Skip to main content
Log in

Contrasts between subsurface microbial communities and their metabolic adaptation to polycyclic aromatic hydrocarbons at a forested and an urban coal-tar disposal site

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The abundance and distribution of microorganisms and their potential for mineralizing polycyclic aromatic hydrocarbons (PAHs) were measured in subsurface sediment samples at two geographically separate buried coal-tar sites. At a relatively undisturbed forested site in the northeastern United States, metabolic adaptation to the PAHs was evident: Radiolabeled naphthalene and phenanthrene were converted to 14CO2 in core material from inside but not outside a plume of groundwater contamination. However, at the urban site in the midwestern United States these PAHs were mineralized in sediments from both contaminated and uncontaminated boreholes. Thus, clear qualitative evidence showing an adaptational response by the subsurface microbial community was not obtained at the urban site. Instead, subtler clues suggesting metabolic adaptation by subsurface microorganisms from the urban site were discerned by comparing lag periods and extents of 14CO2 production from radiolabeled PAHs added to samples from contaminated and uncontaminated boreholes. Despite slightly higher PAH mineralization activity in contaminated borehole samples, p-hydroxybenzoate was mineralized equally in all samples from the urban site regardless of location. No striking trends in the abundances of actinomycetes, fungi, and either viable or total bacteria were encountered. However, colonies of the soil bacterium, Bacillus mycoides, were detected on enumeration plates of several samples from unsaturated and saturated zones in both urban boreholes. Furthermore, other common soil bacteria, Myxococcus xanthus and Chromobacterium violaceum, were identified in samples from the uncontaminated urban borehole. The occurrence of bacteria usually restricted to surface soil, combined with the observation of fragments of building materials in many of the core samples, suggested that past excavation and backfilling operations may have caused mixing of surface soil with subsurface materials at the urban site. We speculate that this mixing, as well as non-coal-tar-derived sources of PAHs, contributed to the PAH-mineralizing activity present in the sediment samples from the uncontaminated urban borehole.

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.

Similar content being viewed by others

References

  1. Aamand J, Jørgensen C, Arvin E, Jensen BK (1989) Microbial adaptation to degradation of hydrocarbons in polluted and unpolluted groundwater. J Contam Hydrol 4:299–312

    Google Scholar 

  2. Aelion CM, Dobbins DC, Pfaender FK (1989) Adaptation of aquifer microbial communities to the biodegradation of xenobiotic compounds: Influence of substrate concentration and preexposure. Environ Toxicol Chem 8:75–86

    Google Scholar 

  3. Alexander M (1977) Introduction to soil microbiology. Second ed. John Wiley & Sons, New York

    Google Scholar 

  4. Alexander M (1981) Biodegradation of chemicals of environmental concern. Science 211:132–138

    Google Scholar 

  5. Anderson JPE (1982) Soil respiration. In: Page AL, Miller RH, Keeney DR (eds), Methods of soil analysis, part 2. Chemical and microbiological properties. Second ed, American Society for Agronomy, Madison, WI, pp 831–871

    Google Scholar 

  6. Armstrong AQ, Hodson RE, Hwang H-M, Lewis DL (1991) Environmental factors affecting toluene degradation in ground water at a hazardous waste site. Environ Toxicol Chem 10:147–158.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  9. Bergey's Manual of Systematic Bacteriology (1984) Vol. 1. Krieg NR, Holt JG (eds) Williams & Wilkins, Baltimore

    Google Scholar 

  10. Bergey's Manual of Systematic Bacteriology (1986) Vol. 2. Sneath PHA, Mair NS, Sharpe ME. Holt JG (eds) Williams & Wilkins, Baltimore

    Google Scholar 

  11. Bergey's Manual of Systematic Bacteriology (1989) Vol. 3, Staley IT, Bryant MP, Pfennig N, Holt JG (eds) Williams & Wilkins, Baltimore

    Google Scholar 

  12. Dagley S (1977) Microbial degradation of organic compounds in the biosphere. Surv Prog Chem 8:121–170

    Google Scholar 

  13. Ghiorse WC, Balkwill DL (1983) Enumeration and morphological characterization of bacteria indigenous to subsurface environments. Dev Ind Microbiol 24:213–224

    Google Scholar 

  14. Ghiorse WC, Wilson JT (1988) Microbial ecology of the terrestrial subsurface. Adv Appl Microbiol 33:107–172

    Google Scholar 

  15. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315

    CAS  PubMed  Google Scholar 

  16. Madsen EL (1991) Determining in situ biodegradation: Facts and challenges. Environ Sci Technol 25:1662–1673

    Google Scholar 

  17. Madsen EL, Bollag JM (1989) Aerobic and anaerobic microbial activity in deep subsurface sediments from the Savannah River Plant. Geomicrobiol 17:93–101

