Abstract
Chlorinated methanes are important environmental pollutants, which can be metabolized by bacteria. The biotransformation of chlorinated methanes by bacteria has been shown to be due either to gratuitous metabolism (cometabolism) or their use as a source of carbon and energy. The reactions which result in carbon-halogen bond cleavage include substitutive, reductive, oxygenative, and gem-elimination mechanisms. Certain methylotrophic bacteria can use dichloromethane as a source of carbon and energy. Dichloromethane dehalogenase catalyzes the first substitutive reaction in this metabolism. The enzyme shows a 1010-fold rate enhancement over the reaction of the bisulfide anion with dichloromethane in water. Pseudomonas putida G786 synthesizes cytochrome P-450CAM which catalyzes the gratuitous reduction of chlorinated methanes. These studies with purified enzymes are beginning to reveal more detailed mechanistic features of bacterial chlorinated methane metabolism.
Similar content being viewed by others
Abbreviations
- DNA:
-
deoxyribonucleic acid
- kcat :
-
catalytic first order rate constant for an enzyme catalyzed reaction
- KM :
-
Michaelis constant for an enzyme catalyzed reaction
- MNDO:
-
modified neglect of diatomic overlap
- PIMA:
-
pattern induced multialignment
- DCMD:
-
dichloromethane dehalogenase
References
Ahmed & Anders (1976) Metabolism of dihalomethanes to formaldehyde and inorganic halide I. In vitro studies. Drug Metab. Dispo. 4: 357–361
AhmedAE & AndersMW (1978) Metabolism of ihalomethanes to formaldehyde and inorganic halide II. Studies on the mechanism of the reaction. Biochem. Pharmacol. 27: 2021
Alvarez-CohenL & McCartyPL (1991a) Two-stage dispersedgrowth treatment of halogenated aliphatic compounds by cometabolism. Environ. Sci. Technol. 25: 1387–1393
Alvarez-CohenL & McCartyPL (1991b) Product toxicity and cometabolic competitive inhibition modeling of chloroform and trichloroethylene transformation by methanotrophic resting cells. Appl. Environ. Microbiol. 57: 1031–1037
AndersMW & PohlLR (1985) Halogenated alkanes. In: AndersMW (Ed) Bioactivation of Foreign Compounds, Halogenated Alkanes (pp 283–315). Academic Press, New York
AndersonJG, TooheyDW & BruneWH (1991) Free radicals within the antarctic vortex: the role of CFC's in antarctic ozone loss. Science 251: 39–46
AnthonyC (1982) The Biochemistry of Methylotrophs. Academic Press, London
ArmstrongRN (1991) Glutathione S-transferases: reaction mechanism, structure, and function. Chem. Res. Toxicol. 4: 131–140
BouwerEJ & McCartyPL (1983) Transformations of 1- and 2-carbon halogenated aliphatic organic compounds under methanogenic conditions. Appl. Environ. Microbiol. 45: 1286–1294
BouwerEJ, RittmanBE & McCartyPL (1981) Anaerobic degradation of halogenated 1- and 2-carbon compounds. Environ. Sci. Tech. 15: 596–599
BradshawWH, ConradHE, CoreyEJ, GunsalusIC & LednicerD (1959) Microbiological degradation of (+)-camphor. J. Am. Chem. Soc. 81: 5507
BrusseauGA, TsienHC, HansonRS & WackettLP (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodegradation 1: 19–29
CastroCE, WadeRS & BelserNO (1985) Biodehalogenation: reactions of cytochrome P-450 with polyhalomethanes. Biochemistry 24: 204–210
ChouPY & FasmanGD (1978) Empirical predictions of protein conformation. Ann. Rev. Biochem. 47: 251–276
ColbyJ, StirlingD & DaltonH (1977) The soluble methane monooxygenase of Methylococcus capsulatus (Bath): its ability to oxygenate n-alkanes, n-alkenes, ethers and alicyclic, aromatic and heterocyclic compounds. Biochem. J. 165: 395–402
