Skip to main content
Log in

Biodegradation of bis(1-chloro-2-propyl) ether via initial ether scission and subsequent dehalogenation by Rhodococcus sp. strain DTB

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Rhodococcus sp. strain DTB (DSM 44534) grows on bis(1-chloro-2-propyl) ether (DDE) as sole source of carbon and energy. The non-chlorinated diisopropyl ether and bis(1-hydroxy-2-propyl) ether, however, did not serve as substrates. In ether degradation experiments with dense cell suspensions, 1-chloro-2-propanol and chloroacetone were formed, which indicated that scission of the ether bond is the first step while dehalogenation of the chlorinated C3-compounds occurs at a later stage of the degradation pathway. Inhibition of ether scission by methimazole suggested that the first step in degradation is catalyzed by a flavin-dependent enzyme activity. The non-chlorinated compounds 1,2-propanediol, hydroxyacetone, lactate, pyruvate, 1-propanol, propanal, and propionate also supported growth, which suggested that the intermediates 1,2-propanediol and hydroxyacetone are converted to pyruvate or to propionate, which can be channeled into the citric acid cycle by a number of routes. Total release of chloride and growth-yield experiments with DDE and non-chlorinated C3-compounds suggested complete biodegradation of the chlorinated ether.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3a–c.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

Abbreviations

AMO :

Ammonia monooxygenase

DDE :

Bis(1-chloro-2-propyl) ether (2,2′-dichlorodiisopropyl ether)

TC-FDM :

Two-component non-heme flavin-diffusible monooxygenase

sMMO :

Soluble methane monooxygenase

TMO :

Toluene 2-monooxygenase

Y x/c :

Yield of biomass (g dry weight/g carbon)

References

  • Abbott BJ, Clamen A (1973) The relationship of substrate, growth rate and maintenance coefficient to single cell protein production. Biotechnol Bioeng 15:117–127

    Google Scholar 

  • Armfield SJ, Sallis PJ, Baker PB, Bull AT, Hardman DJ (1995) Dehalogenation of haloalkanes by Rhodococcus erythropolis Y2. The presence of an oxygenase-type dehalogenase activity complements that of a halidohydrolase activity. Biodegradation 6:237–246

    CAS  PubMed  Google Scholar 

  • Arp DJ, Sayavedra-Soto LA, Hommes NG (2002) Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea. Arch Microbiol 178:250–255 DOI 10.1007/s00203–002–0452–0

    Article  CAS  PubMed  Google Scholar 

  • Becker D, Schraeder T, Andreesen JR (1997) Two-component flavin-dependent pyrrole-2-carboxylate monooxygenase from Rhodococcus sp. Eur J Biochem 249:739–747

    CAS  PubMed  Google Scholar 

  • Bernhardt D, Diekmann H (1991) Degradation of dioxane, tetrahydrofuran and other cyclic ethers by an environmental Rhodococcus strain. Appl Microbiol Biotechnol 36:120–123

    CAS  PubMed  Google Scholar 

  • De Bont JAM, van Dijken JP, van Ginkel KG (1982) The metabolism of 1,2-propanediol by the propylene oxide utilizing bacterium Nocardia A60. Biochim Biophys Acta 714:465–470

    Google Scholar 

  • Ensign SA, Hyman MR, Arp DJ (1993) In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. J Bacteriol 175:1971–1980

    CAS  PubMed  Google Scholar 

  • Ferguson GP, Tötemeyer S, MacLean MJ, Booth IR (1998) Methylglyoxal production in bacteria: suicide or survival? Arch Microbiol 170:209–218

    Article  CAS  PubMed  Google Scholar 

  • Fetzner S (1998) Bacterial dehalogenation. Appl Microbiol Biotechnol 50:633–657

    Article  CAS  PubMed  Google Scholar 

  • Franζois A, Mathis H, Godefroy D, Piveteau P, Fayolle F, Monot F (2002) Biodegradation of methyl tert-butyl ether and other fuel oxygenates by a new strain, Mycobacterium austroafricanum IFP 2012. Appl Environ Microbiol 68:2754–2762

    Article  PubMed  Google Scholar 

  • Franke S, Hildebrandt S, Francke W, Reincke H (1995) The occurance of chlorinated bis-(propyl) ethers in the Elbe River and tributaries. Naturwissenschaften 82:80–83

