Skip to main content
SpringerLink
Log in

Cooxidation of naphthalene and other polycyclic aromatic hydrocarbons by the nitrifying bacterium, Nitrosomonas europaea

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

The soil nitrifying bacterium Nitrosomonas europaea has shown the ability to transform cometabolically naphthalene as well as other 2- and 3-ringed polycyclic aromatic hydrocarbons (PAHs) to more oxidized products. All of the observed enzymatic reactions were inhibited by acetylene, a selective inhibitor of ammonia monooxygenase (AMO). A strong inhibitory effect of naphthalene on ammonia oxidation by N. europaea was observed. Naphthalene was readily oxidized by N. europaea and 2-naphthol was detected as a major product (85%) of naphthalene oxidation. The maximum naphthol production rate was 1.65 nmole/mg protein-min in the presence of 240 μM naphthalene and 10 mM NH4 +. Our results demonstrate that the oxidation between ammonia and naphthalene showed a partial competitive inhibition. The relative ratio of naphthalene and ammonia oxidation, depending on naphthalene concentrations, demonstrated that the naphthalene was oxidized 2200-fold slower than ammonia at lower concentration of naphthalene (15 μM) whereas naphthalene was oxidized only 100-fold slower than ammonia oxidation. NH4 +- and N2H4-dependent O2 uptake measurement demonstrated irreversible inhibitory effects of the naphthalene and subsequent oxidation products on AMO and HAO activity.

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

Similar content being viewed by others

References

  • Abeliovich A & Vonshak A. (1992) Anaerobic metabolism of Nitrosomonas europaea. Archives of Microbiol. 158: 267-270.

    Google Scholar 

  • Bossert ID, Whited G, Gibson DT & Young LY (1989) Anaerobic oxidation of p-cresol mediated by a partially purified methylhydroxylase by a denitrifying bacterium. J. Bacteriol. 171: 2956-2962.

    Google Scholar 

  • Bouchez M, Blanchet D & Vandecasteele JP (1995) Degradation of polycyclic aromatic hydrocarbons by pure strains and by defined strain associations: Inhibition phenomena and cometabolism. Appl. Microbiol. Biotechnol. 43: 156-164.

    Google Scholar 

  • Brusseau GA, Tsien Hsien-Chyang, Hanson RS & Wackett LP (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1: 19-29.

    Google Scholar 

  • Chang SW (1997) Cometabolic biodegradation of polycyclic aromatic hydrocarbons (PAHs) and aromatic ether by phenol-and ammonia-oxidizing bacteria. Ph.D. Dissertation, Oregon State University, Corvallis, Oregon.

    Google Scholar 

  • Chang SW, HymanMR & Williamson KJ (1998) Nitrifying bacteria as "priming catalysts" for the "biodegradation of xenobiotics" In: Wickramanayake GB & Hinchee RE (Eds) Natural Attenuation: Remediation of Chlorinated and Recalcitrant Compounds (pp 51-55). Battelle Press, Columbus, OH.

    Google Scholar 

  • Galushko A, Minz D, Schink B & Widdel F (1999) Anaerobic degradation of naphthalene by a pure culture of novel type of marine sulfate-reducing bacterium. Environ. Microbiol 1(5): 415-420.

    Google Scholar 

  • Gornall AG, Bardawill CJ & David MM (1949) Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177: 751-766.

    Google Scholar 

  • Hageman RH & Hucklesby DP (1971) Nitrate reductase from higher plants. Methods Enzymol. 23: 491-503.

    Google Scholar 

  • Hyman MR & Arp DJ (1992) 14C2H2-and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J. Bacteriol. 267(3): 1534-1545.

    Google Scholar 

  • Hyman MR & Wood PM (1983) Methane oxidation by Nirosomonas europaea. Biochem. J. 212: 31-37.

    Google Scholar 

  • Hyman MR & Wood PM (1984) Ethylene oxidation by Nirosomonas europaea. Arch. Microbiol. 137: 155-158.

    Google Scholar 

  • Hyman MR & Wood PM (1985) Suicidal inactivation and labelling of ammonia mono-oxygenase by acetylene. Biochem. J. 227: 729-725.

    Google Scholar 

  • Hyman MR, Murton IB & Arp DJ (1988) Interaction of ammonia monooxygenase from Nitrosomas europaea with alkanes, alkenes, and alkynes. Appl. Environ. Microbiol. 54(12): 3187-3190.