CriddleCS, DeWittJT & McCartyPL (1990a) Reductive dehalogenation of carbon tetrachloride by Escherichia coli K-12 Appl Environ. Micro. 56: 3247–3254
CriddleCS, DeWittJT, Grbić-CalićD & McCartyPL (1990b) Transformation of carbon tetrachloride by Pseudomonas sp KC under denitrification conditions. Appl. Environ. Microbiol. 56: 3240–3246
DeanJA (1985) Lange's Handbook of Chemistry (13th ed.). McGraw-Hill, New York
DiekertG, KleeB & ThauerRK (1980) Nickel, a component of factor F430 from Methanobacterium thermoautotrophicum. Arch. Microbiol. 124: 103–106
DiStefanoTD, GossetJM & ZinderSH (1991) Reductive dechlorination of high concentrations of tetrachloroethene to ethene by an anaerobic enrichment culture in the absence of methanogenesis. Appl. Environ. Microbiol. 57: 2287–2292
DouglasKT (1987) Mechanism of action of glutathione dependent enzymes. In: MeisterA (Ed) Advances in Enzymology and Related Areas of Molecular Biology 59: 103–167. John Wiley & Sons, New York
EgliC, ScholtzR, CookAM & LeisingerT (1988a) Anaerobic dechlorination of tetrachloromethane and 1,2-dichloroethane to degradable products by pure cultures of Desulfobacterium sp. and Methanobacterium sp. FEMS Microbiol. Lett. 43: 257–261
EgliC, TschanT, ScholtzR, CookAM & LeisingerT (1988b) Transformation of tetrachloromethane to dichloromethane and carbon dioxide by Acetobacterium woodii. Appl. Environ. Microbiol. 54: 2819–2824
EgliC, StromeyerS, CookAM & LeisingerT (1990) Transformation of tetra- and trichloromethane to CO2 by anaerobic bacteria is a non-enzymic process. FEMS Microbiol. Lett. 68: 207–212
FisherMT & SligarSG (1985) Control of heme protein potential and reduction rate: linear free energy relation between potential and ferric spin state equilibrium. J. Am. Chem. Soc. 107: 5018–5019
FoxBG, BornemanJG, WackettLP & LipscombJD (1990) Haloalkane oxidation by the soluble methane monooxygenase from Methylsinus trichosporium OB3b: mechanistic and environmental implications. Biochemistry 29: 6419–6427
FreedmanDL & GossetJM (1991) Biodegradation of dichloromethane and its utilization as a growth substrate under methanogenic conditions. Appl. Environ. Microbiol. 57: 2847–2857
FukuiK, MorokumaK, KatoH & YonezawaT (1963) Polarographic reductive and electronic structures of organic halides. Bull. Chem. Soc. Japan 36: 217–222
Gälli R (1986) Optimierung des mikrobiellen abbaus von dichloromethan in einem wirbelschicht-bioreaktor. Ph.D. dissertation, Swiss Federal Institute of Technology (ETH) Zürich
GälliR & McCartyPL (1989) Biotransformation of 1,1,1-trichloroethane, trichloromethane, and tetrachloromethane by a Clostridium sp. Appl. Environ. Microbiol. 55: 837–844
GälliR, StuckiG & LeisingerT (1982) Mechanism of dehalogenation of dichloromethane by cell extracts of Hyphomicrobium DM2. Experentia 38: 1378
GantzerCJ & WackettLP (1991) Reductive dehalogenation catalyzed by bacterial transition-metal coenzymes. Environ. Sci. Technol. 25: 715–722
GraminskiGF, KuboY, & ArmstrongRN (1989) Spectroscopic and kinetic evidence for the thiolate anion of glutathione at the active site of glutathione S-transferase. Biochemistry 28: 3562–3568
GreimH, BimboesD, EgertG, GoeggelmanW & KraemerM (1977) Mutagenicity and chromosomal aberrations as an analytical tool for in vitro detection of mammalian enzyme-mediated formation of reactive metabolites. Arch. Toxicol. 39: 159–169
GunsalusIC, MeeksJR, LipscombJD, DebrunnerP & MünckE (1974) In: HayaishiO (Ed) Molecular Mechanisms of Oxygen Activation: Bacterial Monooxygenases — The P-450 Cytochrome system (pp 559–613) Academic Press, New York.
