Skip to main content
Log in

Impact of Clay Minerals on Sulfate-Reducing Activity in Aquifers

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Previous studies have shown that sulfate-reduction activity occurs in a heterogeneous manner throughout the terrestrial subsurface. Low-activity regions are often observed in the presence of clay minerals. Here we report that clays inhibit sulfate reduction activity in sediments and in a pure culture of Desulfovibrio vulgaris. Clay minerals including bentonite and kaolinite inhibited sulfate reduction by 70–90% in sediments. Intact clays and clay colloids or soluble components, capable of passing through a 0.2-µm filter, were also inhibitory to sulfate-reducing bacteria. Other adsorbent materials, including anion or cation exchangers and a zeolite, did not inhibit sulfate reduction in sediments, suggesting that the effect of clays was not due to their cation-exchange capacity. We observed a strong correlation between the Al2O3 content of clays and their relative ability to inhibit sulfate reduction in sediments (r 2 = 0.82). This suggested that inhibition might be a direct effect of Al3+ (aq) on the bacteria. We then tested pure aluminum oxide (Al2O3) and showed it to act in a similar manner to clay. As dissolved aluminum is known to be toxic to a variety of organisms at low concentrations, our results suggest that the effects of clay on sulfate-reducing bacteria may be directly due to aluminum. Thus, our experiments provide an explanation for the lack of sulfate-reduction activity in clay-rich regions and presents a mechanism for the effect.

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.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. H-J Albrechtsen (1994) ArticleTitleDistribution of bacteria, estimated by a viable count method, and heterotrophic activity in different size fractions of aquifer sediment. Geomicrobiol J 12 253–264

    Google Scholar 

  2. H-J Albrechtsen A Winding (1992) ArticleTitleMicrobial biomass and activity in subsurface sediments from Vejen, Denmark. Microb Ecol 23 303–317

    Google Scholar 

  3. JE Amonette CK Russell KA Carosino NL Robinson JT Ho (2003) ArticleTitleToxicity of Al to Desulfovibrio desulfuricans. Appl Environ Microbiol . .

    Google Scholar 

  4. RE Beeman JM Suflita (1987) ArticleTitleMicrobial ecology of a shallow unconfined ground water aquifer polluted by municipal landfill leachate. Microb Ecol 14 39–54

    Google Scholar 

  5. 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 

  6. J Cama J Ganor AC Lasaga (1994) ArticleTitleThe kinetics of smectite dissolution. Mineral Mag 58A 140–141

    Google Scholar 

  7. FH Chapelle DR Lovley (1990) ArticleTitleRates of microbial metabolism in deep coastal plain aquifers. Appl Environ Microbiol 56 1865–1874 Occurrence Handle1:CAS:528:DyaK3cXktlOlsrw%3D

    CAS  Google Scholar 

  8. FH Chapelle PB McMahon (1991) ArticleTitleGeochemistry of dissolved inorganic carbon in a Coastal Plain aquifer. 1. Sulfate from confining beds as an oxidant in microbial CO2 production. J Hydrol 127 85–108 Occurrence Handle10.1016/0022-1694(91)90110-4 Occurrence Handle1:CAS:528:DyaK38Xms1Ghsw%3D%3D

    Article  CAS  Google Scholar 

  9. PA Costanzo S Guggenheim (2001) ArticleTitleClays and Clay Minerals: Clay Minerals Society Source Clays. Clay Minerals Society, Aurora, CO . 371–452

    Google Scholar 

  10. DA Elias D Wong LR Krumholz JM Suflita (2003) ArticleTitleCharacterization of microbial activities and uranium reduction in a shallow aquifer contaminated by an UMTRA disposal cell. Microb Ecol 46 83–91 Occurrence Handle1:CAS:528:DC%2BD3sXnt1Git74%3D Occurrence Handle12754659

    CAS  PubMed  Google Scholar 

  11. SE Flis AR Glenn MJ Dilworth (1993) ArticleTitleThe interaction between aluminum and root nodule bacteria. Soil Biol Biochem 25 403–417 Occurrence Handle10.1016/0038-0717(93)90066-K Occurrence Handle1:CAS:528:DyaK3sXkslWmtr0%3D

    Article  CAS  Google Scholar 

  12. JK Fredrickson JP McKinley BN Bjornstad P Long DB Ringelberg DC White LR Krumholz JM Suflita FS Colwell RM Lehman TJ Phelps (1997) ArticleTitlePore-size constraints on the activity and survival of subsurface bacteria in a late Cretaceous shale-sandstone sequence, Northwestern New Mexico. Geomicrobiol J 14 183–202

    Google Scholar 

  13. L Guida Z Saidi MN Hughes RK Poole (1991) ArticleTitleAluminum toxicity and binding to Escherichia coli. Arch Microbiol 56 507–512

