Skip to main content
SpringerLink
Log in

Versatility of soil column experiments to study biodegradation of halogenated compounds under environmental conditions

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

Soil column experiments were performed to obtain insight in the different biological and physico-chemical processes affecting biodegradation of halogenated compounds under natural conditions in a water infiltration site. Lower chlorinated aromatic compounds could be degraded under aerobic conditions, whereas highly chlorinated compounds and chlorinated aliphatic compounds were mainly transformed under anaerobic conditions. Microorganisms which derive energy from reductive dechlorination were enriched and characterized. It was found that microbes could adapt to using chlorinated benzenes by evolution of new enzyme specificities and by exchange of genetic material. For halogenated pollutants, which are generally hydrophobic, sorption processes control the concentration available for biodegradation. The effects of very low concentrations of halogenated compounds on their biodegradability are described. The use of isolated bacterial strains to enhance biodegradation was evaluated with respect to their temperature-related activity and to their adhesion properties.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

3-CB:

3-chlorobenzoate

DCB:

dichlorobenzene

HCH:

hexachlorocyclohexane

IS:

insertion sequence

PER:

tetrachloroethylene

Smin :

minimal substrate concentration for growth

TCB:

trichlorobenzene

TRI:

trichloroethylene

λ:

filtration coefficient

References

  • Aelion CM, Swindoll CM & Pfaender FK (1987) Adaptation to and biodegradation of xenobiotic compounds by microbial communities from a pristine aquifer. Appl. Environ. Microbiol. 53: 2212–2217

    Google Scholar 

  • Alexander M (1985) Biodegradation of organic chemicals. Environ. Sci. Technol. 18: 106–111

    Google Scholar 

  • Bachmann A, de Bruin WP, Jumelet JC, Rijnaarts HHM & Zehnder AJB (1988) Aerobic mineralization of alpha-hexachlorocyclohexane in contaminated soil. Appl. Environ. Microbiol. 54: 548–554

    Google Scholar 

  • Barkay T & Pritchard H (1988) Adaptation of aquatic microbial communities to pollutant stress. Microbiol. Sci. 5: 165–169

    Google Scholar 

  • Bartels I, Knackmuss H-J & Reineke W (1984) Suicide inactivation of catechol 2,3-dioxygenase from Pseudomonas putidamt-2 by 3-halocatechols. Appl. Environ. Microbiol. 47: 500–505

    Google Scholar 

  • Bosma TNP, Holliger C, van Neerven ARW, Schraa G & Zehnder AJB (1988a) Reductive dechlorination of chlorinated hydrocarbons in anaerobic sediment columns. In: Wolf K, van den Brink WJ & Colon FJ (Eds) Contaminated Soil '88 (pp 731–732). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Bosma TNP, Schnoor JL, Schraa G & Zehnder AJB (1988b) Simulation model for biotransformation of xenobiotics and chemotaxis in soil columns. J. Contam. Hydrol. 2: 225–236

    Google Scholar 

  • Bosma TNP, van der Meer JR, Schraa G, Tros ME & Zehnder AJB (1988c) Reductive dechlorination of all trichloro- and dichlorobenzene isomers. FEMS Microbiol. Ecol. 53: 223–229

    Google Scholar 

  • Bosma TNP, te Welscher RAG, Schraa G, Smeenk JGMM & Zehnder AJB (1991) Microbial aspects of the behaviour of chlorinated compounds during soil passage. In: Angeletti G and Bjorseth A (Eds) Organic Micropollutants in the Aquatic Environment (pp 184–192). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Bosma TNP, te Welscher RAG, Smeenk JGMM, Ballemans EMW, Hoekstra NK, Schraa G & Zehnder AJB (in preparation) Biotransformation of organic contaminants in a dune infiltration area and in sediment columns.

