Skip to main content

Advertisement

SpringerLink
Log in

Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Biodegradation of polycyclic aromatic hydrocarbons (PAHs) in the environment is often limited due to unfavorable nutrient conditions for the bacteria that use these PAHs as sole source of carbon and energy. Mycobacterium and Sphingomonas are 2 PAH-degrading specialists commonly present in PAH-polluted soil, but not much is known about their specific nutrient requirements. By adding different inorganic supplements of nitrogen (N) and phosphorus (P), affecting the overall carbon/nitrogen/phosphorus ratio of soil in soil slurry degradation tests, we investigated the impact of soil inorganic N and P nutrient conditions on PAH degradation by PAH-degrading Sphingomonas and Mycobacterium strains. The general theoretically calculated C/N/P ratio of 100/10/1 (expressed in moles) allowed rapid PAH metabolization by Sphingomonas and Mycobacterium strains without limitation. In addition, PAH-degradation rate and extent was not affected when ca. ten times lower concentrations of N and P were provided, indicating that Sphingomonas and Mycobacterium strains are capable of metabolizing PAHs under low nutrient conditions. Nor does PAH-degradation seem to be affected by excesses of N and P creating an imbalanced C/N/P ratio. However, supplements of N and P salts increased the salinity of soil slurry solutions and seriously limited or even completely blocked biodegradation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Alexander M (1994) Biodegradation and bioremediation. Academic Press, New York

    Google Scholar 

  • Atagana HI, Haynes RJ, Wallis FM (2003) Optimization of soil physical and chemical conditions for bioremediation of creosote-contaminated soil. Biodegradation 14:297–307

    Article  CAS  PubMed  Google Scholar 

  • Baker KH, Herson DS (1994) Bioremediation. McGraw-Hill, New York

    Google Scholar 

  • Bastiaens L (1998) Isolation and characterization of polycyclic aromatic hydrocarbon degrading bacteria and evaluation of the use of isolates in soil slurry experiments. PhD thesis. KU Leuven

    Google Scholar 

  • Bastiaens L, Springael D, Wattiau P, Harms H, De Wachter R, Verachtert H, Diels L (2000) Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl Environ Microbiol 66:1834–1843

    Article  CAS  PubMed  Google Scholar 

  • Bossert I, Bartha R (1984) The fate of petroleum in soil ecosystems. In: Atlas RM (ed) Petroleum microbiology. Macmillan, New York, pp 441–473

    Google Scholar 

  • Bouchez M, Blanchet D, Vandecasteele J-P (1995) Degradation of polycyclic aromatic hydrocarbons by pure strains and by defined strain associations: inhibition phenomena and cometabolism. Appl Environ Microbiol 43:156–164

    Article  CAS  Google Scholar 

  • Bouchez M, Blanchet D, Vandecasteele JP (1996) The microbiological fate of polycyclic aromatic hydrocarbons: carbon and oxygen balances for bacterial degradation of model compounds. Appl Microbiol Biotechnol 45:556–561

    Article  CAS  PubMed  Google Scholar 

  • Carmichael L, Pfaender K (1997) The effect of inorganic and organic supplements on the microbial degradation of phenanthrene and pyrene in soils. Biodegradation 8:1–13

    Article  CAS  PubMed  Google Scholar 

  • Cerniglia CE (1984) Microbial degradation of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:31–71

    CAS  PubMed  Google Scholar 

  • Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368

    CAS  Google Scholar 

  • Cookson JRJ (1995) Bioremediation engineering: design and application. McGraw-Hill Inc., New York

    Google Scholar 

  • Daugulis AJ, Janikowshik TB (2002) Scale-up performance of a partitioning bioreactor for the degradation of polyaromatic hydrocarbons by Sphingomonas aromaticivorans. Biotechnol Lett 24:591–594

    Article  CAS  Google Scholar 

  • Edwards NT (1983) Polycyclic aromatic hydrocarbons (PAHs) in the terrestrial environment—a review. J Environ Qual 4:427–441

    Google Scholar 

  • Enzminger JD (1987) Environmental fate of polynuclear aromatic hydrocarbons in coal tar. Environ Technol Lett 8:269–278

    CAS  Google Scholar 

  • Erickson DC, Loehr RC, Neuhauser EF (1993) PAH loss during bioremediation of manufactured gas plant site soils. Water Res 27:911–919

    Article  CAS  Google Scholar 

  • Grosser RJ, Warshawsky D, Vestal JR (1991) Indigenous and enhanced mineralization of pyrene, benzo[a]pyrene, and carbazole in soils. Appl Environ Microbiol 57

  • Hoeppel RE, Hinchee RE (1994) Enhanced biodegradation for on-site remediation of contaminated soils and groundwater. Marcel Dekker Inc., New York

    Google Scholar 

  • Jobson A, McClaughling M, Cook FD, Darby JL (1974) Effects of amendments on the microbial utilization of oil in soil. Appl Microbiol Biotechnol 27:166–171

    CAS  Google Scholar 

  • Johnson CJ, Scow MK (1990) Effect of nitrogen and phosphorus addition on phenanthrene biodegradation in four soils. Biodegradation 10:43–50

    Article  Google Scholar 

  • Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo(a)pyrene. Int J Biodeterior Biodegrad 45:57–88

    Article  CAS  Google Scholar 

  • Kanaly RA, Harayama S (2000) Biodegradation of high molecular weight-polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067

    Article  CAS  PubMed  Google Scholar 

  • Leys NMEJ, Ryngaert A, Bastiaens L, Top E, Springael D (2004) Occurrence and phylogenetic diversity of Sphingomonas in soils contaminated with polycyclic aromatic hydrocarbons (PAHs). Appl Environ Microbiol 70:1944–1955

