Aerobic biodegradation of N-nitrosodimethylamine (NDMA) by axenic bacterial strains.

The water contaminant N-nitrosodimethylamine (NDMA) is a probable human carcinogen whose appearance in the environment is related to the release of rocket fuel and to chlorine-based disinfection of water and wastewater. Although this compound has been shown to be biodegradable, there is minimal information about the organisms capable of this degradation, and little is understood of the mechanisms or biochemistry involved. This study shows that bacteria expressing monooxygenase enzymes functionally similar to those demonstrated to degrade NDMA in eukaryotes have the capability to degrade NDMA. Specifically, induction of the soluble methane monooxygenase (sMMO) expressed by Methylosinus trichosporium OB3b, the propane monooxygenase (PMO) enzyme of Mycobacterium vaccae JOB-5, and the toluene 4-monooxygenases found in Ralstonia pickettii PKO1 and Pseudomonas mendocina KR1 resulted in NDMA degradation by these strains. In each of these cases, brief exposure to acetylene gas, a suicide substrate for certain monooxygenases, inhibited the degradation of NDMA. Further, Escherichia coli TG1/pBS(Kan) containing recombinant plasmids derived from the toluene monooxygenases found in strains PKO1 and KR1 mimicked the behavior of the parent strains. In contrast, M. trichosporium OB3b expressing the particulate form of MMO, Burkholderia cepacia G4 expressing the toluene 2-monooxygenase, and Pseudomonas putida mt-2 expressing the toluene sidechain monooxygenase were not capable of NDMA degradation. In addition, bacteria expressing aromatic dioxygenases were not capable of NDMA degradation. Finally, Rhodococcus sp. RR1 exhibited the ability to degrade NDMA by an unidentified, constitutively expressed enzyme that, unlike the confirmed monooxygenases, was not inhibited by acetylene exposure.

[1]  J. Wishnok.  Relevance of N-Nitroso Compounds to Human Cancer. Exposures and Mechanisms. , 1988 .

[2]  W. A. Smith,et al.  Use of selective inhibitors and chromogenic substrates to differentiate bacteria based on toluene oxygenase activity. , 2001, Journal of microbiological methods.

[3]  P. H. Pritchard,et al.  Trichloroethylene Metabolism by Microorganisms That Degrade Aromatic Compounds , 1988, Applied and environmental microbiology.

[4]  Christy A. Smith,et al.  Characterization of the Initial Reactions during the Cometabolic Oxidation of Methyl tert-Butyl Ether by Propane-Grown Mycobacterium vaccae JOB5 , 2003, Applied and Environmental Microbiology.

[5]  Toxicological Profile for N-nitrosodimethylamine , 2022 .

[6]  S. Harayama,et al.  Characterization in vitro of the hydroxylase component of xylene monooxygenase, the first enzyme of the TOL-plasmid-encoded pathway for the mineralization of toluene and xylenes , 1995 .

[7]  H. Dalton,et al.  Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath) , 1985 .

[8]  D. Koop.  Oxidative and reductive metabolism by cytochrome P450 2E1 , 1992, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[9]  I. Rowland,et al.  The bacterial degradation of nitrosamines. , 1975, Biochemical Society transactions.

[10]  R. Tate,et al.  Stability of nitrosamines in samples of lake water, soil, and sewage. , 1975, Journal of the National Cancer Institute.

[11]  L. Alvarez-Cohen,et al.  Substrate interactions in BTEX and MTBE mixtures by an MTBE-degrading isolate. , 2001, Environmental science & technology.

[12]  A. M. Kaplan,et al.  Biodegradation of N-Nitrosodimethylamine in Aqueous and Soil Systems , 1985, Applied and environmental microbiology.

[13]  L. Newman,et al.  Purification and characterization of toluene 2-monooxygenase from Burkholderia cepacia G4. , 1995, Biochemistry.

[14]  P. Williams,et al.  Metabolism of toluene and xylenes by Pseudomonas (putida (arvilla) mt-2: evidence for a new function of the TOL plasmid , 1975, Journal of bacteriology.