  • Broderick JB & O'Halloran TV (1991) Overproduction, purification, and characterization of chlorocatechol dioxygenase, a non-heme iron dioxygenase with broad substrate tolerance. Biochemistry 30: 734–7358

    Google Scholar 

  • Carney BF, Kröckel L, Leary JV & Focht DD (1989) Identification of Pseudomonas alcaligenes chromosomal DNA in the plasmid DNA of the chlorobenzene-degrading recombinant Pseudomonas putida strain CB1–9. Appl. Environ. Microbiol. 55: 1037–1039

    Google Scholar 

  • Chaudry GR & Chapalamadugu S (1991) Biodegradation of halogenated organic compounds. Microbiol. Rev. 55: 59–79

    Google Scholar 

  • Chesbro W, Evans T & Eifert R (1979) Very slow growth of Escherichia coli. J. Bacteriol. 139: 625–638

    Google Scholar 

  • Commandeur LCM & Parsons JR (1990) Degradation of halogenated aromatic compounds. Biodegradation 1: 207–220

    Google Scholar 

  • de Bruin WP, Kottermann MJJ, Posthumus MA, Schraa G & Zehnder AJB (1992) Complete biological reductive transformation of tetrachloroethene to ethane. Appl. Environ. Microbiol. 58: 1996–2000

    Google Scholar 

  • Don RH & Pemberton JM (1981) Properties of six pesticide degradation plasmids isolated from Alcaligenes paradoxus and Alcaligenes eutrophus. J. Bacteriol. 145: 681–686

    Google Scholar 

  • Faulkner DJ (1980) Natural organohalogen compounds. In: Hutzinger O (Ed) The Handbook of Environmental Chemistry, 1A. The Natural Environment and the Biogeochemical Cycles. Springer Verlag, New York

    Google Scholar 

  • Fortnagel P, Harms H, Wittich R-M, Krohn S, Meyer H, Sinnwell V, Wilkes H & Francke W (1990) Metabolism of dibenzofuran by Pseudomonas sp. strain HH69 and the mized culture HH27. Appl. Environ. Microbiol. 56: 1148–1156

    Google Scholar 

  • Frantz B & Chakrabarty AM (1987) Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc. Natl. Acad. Sci. USA. 84: 4460–4464

    Google Scholar 

  • Furukawa K, Matsumura F & Tonomura K (1978) Alcaligenes and Acinetobacter strains capable of degrading polychlorinated biphenyls. Agric. Biol. Chem. 42: 543–548

    Google Scholar 

  • Gibson DT, Zylstra GJ & Chauhan SS (1990) Biotransformations catalyzed by toluene dioxygenase from Pseudomonas putida F1. In: Silver S, Chakrabarty AM, Iglewski B & Kaplan S (Eds) Pseudomonas: Biotransformations, Pathogenesis and Evolving Biotechnology (pp 121–133). American Society for Microbiology, Washington, DC

    Google Scholar 

  • Goldstein RM, Mallory LM & Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Appl. Environ. Microbiol. 50: 977–983

    Google Scholar 

  • Haggblom M (1990) Mechanisms of bacterial degradation and transformation of chlorinated monoaromatic compounds. J. Basic. Microbiol. 30: 115–141

    Google Scholar 

  • Harayama S & Rekik M (1989) Bacterial aromatic ring-cleavage enzymes are classified into two different gene families. J. Biol. Chem. 264: 15328–15333

    Google Scholar 

  • Harnett C, Neidle EL, Ngai K-L & Ornston LN (1990) DNA sequences of genes encoding Acinetobacter calcoaceticus protocatechuate 3,4-dioxygenase: evidence indicating shuffling of genes and of DNA sequences within genes during their evolutionary divergence. J. Bacteriol. 172: 95–966

    Google Scholar 

  • Holliger C (1992) Reductive dehalogenation by anaerobic bacteria. Ph.D. Thesis, Wageningen Agricultural University, Wageningen, The Netherlands

  • Holliger C, Schraa G, Stams AJM & Zehnder AJB (1992) Enrichment and properties of an anaerobic mixed culture reductively dechlorinating 1,2,3-trichlorobenzene to 1,3-dichlorobenzene. Appl. Environ. Microbiol. 58: 1636–1944