    Article  CAS  PubMed  Google Scholar 

  • Luthy RG, Dzombak DA, Peters CA, Roy SB, Ramaswani A, Nakles DV, Nott BR (1994) Remediating tar-contaminated soils at manufactured gas plant sites. Environ Sci Technol 28:A266–A276

    Google Scholar 

  • Macleod CJA, Semple KT (2002) The adaptation of two similar soils to pyrene catabolism. Environ Pollut 119:357–364

    Article  CAS  PubMed  Google Scholar 

  • Manilal VB, Alexander M (1991) Factors affecting the microbial degradation of phenanthrene in soil. Microbiol Biotechnol 35:401–405

    CAS  Google Scholar 

  • Morgan P, Watkinson RJ (1992) Factors limiting the supply and efficiency of nutrient and oxygen supplements for the in situ biotreatment of contaminated soil and groundwater. Water Res 73–78

    Article  Google Scholar 

  • Mueller JG, Chapman PJ, Blattmann BO, Pritchard PH (1990) Isolation and characterisation of a fluoranthene-utilizing strains of Pseudomonas paucimobilis. Appl Environ Microbiol 56:1079–1086

    CAS  PubMed  Google Scholar 

  • Paul EA, Clark PE (1989) Soil microbiology and biochemistry. Academic Press, New York

    Google Scholar 

  • Rosenberg E, Legman R, Kushmaro A, Adler E, Abir H, Ron EZ (1996) Oil bioremediation using insoluble nitrogen source. J Biotechnol 51:273–278

    Article  CAS  PubMed  Google Scholar 

  • Steffensen W, Alexander M (1995) Role of competition for inorganic nutrients in the biodegradation of mixtures of substrates. Appl Environ Microbiol 61:2859–2862

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Thorton-Manning JR, Jones DD, Federle TW (1987) Effects of experimental manipulations of environmental factors on phenol mineralization in soil. Environ Toxicol Chem 6:615–621

    Google Scholar 

  • Vidali M (2001) Bioremediation. An overview. Pure Appl Chem 73:1163–1172

    CAS  Google Scholar 

  • Vrede K, Heldal M, Norland S, Bratbak G (2002) Elemental composition (C, N, P) and cell volume of exponentially growing and nutrient-limited bacterioplankton. Appl Environ Microbiol 68:2965–2971

    Article  CAS  PubMed  Google Scholar 

  • Ward DM, Liebeg AE, Cutright TJ (1999) The investigation of enhanced bioremediation through the addition of macro- and micro-nutrients in a PAH-contaminated soil. Int J Bioterior Biodegrad 44:55–64

    Article  Google Scholar 

  • Wick LY, Colangelo T, Harms H (2001) Kinetics of mass transfer-limited bacterial growth on solid PAHs. Environ Sci Technol 35:354–361

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, Ruiz de Munain A, Springael D, Harms H (2002a) Responses of Mycobacterium sp. LB501T to the low bioavailability of solid anthracene. Appl Microbiol Biotechnol 58:378–385

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, Wattiau P, Harms H (2002b) Influence of the growth substrate on the mycolic acid profiles of mycobacteria. Environ Microbiol 4:612–616

    Article  CAS  PubMed  Google Scholar 

  • Wick LY, Pelz O, Bernasconi SM, andersen N, Harms H (2003) Influences of the growth substrate on ester-linked phospho- and glycolipid fatty acids of PAH-degrading Mycobacterium sp. LB501T. Environ Microbiol 5:672–680

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Willumsen P, Nielsen JK, Karlson U (2001) Degradation of phenanthrene-analogue azaarenes by Mycobacterium gilvum LB307T under aerobic conditions. Appl Microbiol Biotechnol 56:539–544

    Article  CAS  PubMed  Google Scholar 

  • Wilson SC, Jones KC (1993) Bioremediation of soil contaminated with polynuclear aromatic hydrocarbons (PAHs): a review. Environ Pollut 81:1103–1106

    Article  Google Scholar 

  • Würdemann H, Lund NC, Gudehus G (1995) Assessment of a biological in situ remediation. In: Hinchee RE, Miller RN, Johnson PC (eds) In situ aeration: air sparging, bioventing and related remediation processes. Battelle, Columbus, pp 237–247

    Google Scholar 

Download references

Acknowledgements

This work was partially supported by the EC contract QLK3-1999-00326

Author information

Author notes

  1. Natalie M. Leys

    Present address: Laboratory of Microbiology, Belgian Nuclear Research Centre, Boeretang, 2400, Mol, Belgium

  2. Dirk Springael

    Present address: Laboratory for Soil and Water Management, Catholic University of Leuven, Kasteelpark arenberg 20, 3001, Heverlee, Belgium

Authors and Affiliations

  1. Flemish institute for Technological Research (Vito), Environmental and Process Technology, Boeretang 200, 2400, Mol, Belgium

    Natalie M. Leys, Leen Bastiaens & Dirk Springael

  2. Laboratory of Microbial Ecology and Technology, University of Ghent, Coupure Links 653, 9000, Gent, Belgium

    Natalie M. Leys & Willy Verstraete

Authors
  1. Natalie M. Leys
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Leen Bastiaens
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Willy Verstraete
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dirk Springael
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dirk Springael.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Leys, N.M., Bastiaens, L., Verstraete, W. et al. Influence of the carbon/nitrogen/phosphorus ratio on polycyclic aromatic hydrocarbon degradation by Mycobacterium and Sphingomonas in soil. Appl Microbiol Biotechnol 66, 726–736 (2005). https://doi.org/10.1007/s00253-004-1766-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-004-1766-4

Keywords

Search

Navigation