Chlorinated Hydrocarbon Metabolism

Abstract

The widespread global distribution of chlorinated hydrocarbons, their high lipophilicity and their recalcitrance have contributed to their importance as environmental toxicants. Their metabolism under oxic and anoxic conditions mediated by prokaryotic and eukaryotic cells is discussed. Various aerobic bacteria are able to use chlorinated hydrocarbons as the sole source of carbon and energy and some anaerobic bacteria can use some of these as an artificial electron acceptor in reductive dechlorination. Liver enzymes are responsible for the formation of hydrophilic metabolites ready for excretion which often lead to highly reactive and potentially toxic intermediates. Whereas fungi, especially ligninolytic ones, usually only exhibit ‘side activities’ for chlorinated hydrocarbons. The capabilities of bacteria had led to the development of various bioremediation processes. Both, successes and failures within these processes are known. Therefore, current research aims at a better understanding of global community interactions.

Key Concepts:

  • Chlorinated hydrocarbons have been produced by the chemical industry since nearly a decade in large amounts, but they can also be observed as natural compounds, sometimes exceeding the industrially produced amounts.

  • Even though toxicological properties have pushed the chlorochemistry into the focus of considerable debate and governmental regulatory action, chlorinated hydrocarbons remain essential for certain applications.

  • The aerobic metabolism of chlorinated hydrocarbons by bacteria has been studied in detail and an immense amount of information is available on pathways, enzymes and genes involved in the mineralisation of chloroaromatics.

  • The anaerobic degradation of chlorinated hydrocarbons is due to the capablity of anaerobic bacteria to use them in anaerobic respiration, which results in dechlorination.

  • Dehalococcoides organisms are the most versatile reductive dehalogenators as being capable to dehalogenate chlorinated dioxins, biphenyls, benzenes and vinyl chloride, among others.

  • Microbial activities have been widespread used for bioremediation purposes through natural attenuation, biostimulation and bioaugmentation.

  • The poor understanding of the functioning of the complex microbial activities in situ made bioremediation efforts quite unreliable.

  • The rapid development of molecular techniques in recent years allows immense insights into the processes in situ, but also on the overall physiology of biocatalysts.

Keywords: biodegradation; bioremediation; chlorochemistry; dechlorination; toxicology

Figure 1.

Representative examples of chlorinated and nonchlorinated hydrocarbons known as environmental pollutants.

Figure 2.

Schematic presentation and comparison of logarithmic octanol–water partition coefficients log Kow, water solubilities Swater (mol m−3), vapour pressures p (Pa) and dimensionless Henry's law constants H (mol Lair−1/mol Lwater−1) for some selected chlorinated aliphatic and aromatic hydrocarbons. Grey scales indicate areas of similar partition behaviour between environmental compartments (see text).

Figure 3.

Degradation pathways for chlorinated aromatic compounds used by aerobic bacteria: peripheral, funnelling pathways and chlorocatechol‐degradative modified ortho‐ and meta‐pathway. Subscript numbers depict the amount of chlorine atoms present in the molecule. Only 3‐chlorocatechol is channelled into the meta‐pathway (right column).

Figure 4.

Degradation pathways for chlorinated aromatic compounds used by aerobic bacteria: Hydroquinone pathway determined for 2,4,5‐trichloro‐ and pentachlorophenol.

Figure 5.

Metabolic transformations of chloroaromatic compounds by ligninolytic fungi: Proposed pathway for 2,4‐dichlorophenol by peroxidases and whole cells of Phanerochaete chrysosporium.

Figure 6.

Metabolic transformations of chloroaromatic compounds by liver: Initial reaction steps and intermediates during chlorobenzene metabolism.

Figure 7.

Degradation of chlorinated aliphatic compounds by aerobic bacteria: Dechlorination mechanisms used during growth with chloroaliphatic compounds.

Figure 8.