    Google Scholar 

  • Huntjens JM, Brouwer W, Grobben K, Jansma O, Scheffer F & Zehnder AJB (1988) Biodegradation of α-hexachlorocyclohexane by a bacterium isolated from polluted soil. In: Wolf K, van den Brink W J & Colon FJ (Eds) Contaminated Soil '88. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Karns JS, Kilbane JJ, Duttagupta S & Chakrabarty AM (1983) Metabolism of halophenols by 2,4,5-trichlorophenoxyacetic acid-degrading Pseudomonas cepacia. Appl. Environ. Microbiol. 46: 1176–1181

    Google Scholar 

  • Klein TM & Alexander M (1986) Bacterial inhibitors in lake water. Appl. Environ. Microbiol. 52: 114–118

    Google Scholar 

  • Kröckel L & Focht DD (1987) Construction of chlorbenzene-utilizing recombinants by progenitive manifestation of a rare event. Appl. Environ. Microbiol. 53: 2470–2475

    Google Scholar 

  • Kuhm AE, Schlömann M, Knackmuss H-J & Pieper DH (1990) Purification and characterization of dichloromuconate cycloisomerase from Alcaligenes eutrophus JMP134. Biochem. J. 266: 877–883

    Google Scholar 

  • Latorre J, Reineke W & Knackmuss H-J (1984) Microbial metabolism of chloroanilines: enhanced evolution by naturally genetic exchange. Arch. Microbiol. 140: 159–165

    Google Scholar 

  • Lehrbach PR, Zeyer J, Reineke W, Knackmuss H-J & Timmis KN (1984) Enzyme recruitment in vitro: use of cloned genes to extend the range of haloaromatics degraded by Pseudomonas sp. strain B13. J. Bacteriol. 158: 1025–1032

    Google Scholar 

  • Mondello FJ (1989) Cloning and expression in Escherichia coli of Pseudomonas strain LB400 genes encoding polychlorinated biphenyl degradation. J. Bacteriol. 171: 1725–1732

    Google Scholar 

  • Neidle EL, Hartnett C, Bonitz S & Ornston LN (1988) DNA sequence of the Acinetobacter calcoaceticus catechol 1,2-dioxygenase I structural gene catA: evidence for evolutionary divergence of intradiol dioxygenases by acquisition of DNA sequence repetitions. J. Bacteriol. 170: 4874–4880

    Google Scholar 

  • Neilson AH (1990) The biodegradation of halogenated organic compounds-a review. J. Appl. Bacteriol. 69: 445–470

    Google Scholar 

  • Ngai K-L & Ornston LN (1988) Abundant expression of Pseudomonas genes for chlorocatechol metabolism. J. Bacteriol. 170: 2412–2413

    Google Scholar 

  • Oltmanns RH, Rast HG & Reineke W (1988) Degradation of 1,4-dichlorobenzene by constructed and enriched strains. Appl. Microbiol. Biotechnol. 28: 609–616

    Google Scholar 

  • Ornston LN, Houghton J, Neidle EL & Gregg LA (1990) Subtle selection and novel mutation during evolutionary divergence of the β-ketoadipate pathway. In: Silver S, Chakrabarty AM, Iglewski B & Kaplan S (Eds) Pseudomonas: Biotransformations, Pathogenesis and Evolving Biotechnology (pp 207–225). American Society for Microbiology, Washington, DC

    Google Scholar 

  • Pearson CR (1982) C1 and C2 halocarbons. In: Hutzinger O (Ed) The Handbook of Environmental Chemistry, 3B (pp 69–88). Springer Verlag, New York

    Google Scholar 

  • Perkins EJ, Gordon MP, Caceres O & Lurquin PF (1990) Organization and sequence analysis of the 2,4-dichlorophenol hydroxylase and dichlorocatechol oxidative operons of plasmid pJP4. J. Bacteriol. 172: 2351–2359

    Google Scholar 

  • Pieper DH, Kuhm AE, Stadler-Fritzche K, Fischer P & Knackmuss H-J (1991) Metabolization of 3,5-dichlorocatechol by Alcaligenes eutrophus JMP 134. Arch. Microbiol. 156: 218–222

