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. In contrast, fungi, especially ligninolytic ones, usually only exhibit ‘side activities’ for the transformation of 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 decades 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 capability 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 10. 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).
Figure 2. Organohalogen compounds produced in natural systems (a) complex compounds carrying chloro‐, bromo‐, iodo‐ or fluorosubstituents, (b) compounds with antibiotic behaviour, (c) compounds with high potential of environmental risk: chloro‐ and bromodibenzo‐p‐dioxin or furan.
Figure 3. 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 4. 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 5. Degradation pathways for chlorinated aromatic compounds used by aerobic bacteria: Hydroquinone pathway determined for 2,4,5‐trichloro‐ and pentachlorophenol.
Figure 6. Metabolic transformations of chloroaromatic compounds by ligninolytic fungi: Proposed pathway for 2,4‐dichlorophenol by peroxidases and whole cells of Phanerochaete chrysosporium.
Figure 7. Metabolic transformations of chloroaromatic compounds by liver: Initial reaction steps and intermediates during chlorobenzene metabolism.
Figure 8. Degradation of chlorinated aliphatic compounds by aerobic bacteria: Dechlorination mechanisms used during growth with chloroaliphatic compounds.
Figure 9. Degradation of chlorinated aliphatic compounds by liver: Toxicologically critical reaction types responsible for the formation of highly reactive metabolites during chloroaliphatic metabolism.
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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.

Albers CN , Jacobsen OS , Flores EMM , Pereira JSF and Laier T (2011) Spatial variation in natural formation of chloroform in the soils of four coniferous forests. Biogeochemistry 103: 317–334.

Albers CN , Jacobsen OS , Flores EMM and Johnsen AR (2017) Arctic and subarctic natural soils emit chloroform and brominated analogues by alkaline hydrolysis of trihaloacetyl compounds. Environmental Science and Technology 51: 6131–6138.

Andreae MO and Merlet P (2001) Emission of trace gases and aerosols from biomass burning. Global Biogeochemical Cycles 15: 955–966.

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

Ballschmiter K (2003) Pattern and sources of naturally produced organohalogens in the marine environment: biogenic formation of organohalogens. Chemosphere 52: 313–324.

Bayer K , Scheuermayer M , Fieseler L and Hentschel U (2013) Genomic mining for novel FADH2‐dependent halogenases in marine sponge‐associated microbial consortia. Marine Biotechnology 15: 63–72.

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.

Berg RD and Solomon EA (2016) Geochemical constraints on the distribution and rates of debromination in the deep subseafloor biosphere. Geochimica et Cosmochimica Acta 174: 30–41.

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.

Chlorobenzenes (2017) Chemical Economics Handbook. IHS Markit Global Sarl: Perly, Switzerland.

Chloromethanes (2018) Chemical Economics Handbook. IHS Markit Global Sarl: Perly, Switzerland.

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.

Duarte M , Nielsen A , Camarinha‐Silva A , et al. (2017) Functional soil metagenomics: elucidation of polycyclic aromatic hydrocarbon degradation potential following 12 years of in situ bioremediation. Environmental Microbiology 19: 2992–3011.

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.

Field JA (2016) Natural production of organohalide compounds in the environment. In: Adrian L and Löffler F (eds) Organohalide‐Respiring Bacteria, pp 7–29. Springer‐Verlag: Berlin, Heidelberg.

Futagami T , Morono Y , Terada T , Kaksonen AH and Inagaki F (2009) Dehalogenation activities and distribution of reductive dehalogenase homologous genes in marine subsurface sediments. Applied and Environmental Microbiology 75: 6905–6909.

Gaboyer F , Burgaud G and Alain K (2015) Physiological and evolutionary potential of microorganisms from the Canterbury Basin subseafloor, a metagenomic approach. FEMS Microbiology Ecology 91: fiv029.

Garrido‐Sanz D , Manzano J , Martín M , Redondo‐Nieto M and Rivilla R (2018) Metagenomic analysis of a biphenyl‐degrading soil bacterial consortium reveals the metabolic roles of specific populations. Frontiers in Microbiology. 9: 232. DOI: 10.3389/fmicb.2018.00232.

Gribble GW (2010) Naturally occurring organohalogen compounds – a comprehensive update. In: Progress in the Chemistry of Organic Natural Products, vol. 91. Springer‐Verlag/Wien. DOI: 10.1007/978‐3‐211‐99323‐1_1.

Gribble GW (2015) A recent survey of naturally occurring organohalogen compounds. Environmental Chemistry 12: 396–405.

Hardacre CJ and Heal MR (2013) Characterization of methyl bromide and methyl chloride fluxes at temperate freshwater wetlands. Journal of Geophysical Research: Atmospheres 118: 977–991.

Hashimoto S , Wakimoto T and Tatsukawa R (1995) Possible natural formation of polychlorinated dibenzo‐p‐dioxins as evidenced by sediment analysis from the Yellow Sea, the East China Sea and the Pacific Ocean. Marine Pollution Bulletin 30: 341–346.

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

Hug LA and Edwards EA (2013) Diversity of reductive dehalogenase genes from environmental samples and enrichment cultures identified with degenerate primer PCR screens. Frontiers in Microbiology 4: 341.

Hug LA , Maphosa F , Leys D , et al. (2013) Overview of organohalide‐respiring bacteria and a proposal for a classification system for reductive dehalogenases. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20120322.

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

Jordan A , Harnisch J , Borchers R , Le Guern F and Shinohara H (2000) Volcanogenic halocarbons. Environmental Science and Technology 34: 1122–1124.

Kawai M , Futagami T , Toyoda A , et al. (2014) High frequency of phylogenetically diverse reductive dehalogenase‐homologous genes in deep subseafloor sedimentary metagenomes. Frontiers in Microbiology 5: 90.