Degradation of chlorinated aliphatic compounds by liver: Toxicologically critical reaction types responsible for the formation of highly reactive metabolites during chloroaliphatic metabolism.

Figure 9.

Simplified presentation of the dehalorespiration process, that is, use of chloroaliphatic or chloroaromatic compounds as the terminal electron acceptors leading to the elimination of the chlorine substituent (R=alkyl or arene).

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References

Ahn YB, Rhee SK, Fennell DE et al. (2003) Reductive dehalogenation of brominated phenolic compounds by microorganisms associated with the marine sponge Aplysina aerophoba. Applied and Environmental Microbiology 69: 4159–4166.

Ballschmiter K (1992) Transport and fate of organic compounds in the global environment. Angewandte Chemie International Edition in English 31: 487–515.

Bartels I, Knackmuss H‐J and Reineke W (1984) Inactivation of catechol 2,3‐dioxygenase from Pseudomonas putida mt‐2 by 3‐halocatechols. Applied and Environmental Microbiology 47: 500–505.

Bedard DL (2008) A case study for microbial biodegradation: anaerobic bacterial reductive dechlorination of polychlorinated biphenyls – from sediment to defined medium. Annual Review of Microbiology 62: 253–270.

Beil S, Mason J, Timmis KN and Pieper DH (1998) Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5‐tetrachlorobenzene. Journal of Bacteriology 180: 5520–5528.

Bombach P, Richnow HH, Kästner M and Fischer A (2010) Current approaches for the assessment of in situ biodegradation. Applied Microbiology and Biotechnology 86: 839–852.

Brennerova MV, Josefiova J, Brenner V, Pieper DH and Junca H (2009) Metagenomics reveals diversity and abundance of meta‐cleavage pathways in microbial communities from soil highly contaminated with jet fuel under air‐sparging bioremediation. Environmental Microbiology 11: 2216–2227.

Bunge M and Lechner U (2009) Anaerobic reductive dehalogenation of polychlorinated dioxins. Applied Microbiology and Biotechnology 84: 429–444.

Camara B, Nikodem P, Bielecki P et al. (2009) Characterization of a gene cluster involved in 4‐chlorocatechol degradation by Pseudomonas reinekei MT1. Journal of Bacteriology 191: 4905–4915.

Delzell E, Doull J, Giesy J et al. (1994) Interpretive review of the potential adverse effects of chlorinated organic chemicals on human health and the environment. Regulatory Toxicology and Pharmacology 20: 1–1056.

Dorn E and Knackmuss H‐J (1978) Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2‐dioxygenation of catechol. Biochemical Journal 174: 85–94.

Dybas MJ, Hyndman DW, Heine R et al. (2002) Development, operation, and long‐term performance of a full‐scale biocurtain utilizing bioaugmentation. Environmental Science and Technology 36: 3635–3644.

Ferrer M, Beloqui A, Timmis KN and Golyshin PN (2009) Metagenomics for mining new genetic resources of microbial communities. Journal of Molecular Microbiology and Biotechnology 16: 109–123.

Fetzner S, Müller R and Lingens F (1992) Purification and some properties of 2‐halobenzoate 1,2‐dioxygenase, a two component enzyme system from Pseudomonas cepacia 2CBS. Journal of Bacteriology 174: 279–290.

Goldstein RM, Mallory LM and Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Applied and Environmental Microbiology 50: 977–983.

Gribble GW (2003) The diversity of naturally produced organohalogens. Chemosphere 52: 289–297.

Harayama S, Kishira H, Kasai Y and Shutsubo K (1999) Petroleum biodegradation in marine environments. Journal of Molecular Microbiology and Biotechnology 1: 63–70.

He Z, Gentry TJ, Schad CW et al. (2007) GeoChip: a comprehensive microarray for investigating biogeochemical, ecological and environmental processes. ISME Journal 1: 67–77.