HanzlickRP (1981) Reactivity and toxicity among halogenated methanes and related compounds. Biochem. Pharmacol. 30: 3027–3030
HardmanDJ (1991) Biotransformations of halogenated compounds. CRC Crit. Rev. in Biotech. 11: 1–40
HartmansS, SchmuckleA, CookAM & LeisingerT (1986) Methyl chloride: naturally ocurring toxicant and C-1 growth substrate. J. Gen. Microbiol. 132: 1139–1142
HineJ, DowellAM & SingleyJE (1956) Carbon dihalides as intermediates in the basic hydrolysis of haloforms. IV Relative reactivities of haloforms. J. Am. Chem. Soc. 78: 479–482
Holliger C (1992) Reductive dehalogenation by anaerobic bacteria. Ph.D. dissertation, Wageningen Agricultural University, The Netherlands
JakobyWB & KeenJH (1977) A triple threat in detoxification: the glutathione S-transferases. Trends Biochem. Sci. 2: 229–231
JencksWP (1975) In: MeisterA (Ed) Advances in enzymology and related areas of molecular biology 43: 219. John Wiley & Sons, New York
KeenJH, HabigWH & JakobyWB (1976) Mechanism for the several activities of the glutathione S-transferases. J. Biol. Chem. 251: 6183–6188
KleckaGM & GonsiorSJ (1984) Reductive dechlorination of chlorinated methanes and ethanes by reduced iron(II) porphyrins. Chemosphere 13: 391–402
Kohler-StaubD, HartmansS, GälliR, SuterF & LeisingerT (1986) Evidence for identical dichloromethane dehalogenases in different methylotrophic bacteria. J. Gen. Microbiol. 132: 2837–2843
Kohler-StaubD & LeisingerT (1985) Dichloromethane dehalogenase of Hyphomicrobium sp. strain DM2. J. Bacteriol. 162: 676–681
KroneUE & ThauerRK (1992) Dehalogenation of trichlorofluoromethane (CFC-11) by Methanosarcina barkeri. FEMS Microbiol. Lett. 90: 201–204
KroneUE, LauferK, ThauerRK & HogenkampHPC (1989a) Coenzyme F430 as a possible catalyst for the reductive dehalogenation of chlorinated hydrocarbons in methanogenic bacteria. Biochemistry 28: 10061–10065
KroneUE, ThauerRK & HogenkampHPC (1989b) Reductive dehalogenation of chlorinated C1 hydrocarbons mediated by corrinoids. Biochemistry 28: 4908–4914
KroneUE, ThauerRK, HogenkampHPC & SteinbachK (1991) Reductive formation of carbon monoxide from CCl4 and Freons 11, 12, and 13 catalyzed by corrinoids. Biochemistry 30: 2713–2719
LamT & VilkerVL (1987) Biodehalogenation of bromotrichloromethane and 1,2- dibromo-3-chloropropane by Pseudomonas putida G786. Biotechnol. Bioeng. 29: 151–159
LaRocheSA & LeisingerT (1990) Sequence analysis and expression of the bacterial dichloromethane dehalogenase structural gene, a member of the glutathione S-transferase supergene family. J. Bacteriol. 172: 164–171
LcuschnerF, NewmanBW & HuebscherF (1983) Report on subacute toxicological studies with several fluorocarbons in rats and dogs by inhalation. Arzneim.-Forsch. 33: 1475–1476
LiuS, ZhangP, XinhuaJ, JohnsonWW, GillilandGL & ArmstrongRN (1992) Contribution of tyrosine 6 to the catalytic mechanism of isozyme 3–3 of glutathione S-transferase. J. Biol. Chem. 267: 4296–4299
Logan MSP, Newman LM, Schanke CA & Wackett LP (1992) Co-substrate effects in reductive dehalogenation by Pseudomonas putida G786 expressing cytochrome P-450CAM. Biodegradation (submitted)
LukeBT & LoewGH (1986) A theoretical investigation of the first step in the metabolic reduction of halogenated methanes by cytochrome P-450. Internat. J. Quant. Chem.: Quant. Biol. Symp. 12: 99–112
