Skip to main content
Log in

Biodegradation of Dibenzo-p-dioxin, Dibenzofuran, and Chlorodibenzo-p-dioxins by Pseudomonas veronii PH-03

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

The dioxin-degrading strain Pseudomonas veronii PH-03 was isolated from contaminated soil by selective enrichment techniques. Strain PH-03 grew on dibenzo-p-dioxin and dibenzofuran as a sole carbon source. Further, 1-chlorodibenzo-p-dioxin, 2-chlorodibenzo-p-dioxin and other dioxin metabolites, salicylic acid, and catechol were also metabolized well. Resting cells of strain PH-03 transformed dibenzo-p-dioxin, dibenzofuran, 2,2′,3-trihydroxybiphenyl, and some chlorodioxins to their corresponding metabolic intermediates such as catechol, salicylic acid, 2-hydroxy-(2-hydroxyphenoxy)-6-oxo-2,4-hexadienoic acid, and chlorocatechols. The formation of these metabolites was confirmed by comparison of gas chromatography–mass spectrometry (GC–MS) data with those of authentic compounds. Although we did observe the production of 3,4,5,6-tetrachlorocatechol (3,4,5,6-TECC) from 1,2,3,4-tetrachlorodibenzo-p-dioxin (1,2,3,4-TCDD) with resting cell suspensions of PH-03, growth of strain PH-03 in the presence of 1,2,3,4-TCDD was poor. This result suggests that strain PH-03 is unable to utilize 3,4,5,6-TECC, even at very low concentration (0.01 mM) due to its toxicity. In cell-free extracts of DF-grown cells, 2,2′,3-trihydroxybiphenyl dioxygenase, 2-hydroxy-6-oxo-6-phenyl-2,4-hexadienoic acid hydrolase, and catechol-2,3-dioxygense activities were detected. Moreover, the activities of meta-pyrocatechase and 2,2′,3-trihydroxybiphenyl dioxygenase from the crude cell-free extracts were inhibited by 3-chlorocatechol. However, no inhibition was observed in intact cells when 3-chlorocatechol was formed as intermediate.

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.

Similar content being viewed by others

References

  • Adriaens P, Fu Q & Grbic-Galic D (1995) Bioavailabiliy and transformation of highly chlorinated dibenzo-p-dioxins and dibenzofurans in anaerobic soils and sediments. Environ. Sci. Technol. 29: 2252–2250

    Google Scholar 

  • Arfmann HA, Timmis KN & Wittich RM (1997) Mineralization of 4-chlorodibenzofuran by a consortium consisting of Sphingomonas sp strain R WI and Burkholderia sp strain JWS. Appl. Environ. Microbiol. 63: 3458–3462

    Google Scholar 

  • Bartels I, Knackmuss HJ & Reineke W (1984) Suicide inactivation of catechol 2,3-dioxygenase from Pseudomonas putita mt-2 by 3-halocatechols. Appl. Environ. Microbiol. 60: 2884–2889

    Google Scholar 

  • Beurskens JEM, Toussaint M, Wolf J de, Steen JMD van der, Slot PC, Commandeur LCM & Parsons JR (1995) Dehalogenation of chlorinated dioxins by an anaerobic microbial consortium from sediment. Environ. Toxicol. Chern. 14: 939–943

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248–254

    Article  PubMed  Google Scholar 

  • Bunge M, Adrian L, Kraus A, Opel M, Lorenz WG, Andreesen JR, Gorisch H & Lechner U (2003) Reductive dehalogenation of chlorinated dioxins by an anaerobic bacterium. Nature 421: 357–360

    PubMed  Google Scholar 

  • Bünz PV & Cook AM (1993) Dibenzofuran 4,4a-dioxygenase from Sphingomonas sp. strain R WI: angular dioxygenation by a three-component enzyme system. J. Bacteriol. 175: 6467–6475

    PubMed  Google Scholar 

  • Bünz PV & Schmidt S (1997) The microbial degradation of halogenated diaryl ethers. Biotechnol. Adv. 15: 621–632

    PubMed  Google Scholar 

  • Bünz PV, Falchetto R & Cook AM (1993) Purification and characterization of two isofunctional hydro loses in the degradative pathway for dibenzofuran in Sphingomonas sp strain RWI. Biodegradation 4: 171–178