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

Krzmarzick MJ , Miller HR , Yan T and Novak PJ (2014) Novel Firmicutes group implicated in the dechlorination of two chlorinated xanthones, analogues of natural organochlorines. Applied and Environmental Microbiology 80: 1210–1218.

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.

Löffler FE , Cole JR , Ritalahti KM and Tiedje JM (2004) Diversity of dechlorinating bacteria. In: Häggblom MM and Bossert ID (eds) Dehalogenation: Microbial Processes and Environmental Applications, pp 53–87. Kluwer Academic Publisher Group: Boston, MA.

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.

Lu Y , Atashgahi S , Hug LA and Smidt H (2015) Primers that target functional genes of organohalide‐respiring bacteria. In: McGenity T , Timmis KN and Nogales B (eds) Hydrocarbon and Lipid Microbiology Protocols, Springer Protocols Handbooks, pp 177–205. Springer: Berlin, Heidelberg.

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

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.

Marshall IPG , Karst SM , Nielsen PH and Jørgensen BB (2018) Metagenomes from deep Baltic Sea sediments reveal how past and present environmental conditions determine microbial community composition. Marine Genomics 37: 58–68. DOI: 10.1016/j.margen.2017.08.004.

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.

McMurdie PJ , Behrens SF , Müller JA , et al. (2009) Localized plasticity in the streamlined genomes of vinyl chloride respiring Dehalococcoides . PLoS Genetics 5: e1000714.

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.

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.

Röttjers L and Faust K (2018) From hairballs to hypotheses ‐ biological insights from microbial networks. FEMS Microbiology Reviews. 42: 761–780. DOI: 10.1093/femsre/fuy030.

Ruecker A , Weigold P , Behrens S , et al. (2014) Predominance of biotic over abiotic formation of halogenated hydrocarbons in hypersaline sediments in Western Australia. Environmental Science and Technology 48: 9170–9178.

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.

Schubert T and Diekert G (2016) Comparative biochemistry of organohalide respiration. In: Adrian L and Löffler F (eds) Organohalide‐Respiring Bacteria, pp 397–427. Springer: Berlin, Heidelberg.

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

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.

Temme HR , Carlson A and Novak PJ (2019) Presence, diversity, and enrichment of respiratory reductive dehalogenase and non‐respiratory hydrolytic and oxidative dehalogenase genes in terrestrial environments. Frontiers in Microbiology 10: 1258. DOI: 10.3389/fmicb.2019.01258.

Vaillancourt FH , Yeh E , Vosburg DA , Garneau‐Tsodikova S and Walsh CT (2006) Nature's inventory of halogenation catalysts: oxidative strategies predominate. Chemical Reviews 106: 3364–3378.

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.

Vilchez‐Vargas R , Geffers R , Suárez‐Diez M , et al. (2013) Analysis of the microbial gene landscape and transcriptome for aromatic pollutants and alkane degradation using a novel internally calibrated microarray system. Environmental Microbiology 15: 1016–1039.

Wagner C , El Omari M and König GM (2009) Biohalogenation: nature's way to synthesize halogenated metabolites. Journal of Natural Products 72: 540–553.

Wever R and van der Horst MA (2013) The role of vanadium haloperoxidases in the formation of volatile brominated compounds and their impact on the environment. Dalton Transactions 42: 11778–11786.

Wuosmaa A and Hager L (1990) Methyl chloride transferase: a carbocation route for biosynthesis of halometabolites. Science 249: 160–162.

Yang Y , Higgins SA , Yan J , et al. (2017) Grape pomace compost harbors organohalide‐respiring Dehalogenimonas species with novel reductive dehalogenase genes. ISME Journal 11: 2767–2780.

Zinder SH (2016) The genus Dehalococcoides . In: Adrian L and Löffler F (eds) Organohalide‐Respiring Bacteria, pp 107–136. Springer‐Verlag: Berlin, Heidelberg.

Zinke LA , Mullis MM , Bird JT , et al. (2017) Thriving or surviving? Evaluating active microbial guilds in Baltic Sea sediment. Environmental Microbiology Reports 9: 528–536.

Zlamal JE , Raab TK , Little M , Edwards RA and Lipson DA (2017) Biological chlorine cycling in the Arctic Coastal Plain. Biogeochemistry 134: 243–260.

Further Reading

Adrian L and Löffler FE (2016) Organohalide‐respiring bacteria. Springer‐Verlag: Berlin, Heidelberg.

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

Butler A and Sandy M (2009) Mechanistic considerations of halogenating enzymes. Nature 460: 848–854.

Fincker M and Spormann AM (2017) Biochemistry of catabolic reductive dehalogenation. Annual Reviews of Biochemistry 86: 357–386.

Häggblom MM and Bossert ID (2004) Dehalogenation: Microbial Processes and Environmental Applications. Kluwer Academic Publisher Group: MA.

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

van Pée KH and Unversucht S (2003) Biological dehalogenation and halogenation reactions. Chemosphere 52: 299–312.

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. Springer: Berlin.

Reineke W (2001) Aerobic and anaerobic biodegradation potentials of microorganisms. In: Hutzinger O (ed) The Handbook of Environmental Chemistry Vol. 2K The Natural Environment and Biogeochemical Cycles, (Volume editor: Beek B), pp 1–161. Springer: Berlin.

Schwarzenbach RP , Gschwend PM and Imboden DM (2016) Environmental Organic Chemistry, 3rd edn. John Wiley & Sons, Inc: Hoboken, NJ.

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Reineke, Walter, Mandt, Christian, Kaschabek, Stefan R, and Pieper, Dietmar H(Jul 2020) Chlorinated Hydrocarbon Metabolism. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000472.pub4]