    Google Scholar 

  • Pirt SJ (1975) Principles of Microbe and Cell Cultivation. Blackwell Scientifc Publications, Oxford

    Google Scholar 

  • Reineke W & Knackmuss H-J (1984) Microbial metabolism of haloaromatics: isolation and properties of a chlorobenzenedegrading bacterium. Appl. Environ. Microbiol. 47: 395–402

    Google Scholar 

  • Reineke W & Knackmuss H-J (1988) Microbial degradation of haloaromatics. Annu. Rev. Microbiol. 42: 263–287

    Google Scholar 

  • Rijnaarts H, Norde W, Bouwer E, Lyklema J & Zehnder AJB (in preparation) Reversibility of bacterial adhesion: studies with various strains of Pseudomonas and coryneform bacteria

  • Rijnaarts HHM, Bachmann A, Jumelet JC & Zehnder AJB (1990) Effect of the desorption and intraparticle mass transfer on the aerobic biomineralization of α-hexachlorocyclohexane in a contaminated calcareous soil. Environ. Sci. Technol. 24: 1349–1354

    Google Scholar 

  • Rojo F, Pieper DH, Engesser K-H, Knackmuss H-J & Timmis KN (1987) Assemblage of ortho cleavage route for simultaneous degradation of chloro- and methylaromatics. Science 238: 1395–1398

    Google Scholar 

  • Sander P, Wittich R-M, Fortnagel P, Wilkes H & Francke W (1991) Degradation of 1,2,4-trichloro- and 1,2,4,5-tetrachlorobenzene by Pseudomonas strains. Appl. Environ. Microbiol. 57: 1430–1440

    Google Scholar 

  • Sayler GS, Shields MS, Tedford ET, Breen A, Hooper SW, Sirotkin KM & Davis JW (1985) Application of DNA-DNA colony hybridization to the detection of catabolic genotypes in environmental samples. Appl. Environ. Microbiol. 49: 1295–1303

    Google Scholar 

  • Schlömann M, Pieper DH & Knackmuss H-J (1990) Enzymes of haloaromatics degradation: variations of Alcaligenes on a theme by Pseudomonas. In: Silver S, Chakrabarty AM, Iglewski B & Kaplan S (Eds) Pseudomonas: Biotransformations, Pathogenesis, and Evolving Biotechnology (pp 185–197). American Society for Microbiology, Washington, DC

    Google Scholar 

  • Schmidt E & Knackmuss H-J (1980) Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. Biochem. J. 192: 339–347

    Google Scholar 

  • Schmidt E, Remberg G & Knackmuss H-J (1980) Chemical structure and biodegradability of halogenated aromatic compounds. Halogenated muconic acids as intermediates. Biochem. J. 192: 331–337

    Google Scholar 

  • Schraa G, Bethe B, van Neerven ARW, van den Tweel WJJ, van der Wende E & Zehnder AJB (1987) Degradation of 1,2-dimethylbenzene by Corynebacterium strain C125. Anthonie van Leeuwenhoek 53: 159–170

    Google Scholar 

  • Schraa G, Boone ML, Jetten MSM, van Neerven ARW, Colberg PJ & Zehnder AJB (1986) Degradation of 1,4-dichlorobenzene by Alcaligenes sp. strain A175. Appl. Environ. Microbiol. 52: 1374–1381

    Google Scholar 

  • Schwarzenbach RP & Westall J (1981) Transport of non-polar organic compounds from surface water to groundwater: laboratory sorption studies. Environ. Sci. Technol. 15: 1360–1367

    Google Scholar 

  • Spain JC & Nishino SF (1987) Degradation of 1,4-dichlorobenzene by a Pseudomonas sp. Appl. Environ. Microbiol. 53: 1010–1019

    Google Scholar 

  • Suflita JM, Horowitz A, Shelton DR & Tiedje JM (1982) Dehalogenation: a novel pathway for the anaerobic biodegradation of haloaromatic compounds. Science 218: 1115–1117