    PubMed  Google Scholar 

  • Cerniglia CE, Morgan JC & Gibson DT (1979) Bacterial and fungal oxidation of dibenzofuran. Biochem J. 180: 175–185

    PubMed  Google Scholar 

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

    Google Scholar 

  • Habe H, Chung JS, Lee JH, Kasuga K, Yoshida T, Nojiri H & Omori T (2001) Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by two types of bacteria having angular dioxygenases with different features. Appl. Environ. Microbiol. 67: 3610–3617

    PubMed  Google Scholar 

  • Halden RU & Dwyer DF (1997) Biodegradation of dioxinrelated compounds: a review. Bioremed. J. I: 11–25

    Google Scholar 

  • Happe B, Eltis LD, Poth H, Hedderich R & Timmis KN (1993) Characterization of 2,2',3-trihydroxybiphenyl dioxygenase, an extradiol dioxygenase from the dibenzofuran-and dibenzo-p-dioxin-degrading bacterium Sphingomonas sp. strain RWI. J. Bacteriol. 175: 7313–7320

    PubMed  Google Scholar 

  • Hong HB, Chang YS, Choi SD & Park YH (1999) Degradation of dibenzofuran by Pseudomonas putida PH-Ol. Water Res. 34: 2404–2407

    Google Scholar 

  • Hong HB, Chang YS, Nam IH, Schmidt S & Fortnagel P (2002) Biotransformation of 2,7-dichloro-and 1,2,3,4-tetrachlorodibenzo-p-dioxin by Sphingomonas wittichii RWI. Appl. Environ. Microbiol. 68: 2584–2588

    PubMed  Google Scholar 

  • Kaschabek SR, Kasberg T, Muller D, Mars AE, Janssen DB & Reineke W (1998) Degradation of chloroaromatics: purification and characterization of novel type of chlorocatechol 2,3dioxygenase of Pseudomonas putida G131. J. Bacteiol. 180: 296–302

    Google Scholar 

  • Keim T, Francke W, Schmidt S & Fortnagel P (1999) Catabolism of 2,7-dichloro-and 2,4,8-trichlorodibenzofuran by Sphingomonas sp. strain RWI. J. Ind. Microbiol. Biotechnol. 23: 359–363

    PubMed  Google Scholar 

  • Kimura N & Urushigawa Y (2001) Metabolism of dibenzo-p-dioxin and chlorinated dibenzo-p-dioxin by a gram-positive bacterium Rhodococcus opacus SAOIOI. J. Biosci. Bioeng. 92: 138–143

    Google Scholar 

  • Klecka GM & Gibson DT (1979) Metabolism of dibenzo-p-dioxin by a Pseudomonas species. Biochem. J. 180: 639–645

    PubMed  Google Scholar 

  • Klecka GM & Gibson DT (1980) Metabolism of dibenzo-p-dioxin and chlorinated dibenzo-p-dioxins by a Beijerinckia species. Appl. Environ. Microbiol. 39: 288–296

    Google Scholar 

  • Klecka GM & Gibson DT (1981) Inhibition of catechol 2,3dioxygenase from Pseudomonas putida by 3-chlorocatechol. Appl. Environ. Microbiol. 41: 1159–1165

    PubMed  Google Scholar 

  • Kohler HP, Schmid A & van der Maarel M (1993) Metabolism of 2,2'-dihydroxybiphenyl by Pseudomonas sp. Strain HBPI: production and consumption of 2,2',3-trihydroxybiphenyl. J. Bacteriol. 175: 1621–1628

    PubMed  Google Scholar 

  • Mars AE, Kasberg T, Kaschabek SR, van Agteren MH, Janssen DB & Reineke W (1997) Microbial degradation of chloroaromatics: use of the meta-cleavage pathway for mineralization of chlorobenzene. J. Bacteriol. 179: 4530–4537

    PubMed  Google Scholar 

  • Mars AE, Kingma J, Kaschabek SR, Reineke W & Janssen DB (1999) Conversion of 3-chlorocatechol by various catechol 2,3-dioxygenases and sequence analysis of the chlorocatechol dioxygenase region of Pseudomonas putida G13I. J. Bacteriol. 181: 1309–1318