[15]  Lewis Semprini,et al.  Diversity in Butane Monooxygenases among Butane-Grown Bacteria , 1999, Applied and Environmental Microbiology.

[16]  Thomas K. Wood,et al.  Directed Evolution of Toluene ortho-Monooxygenase for Enhanced 1-Naphthol Synthesis and Chlorinated Ethene Degradation , 2002, Journal of bacteriology.

[17]  P. Chapman,et al.  Novel Pathway of Toluene Catabolism in the Trichloroethylene-Degrading Bacterium G4 , 1989, Applied and environmental microbiology.

[18]  Comparison of factors influencing trichloroethylene degradation by toluene-oxidizing bacteria. , 1996, Applied and environmental microbiology.

[19]  J. Pennington,et al.  Attenuation mechanisms of N-nitrosodimethylamine at an operating intercept and treat groundwater remediation system. , 2000, Journal of hazardous materials.

[20]  T. Yoshinari,et al.  Degradation of dimethyl nitrosamine by Methylosinus trichosporium OB3b. , 1990, Canadian journal of microbiology.

[21]  Lawrence P. Wackett,et al.  Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. , 1983, Science.

[22]  R. H. Olsen,et al.  Nucleotide sequence analysis of genes encoding a toluene/benzene-2-monooxygenase from Pseudomonas sp. strain JS150 , 1995, Applied and environmental microbiology.

[23]  L. Alvarez-Cohen,et al.  Temperature effects and substrate interactions during the aerobic biotransformation of BTEX mixtures by toluene-enriched consortia and Rhodococcus rhodochrous. , 1999, Biotechnology and bioengineering.

[24]  R. Trussell,et al.  NDMA Formation in Water and Wastewater , 2001 .

[25]  K. Timmis,et al.  Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid , 1994, Journal of bacteriology.

[26]  C. S. Yang,et al.  Demethylation and denitrosation of nitrosamines by cytochrome P-450 isozymes. , 1985, Archives of biochemistry and biophysics.

[27]  D. Gibson,et al.  Incorporation of oxygen-18 into benzene by Pseudomonas putida. , 1970, Biochemistry.

[28]  R. B. Winter,et al.  Cloning and characterization of a Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase , 1991, Journal of bacteriology.

[29]  L. Alvarez-Cohen,et al.  Transformation capacities of chlorinated organics by mixed cultures enriched on methane, propane, toluene, or phenol , 1995, Biotechnology and bioengineering.

[30]  J. E. Oliver,et al.  Volatilization of Some Herbicide-Related Nitrosamines from Soils 1 , 1979 .

[31]  E. Frei,et al.  Oxidation of xenobiotics by plant microsomes, a reconstituted cytochrome P450 system and peroxidase: a comparative study. , 2000, Phytochemistry.

[32]  P. Magee,et al.  alpha-Hydroxylation pathway in the in vitro metabolism of carcinogenic nitrosamines: N-nitrosodimethylamine and N-nitroso-N-methylaniline. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Mirvish,et al.  Air-water and ether-water distribution of N-nitroso compounds: implications for laboratory safety, analytic methodology, and carcinogenicity for the rat esophagus, nose, and liver. , 1976, Journal of the National Cancer Institute.

[34]  L. Wackett,et al.  Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity , 1990, Biodegradation.

[35]  L. Wackett,et al.  Survey of microbial oxygenases: trichloroethylene degradation by propane-oxidizing bacteria , 1989, Applied and environmental microbiology.

[36]  H. Bartsch,et al.  Relevance of N-nitroso compounds to human cancer: exposures and mechanisms. Proceedings of the IXth International Symposium on N-Nitroso Compounds. Baden, Austria, 1-5 September 1986. , 1987, IARC scientific publications.

[37]  L. Wackett,et al.  Degradation of trichloroethylene by toluene dioxygenase in whole-cell studies with Pseudomonas putida F1 , 1988, Applied and environmental microbiology.

[38]  B. Fox,et al.  Toluene Monooxygenase-Catalyzed Epoxidation of Alkenes , 2000, Applied and Environmental Microbiology.