    Article  CAS  Google Scholar 

  • Galan B, Diaz E, Prieto MA, Garcia JL (2000) Functional analysis of the small component of the 4-hydroxyphenylacetate 3-monooxygenase of Escherichia coli W: a prototype of a new flavin:NAD(P)H reductase subfamily. J Bacteriol 182:627–636

    Article  CAS  PubMed  Google Scholar 

  • Green J, Prior SD, Dalton H (1985) Copper ions as inhibitors of protein C of soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 153:137–144

    CAS  PubMed  Google Scholar 

  • Grothusen A, Hardt J, Bräutigam L, Lang D, Böcker R (1996) A convenient method to discriminate between cytochrome P450 enzymes and flavin-containing monooxygenases in human liver microsomes. Arch Toxicol 71:64–71

    Article  CAS  PubMed  Google Scholar 

  • Hardison LK, Curry SS, Ciuffetti LM, Hyman MR (1997) Metabolism of diethyl ether and cometabolism of methyl tert-butyl ether by a filamentous fungus, a Graphium sp. Appl Environ Microbiol 63:3059–3067

    CAS  Google Scholar 

  • Hauck R, Adrian L, Wendler P, Amidjojo M, Hegemann W, Görisch H (2001) Transformation of 2,2'-dichlorodiisopropyl ether in mixed and pure culture. Appl Microbiol Biotechnol 56:491–495 DOI 10.1007/s002530100659

    Article  CAS  PubMed  Google Scholar 

  • Hur HG, Newman LM, Wackett LP, Sadowsky MJ (1997) Toluene 2-monooxygenase-dependent growth of Burkholderia cepacia G4/PR1 on diethyl ether. Appl Environ Microbiol 63:1606–1609

    CAS  Google Scholar 

  • Hyman MR (1999) Final report: Aerobic cometabolism of ether-bonded compounds. National Center for Environmental Research. EPA Grant Number: R823426

    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 60:3033–3035

    CAS  PubMed  Google Scholar 

  • International Agency for Research on Cancer (IARC) (1987) IARC monographs on the evaluation of carcinogenic risk of chemicals to humans; overall evaluation of carcinogenicity: an updating of IARC monographs, volumes 1–42, Supplement 7, IARC, Lyon, p. 59

    Google Scholar 

  • Janssen DB, Gerritse J, Brackman J, Kalk C, Jager D, Witholt B (1988) Purification and characterization of a bacterial dehalogenase with activity toward halogenated alkanes, alcohols and ethers. Eur J Biochem 171:67–72

    CAS  PubMed  Google Scholar 

  • Kadiyala V, Spain JC (1998) A two-component monooxygenase catalyzes both the hydroxylation of p-nitrophenol and the oxidative release of nitrite from 4-nitrocatechol in Bacillus sphaericus JS905. Appl Environ Microbiol 64:2479–2484

    CAS  PubMed  Google Scholar 

  • Kawamoto K, Urano K (1990) Parameters for predicting fate of organochlorine pesticides in the environment (III). Biodegradation rate constants. Chemosphere 21:1141–1152

    CAS  Google Scholar 

  • Kharoune M, Kharoune L, Lebeault JM, Pauss A (2001) Isolation and characterization of two aerobic bacterial strains that completely degrade ethyl tert-butyl ether (ETBE). Appl Microbiol Biotechnol 55:348–353 DOI 10.1007/s002530000528

    Article  CAS  PubMed  Google Scholar 

  • Lei B, Tu SC (1996) Gene overexpression, purification, and identification of a desulfurization enzyme from Rhodococcus sp strain IGTS8 as a sulfide/sulfoxide monooxygenase. J Bacteriol 178:5699–5705

    CAS  PubMed  Google Scholar 

  • Leisinger T, Bader R (1993) Microbial dehalogenation of synthetic organohalogen compounds: hydrolytic dehalogenases. Chimia 47:116–121

    CAS  Google Scholar 

  • Martin-Le Garrec G, Artaud I, Capeillere-Blandin C (2001) Purification and catalytic properties of the chlorophenol 4-monooxygenase from Burkholderia cepacia strain AC1100. Biochim Biophys Acta 1547:288–301

    PubMed  Google Scholar 

  • Matsubara T, Ohshiro T, Nishina Y, Izumi Y (2001) Purification, characterization, and overexpression of flavin reductase involved in dibenzothiophene desulfurization by Rhodococcus erythropolis D-1. Appl Environ Microbiol 67:1179–1184