    PubMed  Google Scholar 

  • Meharg AA & Osborn D (1995) Dioxins released from chemical accidents. Nature 375: 353–354

    PubMed  Google Scholar 

  • Monna L, Omori T & Kodama T (1993) Microbial degradation of dibenzofuran, fluorene, and dibenzo-p-dioxin by Staphylococcus auriculans DBF63. Appl. Environ. Microbiol. 59: 285–289

    PubMed  Google Scholar 

  • Nam IH, Chang YS, Hong HB & Lee YE (2003) A novel catabolic activity of Pseudomonas veronii in biotransformation of pentachlorophenol. Appl. Microbiol. Biotechnol. 62: 284–290

    PubMed  Google Scholar 

  • Nojiri H, Habe H & Omori T (2001) Bacterial degradation of aromatic compounds via angular dioxygenation. J. Gen. Appl. Microbiol. 47: 279–305

    PubMed  Google Scholar 

  • Nokazawa T & Nokazawa A (1970) Pyrocatechase (Pseudomonas). Meth. Enzymol. 17A: 518–522

    Google Scholar 

  • Nozaki M (1970) Metapyrocatechase (Pseudomonas). Meth. Enzymol. 17A: 522–525

    Google Scholar 

  • Oh JE, Lee KT, Lee JW & Chang YS (1999) The evaluation of PCDD/Fs from various Korean incinerators. Chemosphere 38: 2097–2108

    Google Scholar 

  • Omori T, Sugimura K, Ishigooka H & Minoda Y (1986) Purification and some properties of a 2-hydroxy-6-oxo-6phenylhexa-2,4-dienoic acid hydrolyzing enzyme from Pseudomonas cruciviae S93 BI involved in the degradation of biphenyl. Agric. BioI. Chem. 50: 931–937

    Google Scholar 

  • Parsons JR & Storms MCM (1989) Biodegradation of chlorinated dibenzo-p-dioxins in batch and continuous cultures of strain JBI. Chemosphere 19: 1297–1308

    Google Scholar 

  • Pearson WR & Lipman DJ (1988) Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85: 2444–2448

    Google Scholar 

  • Pollitt F (1999) Polychlorinated dibenzodioxins and polychlorinated dibenzofurans. Regul. Toxicol. Pharm. 30: S63-S68

    Google Scholar 

  • Schreiner G, Wiedmann T, Schimmel H & Ballschmiter K (1997) Influence of the substitution pattern on the microbial degradation of mono-to tetrachlorinated dibenzo-p-dioxins and dibenzofurans. Chemosphere 34: 1315–1331

    Google Scholar 

  • Shin WY, Doucette W, Frank APCG, Andren A & Donald M (1988) Physical chemical properities of chlorinated dibenzo-p-dioxins. Environ. Sci. Technol. 22: 651–658

    Google Scholar 

  • Wilkes H, Francke W, Wittich RM, Harms H, Schmidt S & Fortnagel P (1992) Mechanistic investigation on microbial degradation of diaryl ethers — analysis of isotope-labelled reaction products. Naturwissenschaften 79: 269–271

    Google Scholar 

  • Wilkes H, Wittich RM, Timmis KN, Fortnagel P & Francke W (1996) Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by Sphingomonas sp. strain RWI. Appl. Environ. Microbiol. 62: 367–371

    Google Scholar 

  • Wittich RM (1998) Degradation of dioxin-like compounds by microorganisms. Appl. Microbiol. Biotechnol. 49: 489–499

    PubMed  Google Scholar 

  • Wittich RM, Wilkes H, Sinnwell V, Francke W & Fortnagel P (1992) Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RWI. Appl. Environ. Microbiol. 58: 1005–1010

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hong, HB., Nam, IH., Murugesan, K. et al. Biodegradation of Dibenzo-p-dioxin, Dibenzofuran, and Chlorodibenzo-p-dioxins by Pseudomonas veronii PH-03. Biodegradation 15, 303–313 (2004). https://doi.org/10.1023/B:BIOD.0000042185.04905.0d

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:BIOD.0000042185.04905.0d

Navigation