    Google Scholar 

  • Hyman MR, Page CL & ARP DJ (1994) Oxidation of methyl fluoride and dimethyl ether by ammonia monooxygenase in Nitrosomonas europaea. Appl. Environ. Microbiol. 60(8): 3033-3035.

    Google Scholar 

  • Juliette LY, Hyman MR & Arp DJ (1993) Inhibition of ammonia oxidation in Nitrosomonas europaea by sulfure compounds: Thioethers are oxidized to sulfoxides by ammonia oxygenase. Appl. Environ. Microbiol. 59(11): 3718-3727.

    Google Scholar 

  • KeenerWK & Arp DJ (1993) Kinetic studies of ammonia monooxygenase inhibition in Nitrosomonas europaea by hydrocarbons and halogenated hydrocarbons in an optimized whole-cell assay. Appl. Environ. Microbiol. 59(8): 2501-2510.

    Google Scholar 

  • Keener WK & Arp DJ (1994) Transformations of aromatic compounds by Nitrosomonas europaea. Appl. Environ. Microbiol. 60(6): 1914-1920

    Google Scholar 

  • Lee TJ, Chang SW, Hyman MR & Williamson KJ (1998) Cometabolic degradation of polycyclic aromatic hydrocarbons (PAHs) by a phenol-oxidizing bacteria. In: Proceeding of the 2nd International Conference of Advanced Wastewater Treatment, Recycling and Reuse, Vol. 2 (pp 607-615).

  • Lovley DR & Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl. Environ. Microbiol. 56(6): 1858-1864.

    Google Scholar 

  • Mihelcic JR & Luthy RG (1988) Degradation of polycyclic aromatic hydrocarbon compounds under various redox conditions in soilwater systems. Appl. Environ. Microbiol. 54: 1182-1187.

    Google Scholar 

  • Rasche ME, Hicks RE, Hyman MR & Arp DJ (1990) Oxidation of monohalogenated ethanes and n-chlorinated alkanes by whole cells of Nirosomonas europaea. J. Bacteriol. 172(9): 5368-5373.

    Google Scholar 

  • Rasche ME, Hyman MR & Arp DJ (1990) Biodegradation of halogenated hydrocarbon fumigants by nitrifying bacteria. Appl. Environ. Microbiol. 56(8): 2568-2571.

    Google Scholar 

  • Rasche ME, Hyman MR & Arp DJ (1991) Factors limiting aliphatic chlorocarbon degradation by Nitrosomonas europaea: Cometabolic inactivation of ammonia monooxygenase and substrate specificity. Appl. Environ. Microbiol 57(10): 2986-2994.

    Google Scholar 

  • Truesdale GA & Downing AL (1954) Solubility of oxygen in water. Nature (London) 173: 1236.

    Google Scholar 

  • Tschech A & Fuches G (1987) Anaerobic degradation of phenol by pure cultures of newly isolated denitrifying pseudomonas. Arch Microbiol. 148: 213-217.

    Google Scholar 

  • Walter U, Beyer M, Klein J & Rehm HJ (1991) Degradation of pyrene by Rhodococcus sp. UW1. Appl. Microbiol. Biotechnol. 34: 671-676.

    Google Scholar 

  • Weissenfels WD, Klein M, Beyer J & Rehm HJ (1991) Microbial metabolism of fluoranthene: Isolation and identification of ring fission products. Appl. Microbiol. Biotechnol. 34: 528-535.

    Google Scholar 

  • Wilson BH, Smith GB & Rees JF (1986) Biotransformation of selected alkylbenzenes and halogenated aliphatic hydrocarbons in methanogenic and aquifer materials: A microcosm study. Environ. Sci. Technol. 20: 997-1002.

    Google Scholar 

  • Wood PM (1986) Nitrification as a bacterial energy source. In: Prosser JI (Ed) Nitrification (pp 39-62). IRL Press, Oxford.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Kyonggi University, Suwon City, Korea

    Soon W. Chang

  2. Department of Microbiology, North Carolina State University, Raleigh, North Carolina, 27695, USA

    Michael R. Hyman

  3. Department of Civil, Construction, and Environmental Engineering, Oregon State University, Corvallis, OR, 97331, USA

    Kenneth J. Williamson

Authors
  1. Soon W. Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael R. Hyman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenneth J. Williamson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chang, S.W., Hyman, M.R. & Williamson, K.J. Cooxidation of naphthalene and other polycyclic aromatic hydrocarbons by the nitrifying bacterium, Nitrosomonas europaea . Biodegradation 13, 373–381 (2002). https://doi.org/10.1023/A:1022811430030

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022811430030

Search

Navigation