Hudlicky T, Gonzalez D and Gibson DT (1999) Enzymatic dihydroxylation of aromatics in enantioselective synthesis: expanding asymmetric methodology. Aldrichimica Acta 32: 35–62.

Janssen DB, Pries F and van der Ploeg JR (1994) Genetics and biochemistry of dehalogenating enzymes. Annual Review of Microbiology 48: 163–191.

Kaschabek SR and Reineke W (1992) Maleylacetate reductase of Pseudomonas sp. strain B13: dechlorination of chloromaleylacetates, metabolites in the degradation of chloroaromatic compounds. Archives of Microbiology 158: 412–417.

Klaasen CD (1996) Casarett and Doull's Toxicology. The Basic Science of Poisons, 5th edn. New York: McGraw‐Hill.

Lendvay JM, Löffler FE, Dollhopf M et al. (2003) Bioreactive barriers: a comparison of bioaugmentation and biostimulation for chlorinated solvent remediation. Environmental Science and Technology 37: 1422–1431.

Lorah MM and Voytek MA (2004) Degradation of 1,1,2,2‐tetrachloroethane and accumulation of vinyl chloride in wetland sediment microcosms and in situ porewater: biogeochemical controls and associations with microbial communities. Journal of Contaminant Hydrology 70: 117–145.

Macbeth TW, Cummings DE, Spring S, Petzke LM and Sørenson KS Jr (2004) Molecular characterization of a dechlorinating community resulting from in situ biostimulation in a trichloroethene‐contaminated deep, fractured basalt aquifer and comparison to a derivative laboratory culture. Applied and Environmental Microbiology 70: 7329–7341.

Machackova J, Wittlingerova Z, Vlk K, Zima J and Linka A (2008) Comparison of two methods for assessment of in situ jet‐fuel remediation efficiency. Water, Air and Soil Pollution 187: 181–194.

Madsen EL (2006) The use of stable isotope probing techniques in bioreactor and field studies on bioremediation. Current Opinion in Biotechnology 17: 92–97.

Major DW, McMaster ML, Cox EE et al. (2002) Field demonstration of successful bioaugmentation to achieve dechlorination of tetrachloroethene to ethene. Environmental Science and Technology 36: 5106–5116.

Mars AE, Kasberg T, Kaschabek SR et al. (1997) Microbial degradation of chloroaromatics: use of the meta‐cleavage pathway for mineralization of chlorobenzene. Journal of Bacteriology 179: 4530–4537.

Mars AE, Kingma J, Kaschabek SR, Reineke W and Janssen DB (1999) Conversion of 3‐chlorocatechol by various catechol 2,3‐dioxygenases and sequence analysis of the chlorocatechol dioxygenase region of Pseudomonas putida GJ31. Journal of Bacteriology 181: 1309–1318.

Maymo‐Gatell X, Nijenhuis I and Zinder SH (2001) Reductive dechlorination of cis‐1,2‐dichloroethene and vinyl chloride by ‘Dehalococcoides ethenogenes’. Environmental Science and Technology 35: 516–521.

McCarty PL, Goltz MN, Hopkins GD et al. (1998) Full‐scale evaluation of in situ cometabolic degradation of trichloroethylene in groundwater through toluene injection. Environmental Science and Technology 32: 88–100.

van der Meer JR (1994) Genetic adaptation of bacteria to chlorinated aromatic compounds. FEMS Microbiology Reviews 15: 239–249.

van der Meer JR and Sentchilo V (2003) Genomic islands and the evolution of catabolic pathways in bacteria. Current Opinion in Biotechnology 14: 248–254.

Moiseeva OV, Solyanikova IP, Kaschabek SR et al. (2002) A new modified ortho cleavage pathway of 3‐chlorocatechol degradation by Rhodococcus opacus 1CP: Genetic and biochemical evidence. Journal of Bacteriology 184: 5282–5292.

Pazos F, Valencia A and de Lorenzo V (2003) The organization of the microbial biodegradation network from a systems biology perspective. EMBO Report 4: 994–999.

