRNA. Syst Appl Microbiol 20(3):492–503

    Google Scholar 

  • Ventullo RM, Ladd TI, Costerton JW (1983) Distribution and activity of particle-bound and free-living suspended bacteria in groundwater. Abstracts of Papers of the American Chemical Society, 186(AUG): 105-ENVR

  • Vervier P, Gibert J (1991) Dynamics of surface-water groundwater ecotones in a karstic aquifer. Freshwater Biol 26(2):241–250

    Google Scholar 

  • Vervier P, Gibert J, Marmonier P, Doleolivier MJ (1992) A perspective on the permeability of the surface fresh-water-groundwater ecotone. J N Am Benthological Soc 11(1):93–102

    Google Scholar 

  • Vives-Rego J, Lebaron P, Nebe-von Caron G (2000) Current and future applications of flow cytometry in aquatic microbiology. FEMS Microbiol Rev 24(4):429–448

    PubMed  Google Scholar 

  • Wackett LP (2004) Stable isotope probing in biodegradation research. Trends Biotechnol 22(4):153–154

    Article  PubMed  Google Scholar 

  • Wagner M, Horn M, Daims H (2003) Fluorescence in situ hybridisation for the identification and characterisation of prokaryotes. Curr Opin Microbiol 6(3):302–309

    Article  PubMed  Google Scholar 

  • Ward JV, Palmer MA (1994) Distribution patterns of interstitial fresh-water meiofauna over a range of spatial scales, with emphasis on alluvial river aquifer systems. Hydrobiologia 287(1):147–156

    Article  Google Scholar 

  • Williams DD (1993) Changes in fresh-water meiofauna communities along the groundwater-hyporheic water ecotone. Trans Am Microsc Soc 112(3):181–194

    Google Scholar 

  • Wilson MS, Bakermans C, Madsen EL (1999) In situ, real-time catabolic gene expression: Extraction and characterization of naphthalene dioxygenase mRNA transcripts from groundwater. Appl Environ Microbiol 65(1):80–87

    PubMed  Google Scholar 

  • Winding A (1994) Fingerprinting bacterial soil communities using Biolog microtitre plates. In: Ritz K, Dighton J, Giller KE (eds), Beyond the biomass. Wiley, New York, pp 85–94

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51(2):221–271

    PubMed  Google Scholar 

  • Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95(16):9710–9710

    Google Scholar 

  • Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97(15):8392–8396

    Article  PubMed  Google Scholar 

  • Wood PJ, Gunn J, Perkins J (2002) The impact of pollution on aquatic invertebrates within a subterranean ecosystem—out of sight out of mind. Archiv für Hydrobiologie 155(2):223–237

    Google Scholar 

  • Zhang CL, Palumbo AV, Phelps TJ, Beauchamp JJ, Brockman FJ, Murray CJ, Parsons BS, Swift DJP (1998) Grain size and depth constraints on microbial variability in coastal plain subsurface sediments. Geomicrobiol J 15(3):171–185

    Article  Google Scholar 

  • Zhou JZ, Xia BC, Treves DS, Wu LY, Marsh TL, O'Neill RV, Palumbo AV, Tiedje JM (2002) Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol 68(1):326–334

    Article  PubMed  Google Scholar 

Download references

Acknowledgement

The Swiss Federal Office for the Environment (FOEN) funded this study. We thank Dr. Ronald Kozel and Dr. Benjamin Meylan for the good cooperation. We are particularly grateful to Dr. Jakob Zopfi (Neuchâtel) for numerous valuable suggestions and fruitful discussions. We acknowledge Christine Burn's contribution to the literature search. We also thank Dr. Franziska Zibuschka (Vienna) and Dr. Patrick Höhener (Lausanne) for useful comments. We thank Dr. Sascha Oswald (Associate Editor), Dr. Ralph David and an anonymous reviewer for their valuable comments and suggestions, and Dr. David Drew (Dublin) for the language check.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nico Goldscheider.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goldscheider, N., Hunkeler, D. & Rossi, P. Review: Microbial biocenoses in pristine aquifers and an assessment of investigative methods. Hydrogeol J 14, 926–941 (2006). https://doi.org/10.1007/s10040-005-0009-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10040-005-0009-9

Keywords

Navigation