[39]  C. Pettigrew,et al.  Biodegradation of mixtures of substituted benzenes by Pseudomonas sp. strain JS150 , 1992, Applied and environmental microbiology.

[40]  L. Wackett,et al.  Trichloroethylene degradation by Escherichia coli containing the cloned Pseudomonas putida F1 toluene dioxygenase genes , 1989, Applied and environmental microbiology.

[41]  L. Wackett,et al.  Biodegradation of trichloroethylene by Methylosinus trichosporium OB3b , 1989, Applied and environmental microbiology.

[42]  P. H. Pritchard,et al.  Biodegradation of trichloroethylene and involvement of an aromatic biodegradative pathway , 1987, Applied and environmental microbiology.

[43]  R. Rhodes Trussell,et al.  N-Nitrosodimethylamine (NDMA) as a Drinking Water Contaminant: A Review , 2003 .

[44]  J. Kukor,et al.  Genetic and Functional Analysis of the tbc Operons for Catabolism of Alkyl- and Chloroaromatic Compounds inBurkholderia sp. Strain JS150 , 2001, Applied and Environmental Microbiology.

[45]  W. Bentley,et al.  Oxidation of Benzene to Phenol, Catechol, and 1,2,3-Trihydroxybenzene by Toluene 4-Monooxygenase of Pseudomonas mendocina KR1 and Toluene 3-Monooxygenase of Ralstonia pickettii PKO1 , 2004, Applied and Environmental Microbiology.

[46]  P. Bottomley,et al.  Inactivation of Toluene 2-Monooxygenase in Burkholderia cepacia G4 by Alkynes , 1999, Applied and Environmental Microbiology.

[47]  B. Fox,et al.  Recombinant toluene-4-monooxygenase: catalytic and Mössbauer studies of the purified diiron and rieske components of a four-protein complex. , 1996, Biochemistry.

[48]  A. Hooper,et al.  Degradation of trichloroethylene by the ammonia-oxidizing bacterium Nitrosomonas europaea. , 1989, Biochemical and biophysical research communications.

[49]  H. Yamazaki,et al.  Participation of rat liver cytochrome P450 2E1 in the activation of N-nitrosodimethylamine and N-nitrosodiethylamine to products genotoxic in an acetyltransferase-overexpressing Salmonella typhimurium strain (NM2009). , 1992, Carcinogenesis.

[50]  M. Alexander,et al.  Plant uptake and leaching of dimethylnitrosamine , 1976, Nature.

[51]  A. Roche,et al.  Organic Chemistry: , 1982, Nature.

[52]  D. Leak,et al.  Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures , 2004, Biotechnology Letters.

[53]  P. Mccarty,et al.  Effects of toxicity, aeration, and reductant supply on trichloroethylene transformation by a mixed methanotrophic culture , 1991, Applied and environmental microbiology.

[54]  B. Fox,et al.  Chloroform mineralization by toluene-oxidizing bacteria , 1996, Applied and environmental microbiology.

[55]  L. Semprini,et al.  Chloroform Cometabolism by Butane-Grown CF8, Pseudomonas butanovora, and Mycobacterium vaccae JOB5 and Methane-Grown Methylosinus trichosporium OB3b , 1997, Applied and environmental microbiology.

[56]  R. H. Olsen,et al.  Multiple pathways for toluene degradation in Burkholderia sp. strain JS150 , 1997, Applied and environmental microbiology.

[57]  R. H. Olsen,et al.  Catechol 2,3-dioxygenases functional in oxygen-limited (hypoxic) environments , 1996, Applied and environmental microbiology.

[58]  T. Wood,et al.  Toluene 3-Monooxygenase of Ralstonia pickettii PKO1 Is a para-Hydroxylating Enzyme , 2004, Journal of bacteriology.

[59]  David L Sedlak,et al.  Formation of N-nitrosodimethylamine (NDMA) from dimethylamine during chlorination. , 2002, Environmental science & technology.

[60]  Maryline C. Laugier,et al.  Impact of Ethanol on Benzene Plume Lengths: Microbial and Modeling Studies , 2002 .