Perez‐Pantoja D, Gonzalez B and Pieper DH (2009) Aerobic degradation of aromatic hydrocarbons. In: Timmis KN, McGenity T, van der Meer JR and de Lorenzo V (eds) Handbook of Hydrocarbon and Lipid Microbiology, vol. 2, pp. 800–829. Berlin: Springer.

Pieper DH, Gonzalez B, Camara B, Perez‐Pantoja D and Reineke W (2009) Aerobic degradation of chloroaromatics. In: Timmis KN, McGenity T, van der Meer JR and de Lorenzo V (eds) Handbook of Hydrocarbon and Lipid Microbiology, vol. 2, pp. 840–859. Berlin: Springer.

Potrawfke T, Armengaud J and Wittich RM (2001) Chlorocatechols at positions 4 and 5 are substrates of the broad‐spectrum chlorocatechol 1,2‐dioxygenase of Pseudomonas chlororaphis RW71. Journal of Bacteriology 183: 997–1011.

Reineke W (1998) Development of hybrid strains for the mineralization of chloroaromatics by patchwork assembly. Annual Review of Microbiology 52: 287–331.

Safe S (1997/1998) Limitations of the toxic equivalency factor approach for risk assessment of TCDD and related compounds. Teratogenesis, Carcinogenesis, and Mutagenesis 17: 285–304.

Schlömann M (1994) Evolution of chlorocatechol catabolic pathways. Conclusions to be drawn from comparison of lactone hydrolases. Biodegradation 5: 301–321.

Schmitz A, Gartemann K‐H, Fiedler J, Grund E and Eichenlaub R (1992) Cloning and sequence analysis of genes for dehalogenation of 4‐chlorobenzoate from Arthrobacter sp. strain SU. Applied and Environmental Microbiology 58: 4068–4071.

Scow KM and Hicks KA (2005) Natural attenuation and enhanced bioremediation of organic contaminants in groundwater. Current Opinion in Biotechnology 16: 246–253.

Shi Y, Tyson GW and DeLong EF (2009) Metatranscriptomics reveals unique microbial small RNAs in the ocean's water column. Nature 459: 266–269.

Smidt H and de Vos WM (2004) Anaerobic microbial dehalogenation. Annual Review of Microbiology 58: 43–73.

Taş N, van Eekert MH, de Vos WM and Smidt H (2010) The little bacteria that can – diversity, genomics and ecophysiology of ‘Dehalococcoides’ spp. in contaminated environments. Microbial Biotechnology 3: 389–402.

Valli K and Gold MH (1991) Degradation of 2,4‐dichlorophenol by the lignin‐degrading fungus Phanerochaete chrysosporium. Journal of Bacteriology 173: 345–352.

Vilchez‐Vargas R, Junca H and Pieper DH (2010) Metabolic networks, microbial ecology and ‘omics’ technologies: towards understanding in situ biodegradation processes. Environmental Microbiology 12: 3089–3104.

Further Reading

van Agteren MH, Keuning S and Janssen DB (1998) Handbook on Biodegradation and Biological Treatment of Hazardous Organic Compounds. Dordrecht: Kluwer Academic.

Gibson DT and Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Current Opinion in Biotechnology 11: 236–243.

Janssen DB, Oppentocht JE and Poelarends GJ (2001) Microbial dehalogenation. Current Opinion in Biotechnology 12: 245–258.

Reineke W (2001) Aerobic and anaerobic biodegradation potentials of microorganisms. The Handbook of Environmental Chemistry 2K: 1–161.

Schwarzenbach RP, Gschwend PM and Imboden DM (2003) Environmental Organic Chemistry, 2nd edn. Hoboken, NJ: Wiley.

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Reineke, Walter, Mandt, Christian, Kaschabek, Stefan R, and Pieper, Dietmar H(Nov 2011) Chlorinated Hydrocarbon Metabolism. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000472.pub3]