    Google Scholar 

  • Swindoll CM, Aelion CM & Pfaender FK (1988) Influence of inorganic and organic nutrients on aerobic biodegradation and on the adaptation response of subsurface microbial communities. Appl. Environ. Microbiol. 54: 212–217

    Google Scholar 

  • van der Meer JR (1992) Molecular mechanisms of adaptation of soil bacteria to chlorinated benzenes. Ph.D. Thesis, Wageningen Agricultural University, Wageningen, The Netherlands

  • van der Meer JR, Roelofsen W, Schraa G & Zehnder AJB (1987) Degradation of low concentrations of dichlorobenzenes and 1,2,4-trichlorobenzene by Pseudomonas sp. strain P51 in nonsterile soil columns. FEMS Microbiol. Ecol. 45: 333–341

    Google Scholar 

  • van der Meer JR, Eggen RIL, Zehnder AJB & de Vos WM (1991a) Sequence analysis of the Pseudomonas sp. strain P51 tcb gene cluster, which encodes metabolism of chlorinated catechols: evidence for specialization of catechol 1,2-dioxygenases for chlorinated substrates. J. Bacteriol. 173: 2425–2434

    Google Scholar 

  • van der Meer JR, van Neerven ARW, de Vries EJ, de Vos WM & Zehnder AJB (1991b) Cloning and characterization of plasmid-encoded genes for the degradation of 1,2-dichloro-, 1,4-dichloro-, and 1,2,4-trichlorobenzene of Pseudomonas sp. strain P51. J. Bacteriol. 173: 6–15

    Google Scholar 

  • van der Meer JR, Zehnder AJB & de Vos WM (1991c) Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51. J. Bacteriol. 173: 7077–7083

    Google Scholar 

  • van der Meer JR, de Vos WM, Harayama S & Zehnder AJB (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol. Rev. 56: 677–694

    Google Scholar 

  • van Loosdrecht MCM, Lyklema J, Norde W, Schraa G & Zehnder AJB (1987a) Electrophoretic mobility and hydrophobicity as a measure to predict the initial steps of bacterial adhesion. Appl. Environ. Microbiol. 53: 1898–1901

    Google Scholar 

  • van Loosdrecht MCM, Lyklema J, Norde W, Schraa G & Zehnder AJB (1987b) The role of bacterial cell wall hydrophobicity in adhesion. Appl. Environ. Microbiol. 53: 1893–1897

    Google Scholar 

  • van Loosdrecht MCM, Lyklema J, Norde W & Zehnder AJB (1989) Bacterial adhesion: a physicochemical approach. Microb. Ecol. 1: 1–15

    Google Scholar 

  • Zeyer J, Wasserfallen A & Timmis KN (1985) Microbial mineralization of ring-substituted anilines through an ortho-cleavage pathway. Appl. Environ. Microbiol. 50: 447–453

    Google Scholar 

Download references

Author information

Author notes

  1. Jan Roelof van der Meer & Alexander J. B. Zehnder

    Present address: EAWAG/ETH, CH-8600, Dübendorf

  2. Christof Holliger

    Present address: EAWAG/ETH, CH-6047, Kastanienbaum, Switzerland

Authors and Affiliations

  1. Department of Microbiology, Wageningen Agricultural University, Hesselink van Suchtelenweg 4, 6703 CT, Wageningen, The Netherlands

    Jan Roelof van der Meer, Tom N. P. Bosma, Wil P. de Bruin, Hauke Harms, Christof Holliger, Huub H. M. Rijnaarts, Marijke E. Tros, Gosse Schraa & Alexander J. B. Zehnder

Authors
  1. Jan Roelof van der Meer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tom N. P. Bosma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wil P. de Bruin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hauke Harms
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christof Holliger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huub H. M. Rijnaarts
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marijke E. Tros
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gosse Schraa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alexander J. B. Zehnder
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Meer, J.R., Bosma, T.N.P., de Bruin, W.P. et al. Versatility of soil column experiments to study biodegradation of halogenated compounds under environmental conditions. Biodegradation 3, 265–284 (1992). https://doi.org/10.1007/BF00129088

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00129088

Key words

Search

Navigation