MabeyW & MillT (1978) Critical review of hydrolysis of organic coumpounds in water under environmental conditions. J. Phys. Chem. Ref. Data 7: 383–415
MarchJ (1985) Advanced organic chemistry: reactions, mechanisms and structure. John Wiley & Sons, New York
MeyerDJ, ColesB, PembleSE, GilmoreKS, FraserGM & KettererB (1991) Theta, a new class of glutathione transferases purified from rat and man. Biochem. J. 274: 409–414
MeyerO & SchlegelHG (1983) Biology of aerobic carbon monoxide-oxidizing bacteria. Ann. Rev. Microbiol. 37: 277–310
MikesellMD & BoydSA (1990) Dechlorination of chloroform by Methanosarcina strains. Appl. Environ. Microbiol. 56: 1198–1201
Moelwyn-HughesEA (1949) Kinetics of certain reactions between methyl halides and anions in water. Proc. Royal Soc. (London) Ser. A 196: 540–553
MohnWW & TiedjeJM (1990) Strain DCB-1 conserves energy for growth from reductive dehalogenation coupled to formate oxidation. Arch. Microbiol. 153: 267–271
MohnWW & TiedjeJM (1992) Microbial reductive dehalogenation Microbiol. Rev. 56: 482–507
NeidlemanSL & GeigertJ (1986) Biohalogenation: Principles, Basic Roles and Applications. Ellis Horwood Ltd, Chichester, UK
OldenhuisR, OedzesJY, van derWaardeJJ & JanssenDB (1991) Kinetics of chlorinated hydrocarbon degradation by Methylosinus trichorsporium OB3b and toxicity of trichloroethylene. Appl. Environ. Microbiol. 57: 7–14
PatelRN, HouCT, LaskinAI & FelixA (1982) Microbial oxidation of hydrocarbons: properties of a soluble methane monooxygenase from a facultative methane-utilizing organism, Methylobacterium sp. strain CRL-26. Appl. Environ. Microbiol. 44: 1130–1137
PfaltzA, JuanB, FasslerA, EschenmoserA, JaenchenR, GillesHH, DiekertG & ThauerRK (1982) Zur kenntnis des faktors F430 aus Methanogenen Bakterien: Struktur des pophinoiden Ligandsystems. Helv. Chim. Acta 65: 828–865
PoulosTL, FinzelBC, GunsalusIC, WagnerGC & KrautJ (1985) The 2.6 Å crystal structure of Pseudomonas putida cytochrome P-450. J. Biol. Chem. 260: 16122–16130
PoulosTL & RaagR (1992) Cytochrome P-450CAM: crystallography, oxygen activation, and electron transfer. FASEB J. 6: 674–679
RagsdaleSW & WoodHG (1985) Acetate biosynthesis by acetogenic bacteria. J. Biol. Chem. 260: 3970–3977
RasmussenRA, KhalilMAR & DallugeRW (1980) Concentration and distribution of methyl chloride in the atmosphere. J. Geophys. Res. 85: 7350–7356
RaybuckSA, BastianNR, ZydowskyLD KobayashiK, FlossHG, Orme-JohnsonWH & WalshCT (1987) Nickel containing CO dehydrogenase catalyzes reversible decarbonylation of acetyl CoA with retention of stereochemistry at the methyl group. J. Am. Chem. Soc. 109: 3171–3173
ReinemerP, DirrHW, LadensteinR, SchafferJ, GallayO & HuberR (1991) The three dimensional structure of class π glutathione S-transferase in complex with glutathione sulfonate at 2.3 Å resolution. EMBO J. 10: 1997–2005
Roberts AL (1991) Dehalogenation reactions of polyhalogenated alkanes in aquatic environments. Ph. D. Dissertation Massachusetts Institute of Technology
Roberts AL & Gschwend PM (1992) Nucleophilic substitution reactions of dihalomethanes with the bisulfide ion HS-. Environ. Sci. Technol. (in press)
SchankeCA & WackettLP (1992) Environmental reductive elimination reactions of polychlorinated ethanes mimicked by transition-metal coenzymes. Environ. Sci. Technol. 26: 830–833