    Google Scholar 

  14. A Guzzo C Diorio MS Dubow (1991) ArticleTitleTranscription of Escherichia coli fliC gene is regulated by metal ions. Appl Environ Microbiol 57 2255–2259 Occurrence Handle1:CAS:528:DyaK3MXlslKhsrw%3D Occurrence Handle1768097

    CAS  PubMed  Google Scholar 

  15. J Guzzo A Guzzo MS DuBow (1992) ArticleTitleCharacterization of the effects of aluminum on luciferase biosensors for the detection of ecotoxicity. Toxicol Lett 64/65 687–693 Occurrence Handle10.1016/0378-4274(92)90248-I

    Article  Google Scholar 

  16. BC Hard C Walther W Babel (1999) ArticleTitleSorption of aluminum by sulfate-reducing bacteria isolated from uranium mine tailings. Geomicrobiol J 16 267–275 Occurrence Handle10.1080/014904599270532 Occurrence Handle1:CAS:528:DC%2BD3cXkt1an

    Article  CAS  Google Scholar 

  17. P Illmer F Schinner (1999) ArticleTitleInfluence of nutrient solution on Al-tolerance of Pseudomonas sp. FEMS Microbiol Lett 170 187–190 Occurrence Handle10.1016/S0378-1097(98)00549-7 Occurrence Handle1:CAS:528:DyaK1cXotFWitrk%3D

    Article  CAS  Google Scholar 

  18. AC Johnson M Wood (1990) ArticleTitleDNA as a possible site of action of aluminum in Rhizobium spp. Appl Environ Microbiol 56 3629–3633 Occurrence Handle1:CAS:528:DyaK3MXlslWntA%3D%3D

    CAS  Google Scholar 

  19. RE Jones RE Beeman JM Suflita (1989) ArticleTitleAnaerobic metabolic processes in the deep terrestrial subsurface. Geomicrobiol J 7 117–130 Occurrence Handle1:CAS:528:DyaK3cXotlGluw%3D%3D

    CAS  Google Scholar 

  20. K Kapoor L Arora (1998) ArticleTitleAluminum induced toxicity and growth responses of Cyanobacteria. Pollut Res 17 25–31 Occurrence Handle1:CAS:528:DyaK1cXivFWltrY%3D

    CAS  Google Scholar 

  21. JE Kostka JW Stucki KH Nealson J Wu (1996) ArticleTitleReduction of structural Fe(III) in smectite by a pure culture of Shewanella putrefaciens strain MR-1. Clays Clay Miner 44 522–529

    Google Scholar 

  22. LR Krumholz JP McKinley GA Ulrich JM Suflita (1997) ArticleTitleConfined subsurface microbial communities in Cretaceous rock. Nature 386 64–66 Occurrence Handle1:CAS:528:DyaK2sXhslCnsL0%3D

    CAS  Google Scholar 

  23. HJ Laanbroek HJ Geerligs (1983) ArticleTitleInfluence of clay particles (illite) on substrate utilization by sulfate-reducing bacteria. Arch Microbiol 134 161–163 Occurrence Handle1:CAS:528:DyaL3sXktVart74%3D

    CAS  Google Scholar 

  24. B Mason LG Berry (1968) Elements of Mineralogy. WH Freeman San Francisco

    Google Scholar 

  25. HM May DG Kinniburgh PA Helmke ML Jackson (1986) ArticleTitleAqueous dissolution, solubilities and thermodynamic stabilities of common aluminosilicate clay minerals: Kaolinite and smectites. Geochim Cosmochim Acta 50 1667–1677 Occurrence Handle10.1016/0016-7037(86)90129-8 Occurrence Handle1:CAS:528:DyaL28XltFygsrk%3D

    Article  CAS  Google Scholar 

  26. PB McMahon FH Chapelle (1991) ArticleTitleRole of microbial processes in linking sandstone diagenesis with organic rich clays. J Sed Petrol 62 1–10

    Google Scholar 

  27. PB McMahon FH Chapelle (1991) ArticleTitleMicrobial organic acid production in aquitard sediments and its role in aquifer geochemistry. Nature 349 233–235 Occurrence Handle10.1038/349233a0 Occurrence Handle1:CAS:528:DyaK3MXovVWltQ%3D%3D

    Article  CAS  Google Scholar 

  28. M Motamedi O Karland K Pedersen (1996) ArticleTitleSurvival of sulfate reducing bacteria at different water activities in compacted bentonite. FEMS Microbiol Lett 141 83–87 Occurrence Handle10.1016/0378-1097(96)00213-3 Occurrence Handle1:CAS:528:DyaK28XktVOlsLc%3D

    Article  CAS  Google Scholar 

  29. EH Oelkers J Schott JL Devidal (1994) ArticleTitleThe effect of aluminum, pH, and chemical affinity on the rates of aluminosilicate dissolution reactions. Geochim Cosmochim Acta 58 2011–2024 Occurrence Handle10.1016/0016-7037(94)90281-X Occurrence Handle1:CAS:528:DyaK2cXktFChsrY%3D