    PubMed  Google Scholar 

  • Nishio N, Kawagishi T, Matsuno R, Kamikubo T (1978) Metabolism of 1,2-propanediol by methanol-utilizing bacteria and some properties of 1,2-propanediol dehydrogenating enzyme. Agric Biol Chem 42:1095–1100

    CAS  Google Scholar 

  • OEHHA, USA, (2002) Evidence on the carcinogenicity of technical grade bis (2-chloro-1-methylethyl) ether. http://www.oehha.ca.gov/prop65/prop65_list/062802LSTc.pdf

  • Patterson JW, Kodukula PS (1981) Emission and effluent control: Biodegradation of hazardous organic pollutants. Chem Eng Prog 77:48–55

    CAS  Google Scholar 

  • Plinke E, Schüssler R, Kämpf K (1994) Konversion Chlorchemie. Hessisches Ministerium für Umwelt, Energie und Bundesangelegenheiten, Eigendruck, Wiesbaden

  • Sallis PJ, Armfield SJ, Bull AT, Hardman DJ (1990) Isolation and characterization of a haloalkane halidohydrolase from Rhodococcus erythropolis Y2. J Gen Microbiol 136:115–120

    CAS  PubMed  Google Scholar 

  • Steffan JR, McClay K, Vainberg S, Condee WC, Zhang D (1997) Biodegradation of the gasoline oxygenates methyl tert-butyl ether, ethyl tert-butyl ether, and tert-amyl methyl ether by propane-oxidizing bacteria. Appl Environ Microbiol 63:4216–4222

    CAS  PubMed  Google Scholar 

  • Stirling DI, Dalton H (1980) Oxidation of dimethyl ether methyl formate and bromomethane by Methylococcus capsulatus (Bath). J Gen Microbiol 116:277–283

    CAS  Google Scholar 

  • Testa B, Jenner P (1981) Inhibitors of cytochrome P450s and their mechanism of action. Drug Metab 12:1-117

    CAS  PubMed  Google Scholar 

  • Textor S, Wendisch VF, De Graaf AA, Müller U, Linder MI, Linder D, Buckel W (1997) Propionate oxidation in Escherichia coli: evidence for operation of a methylcitrate cycle in bacteria. Arch Microbiol 168:428–436

    Article  CAS  PubMed  Google Scholar 

  • Thiemer B, Andreesen JR, Schrader T (2001) The NADH-dependent reductase of a putative multicomponent tetrahydrofuran mono-oxygenase contains a covalently bound FAD. Eur J Biochem 268:3774–3782

    Article  CAS  PubMed  Google Scholar 

  • Tomasi I, Artaud I, Bertheau Y, Mansuy D (1995) Metabolism of polychlorinated phenols by Pseudomonas cepacia AC1100: determination of the first two steps and inhibitory effect of methimazole. J Bacteriol 177:307–311

    CAS  PubMed  Google Scholar 

  • Van den Wijngaard AJ, Prins J, Smal AJAC, Janssen DB (1993) Degradation of 2-chloroethylvinylether by Ancylobacter aquaticus AD25 and AD27. Appl Environ Microbiol 59:2777–2783

    Google Scholar 

  • White GF, Russell NJ, Tidswell EC (1996) Bacterial scission of etherbonds. Microbiol Rev 60:216–232

    CAS  PubMed  Google Scholar 

  • Yeager CM, Bottomley PJ, Arp DJ, Hyman MR (1999) Inactivation of toluene 2-monooxygenase in Burkholderia cepacia G4 by alkynes. Appl Environ Microbiol 65:632–639

    CAS  PubMed  Google Scholar 

  • Ziegler DM (1993) Recent studies on the structure and function of multisubstrate flavin-containing monnooxygenases. Annu Rev Pharmacol Toxicol 33:179–199

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. U. Kretzschmar for her continuous interest in this work and for helpful discussions. Dr. H. Schulz is acknowledged for his help with analytical problems and we are grateful to W. Poppe for skillful technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Helmut Görisch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moreno Horn, M., Garbe, LA., Tressl, R. et al. Biodegradation of bis(1-chloro-2-propyl) ether via initial ether scission and subsequent dehalogenation by Rhodococcus sp. strain DTB. Arch Microbiol 179, 234–241 (2003). https://doi.org/10.1007/s00203-003-0522-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-003-0522-y

Keywords

Navigation