ScholtzR, WackettLP, EgliC, CookAM & LeisingerT (1988) Dichloromethane dehalogenase with improved catalytic activity isolated from a fast growing dichloromethane-utilizing bacterium. J. Bacteriol. 170: 5698–5704
SchrauzerGN & Deutsch (1969) Reactions of cobalt(I) supernucleophiles. The alkylation of vitamin B12s, cobaloximes(I) and related compounds. J. Am. Chem. Soc. 91: 3341–3350
SligarSG, FilipovicD & StaytonPS (1991) Mutagenesis of cytochrome P-450CAM and b 5. Met. Enzymol206: 31–49
SligarSG & GunsalusIC (1976) A thermodynamic model of regulation: modulation of redox equilibria in camphor monooxygenase. Proc. Natl. Acad. Sci. USA 73: 1078–1082
SmithRF & SmithTF (1990) Automatic generation of primary sequence patterns from sets of related sequences. Proc. Natl. Acad. Sci. USA 87: 118–122
StromeyerSA, WinkelbauerW, KohlerH, CookAM & LeisingerT (1991) Dichloromethane utilized by an anaerobic mixed culture: acetogenesis and methanogenesis. Biodegradation 2: 129–137
StuckiG, BrunnerW, StaubD, & LeisingerT (1981a) Microbial degradation of chlorinated C1 and C2 hydrocarbons. In: LeisingerT & CookAM (Eds) Microbial Degradation of Xenobiotics and Recalcitrant Compounds (pp 131–137). Academic Press, New York
StuckiG, GälliR, EbersoldHR & LeisingerT. (1981b) Dehalogenation of dichloromethane by cell extracts of Hyphomicrobium DM2. Arch. Microbiol. 130: 366–371
TiedjeJM, BoydSA & FathepureBZ (1987) Anaerobic degradation of chlorinated aromatic compounds. Dev. Ind. Microbiol. 27: 117–127
TrauneckerJ, PreubA & DiekertG (1991) Isolation and characterization of a methyl chloride utilizing strictly anaerobic bacterium. Arch. Microbiol. 156: 416–421
VanelliT, LoganM, ArcieroDM, & HooperAB (1990) Degradation of halogenated aliphatic compounds by the ammoniaoxidizing bacterium Nitrosomonas europaea. Appl. Environ. Microbiol. 56: 1169–1171
VogelTM, CriddleCS & McCartyPL (1987) Transformations of halogenated aliphatic compounds. Environ. Sci. Technol. 21: 711–736
WadeRS & CastroCE (1973) Oxidation of iron(II) porphyrins by alkyl halides. J. Am. Chem. Soc. 95: 226–230
WalshCT (1979) Enzymatic Reaction Mechanisms (pp 24–48). WH Freeman & Company, San Francisco
WolfCR, KingLJ & ParkeDV (1978) The anaerobic dechlorination of trichlorofluoromethane by rat liver preparations in vitro. Chem.-Biol. Interact. 21: 277–288
WolfCR, MansuyD, NastaincyzkW, DeutschmannG & UllrichV (1977) The reduction of polyhalogenated methanes by liver microsomal P-450. Mol. Pharmacol. 13: 698–705
WolfeRS (1985) Unusual coenzymes of methanogenesis. Trends Biochem. Sci. 10: 396–399
WoodJM, KennedyFS & WolfeRS (1968) The reaction of multihalogenated hydrocarbons with free and bound reduced vitamin B12. Biochemistry 7: 1707–1713
WoodJM, MouraI, MouraJJG, SantosMH, XavierAV, LeGallJ & ScandellariM (1982) Role of vitamin B12 in methyl transfer for methane biosynthesis of Methanosarcina barkeri. Science 216: 303–305
WuosmaaAM & HagerLP (1990) Methyl chloride transferase: a carbocation route for the synthesis of halometabolites. Science 249: 160–162
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wackett, L.P., Logan, M.S.P., Blocki, F.A. et al. A mechanistic perspective on bacterial metabolism of chlorinated methanes. Biodegradation 3, 19–36 (1992). https://doi.org/10.1007/BF00189633
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00189633