    Article  CAS  Google Scholar 

  30. K Pedersen M Motamedi O Karnland T Sandén (2000) ArticleTitleMixing and sulphate-reducing activity of bacteria in swelling compacted bentonite clay under high-level radioactive waste repository conditions. J Appl Microbiol 89 1038–1047 Occurrence Handle10.1046/j.1365-2672.2000.01212.x Occurrence Handle1:CAS:528:DC%2BD3MXot1SmsQ%3D%3D Occurrence Handle11123477

    Article  CAS  PubMed  Google Scholar 

  31. K Pedersen M Motamedi O Karnland T Sandén (2000) ArticleTitleCultivability of microorganisms introduced into a compacted bentonite clay buffer under high-level radioactive waste repository conditions. Eng Geol 58 149–161 Occurrence Handle10.1016/S0013-7952(00)00056-9

    Article  Google Scholar 

  32. RG Pina C Cervantes (1996) ArticleTitleMicrobial interactions with aluminum. Biometals 9 311–316 Occurrence Handle1:STN:280:BymB1cfptF0%3D Occurrence Handle8696081

    CAS  PubMed  Google Scholar 

  33. KV Ragnarsdottir (1993) ArticleTitleDissolution kinetics of heulandite at pH 2–12 and 25°C. Geochim Cosmochim Acta . 2439–2449 Occurrence Handle10.1016/0016-7037(93)90408-O

    Article  Google Scholar 

  34. BJ Rapp JD Wall (1987) ArticleTitleGenetic transfer in Desulfovibrio desulfuricans. Proc Natl Acad Sci USA 84 9128–9130 Occurrence Handle1:CAS:528:DyaL1cXhtVOgu7w%3D

    CAS  Google Scholar 

  35. P Rubini A Lakatos D Champmartin T Kiss (2002) ArticleTitleSpeciation and structural aspects of interactions of Al(III) with small biomolecules. Coord Chem Rev 228 137–152 Occurrence Handle10.1016/S0010-8545(01)00467-2 Occurrence Handle1:CAS:528:DC%2BD38XksVelsr4%3D

    Article  CAS  Google Scholar 

  36. R Scharf R Mamet Y Zimmels S Kimchie N Schoenfeld (1994) ArticleTitleEvidence for the interference of aluminum with bacterial porphyrin biosynthesis. Biometals 7 135–141 Occurrence Handle1:CAS:528:DyaK2cXjtFOntLs%3D Occurrence Handle8148615

    CAS  PubMed  Google Scholar 

  37. JL Sinclair WC Ghiorse (1989) ArticleTitleDistribution of aerobic bacteria, protozoa, algae, and fungi in deep subsurface sediments. Geomicrobiol J 7 15–31

    Google Scholar 

  38. G Stozky (1966) ArticleTitleInfluence of clay minerals on microorganisms. III. Effect of particle size, cation exchange capacity, and surface area on bacteria. Can J Microbiol 12 1235–1246 Occurrence Handle5963334

    PubMed  Google Scholar 

  39. W Stumm JJ Morgan (1981) Aquatic Chemistry. Wiley Interscience New York

    Google Scholar 

  40. GA Ulrich LR Krumholz JM Suflita (1997) ArticleTitleA rapid and simple method for estimating sulfate reduction activity and quantifying inorganic sulfides. Appl Environ Microbiol 63 1627–1630 Occurrence Handle1:CAS:528:DyaK2sXisVWrs7c%3D

    CAS  Google Scholar 

  41. GA Ulrich D Martino K Burger J Routh EL Grossman JW Ammerman JM 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 

  42. TL Weaver PR Dugan (1972) ArticleTitleEnhancement of bacterial methane oxidation by clay minerals. Nature 237 518 Occurrence Handle1:CAS:528:DyaE38XkvFylsLg%3D Occurrence Handle12635206

    CAS  PubMed  Google Scholar 

  43. RT Wilkin (1998) ArticleTitleSolubility and stability of zeolites in aqueous solution: I. Analcime, Na- and K-clinoptilolite. Am Mineral 83 746–761

    Google Scholar 

Download references

Acknowledgements

This work was funded by the Natural and Accelerated Bioremediation Research Program (NABIR) of the Office of Biological and Environmental Research of the U.S. Department of Energy’s Office of Science. We thank Anne Spain for her critical reading of the manuscript.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wong, D., Suflita, J., McKinley, J. et al. Impact of Clay Minerals on Sulfate-Reducing Activity in Aquifers . Microb Ecol 47, 80–86 (2004). https://doi.org/10.1007/s00248-003-1021-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-1021-z

Keywords

Navigation