    Google Scholar 

  18. Madsen EL, Levine SN, Ghiorse WC (1991) Microbiology of a coal-tar disposal site. Final Report EN-7319. Electric Power Research Institute, 3412 Hillview Ave., Palo Alto, CA 94304

    Google Scholar 

  19. Madsen EL, Ghiorse WC (1992) Ground water microbiology: Subsurface ecosystem processes. In: Ford T (ed) Aquatic microbiology: An ecological approach. Blackwell Scientific Publishers, Inc., Cambridge, MA (in press)

    Google Scholar 

  20. Madsen EL, Sinclair JL, Ghiorse WC (1991) In situ biodegradation: Microbiological patterns in a contaminated aquifer. Science 252:830–833

    CAS  PubMed  Google Scholar 

  21. Moss MO, Ryall C (1981) The genus chromobacterium. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes, vol. II. Springer-Verlag, Berlin, pp 1355–1363

    Google Scholar 

  22. Moorman TB (1990) Adaptation of microorganisms in subsurface environments. In: Racke KD, Coats JR (eds) Enhanced biodegradation of pesticides in the environment. American Chemical Society, Washington, DC, pp 167–180

    Google Scholar 

  23. Norris JR, Berkeley RCW, Logan NA, O'Donnell AG (1981) The genera Bacillus and Sporolactobacillus. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes, vol. II. Springer-Verlag, Berlin, pp 1711–1742

    Google Scholar 

  24. Reichenbach H, Dworkin M (1981) The order Myxobacterales. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes, vol. I. Springer-Verlag, Berlin, pp 328–355

    Google Scholar 

  25. Seeley HW Jr, VanDemark PJ (1981) Microbes in action. Third ed. WH Freeman and Co, San Francisco

    Google Scholar 

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

    Google Scholar 

  27. 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 28:369–377

    Google Scholar 

  28. Smith RL, Harvey RW, LeBlanc DR (1991) Importance of closely spaced vertical sampling in delineating chemical and microbiological gradients in groundwater studies. J Contaminant Hydrol 7:285–300

    Google Scholar 

  29. Suflita JM, Miller GD (1985) Microbial metabolism of chlorophenolic compounds in groundwater aquifers. Environ Toxicol Chem 4:751–758

    Google Scholar 

  30. Swindoll CM, Aelion CM, Pfaender FK (1988) Influence of inorganic and organic nutrients on aerobic biodegradation and on the adaptation response of subsurface microbial communities. Appl Environ Microbiol 54:212–217

    Google Scholar 

  31. Taylor B, Mauro D, Hayes MB, Holmen B, Young M (1990) Composition and migration of coal tar derived organic compounds in a sandy aquifer. Proceedings: Environmental Research Conference on Groundwater Quality and Waste Disposal. EN-6749. Electric Power Research Institute, 3412 Hillview Ave., Palo Alto, CA 94304

    Google Scholar 

  32. Thomas JM, Lee MD, Scott MJ, Ward CH (1989) Microbial ecology of the subsurface at an abandoned creosote waste site. J Ind Microbiol 4:109–120

    CAS  PubMed  Google Scholar 

  33. Villaume JF (1984) Coal tar wastes: Their environmental fate and effects. In: Majumdar SK & Miller EW (eds), Hazardous and toxic wastes: Technology management and health effects. The Pennsylvania Academy of Science, Easton, PA, pp 362–375

    Google Scholar 

  34. Wiggins BA, Jones SH, Alexander M (1987) Explanations for the acclimation period preceding the mineralization of organic chemicals in aquatic environments. Appl Environ Microbial 53:791–796

    Google Scholar 

  35. Wilson JT, McNabb JF, Cochran JW, Wang TH, Tomson MB, Bedient PB (1985) Influence of microbial adaptation on the fate of organic pollutants in ground water. Environ Toxicol Chem 4:721–726

    Google Scholar 

  36. Zehnder AJB, Stumm W (1988) Geochemistry and biogeochemistry of anaerobic habitats. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 1–38

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Madsen, E.L., Winding, A., Malachowsky, K. et al. Contrasts between subsurface microbial communities and their metabolic adaptation to polycyclic aromatic hydrocarbons at a forested and an urban coal-tar disposal site. Microb Ecol 24, 199–213 (1992). https://doi.org/10.1007/BF00174455

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00174455

Keywords

Navigation