Skip to main content

Advertisement

Log in

Degradation of carbazole and its derivatives by a Pseudomonas sp.

  • ENVIRONMENTAL BIOTECHNOLOGY
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Carbazole, carbazoles with monomethyl or dimethyls substituted on different positions (C1-carbazoles or C2-carbazoles), and benzocarbazoles, as toxic and mutagenic components of petroleum and creosote contamination, were biodegradable by an isolated bacterial strain Pseudomonas sp. XLDN4-9. C1-carbazoles were degraded in preference to carbazole and C2-carbazoles. The biodegradation of C1-carbazoles or C2-carbazoles was influenced by the positions of methyl substitutions. Among C1-carbazole isomers, 1-methyl carbazole was the most susceptible. C2-carbazole isomers with substitutions on the same benzo-nucleus were more susceptible at a concentration of less than 3.4 μg g−1 petroleum, especially when harboring one substitution on position 1. In particular, 1,5-dimethyl carbazole was the most recalcitrant dimethyl isomer.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aitken MD, Stringfellow WT, Nagel RD, Kazunga C, Chen SH (1998) Characteristics of phenanthrene-degrading bacteria isolated from soils contaminated with polycyclic aromatic hydrocarbons. Can J Microbiol 44:743–752

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K (1995) Short protocols in molecular biology, 3rd edn. Wiley, New York

    Google Scholar 

  • Benedik MJ, Gibbs PR, Riddle RR, Willson RC (1998) Microbial denitrogenation of fossil fuels. Trends Biotechnol 16:390–395

    Article  CAS  PubMed  Google Scholar 

  • Fedorak PM, Westlake DWS (1984) Microbial degradation of alkyl carbazoles in Norman Wells crude oil. Appl Environ Microbiol 47:858–862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbs PR, Riddle RR, Marchal L, Benedik MJ, Willson RC (2003) Purification and characterization of 2′-aminobiphenyl-2,3-diol 1,2-dioxygenase from Pseudomonas sp. LD2. Protein Expr Purif 32:35–43

    Article  CAS  PubMed  Google Scholar 

  • Gieg LM, Otter A, Fedorak PM (1996) Carbazole degradation by Pseudomonas sp. LD2 metabolic characteristics and the identification of some metabolites. Environ Sci Technol 30:575–585

    Article  CAS  Google Scholar 

  • Grosser RJ, Warshawsky D, Vestal JR (1991) Indigenous and enhanced mineralization of pyrene, bezo[a]pyrene, and carbazole in soils. Appl Environ Microbiol 57:3462–3469

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwata K, Nojiri H, Shimizu K, Yoshida T, Habe H, Omori T (2003) Expression, purification, and characterization of 2′-aminobiphenyl-2,3-diol 1,2-dioxygenase from carbazole-degrader Pseudomonas resinovorans strain CA10. Biosci Biotechnol Biochem 67:300–307

    Article  CAS  PubMed  Google Scholar 

  • Jha AM, Bharti MK (2002) Mutagenic profiles carbazole in the male germ cells of Swiss albino mice. Mutat Res 500:97–101

    Article  CAS  PubMed  Google Scholar 

  • Kilbane JJ II, Daram A, Abbasian J, Kayser KJ (2002) Isolation and characterization of Sphingomonas sp. GTIN11 capable of carbazole metabolism in petroleum. Biochem Biophys Res Commun 297:242–248

    Article  CAS  PubMed  Google Scholar 

  • Kirimura K, Nakagawa H, Tsuji K, Matsuda K, Kurane R, Usami S (1999) Selective and continuous degradation of carbazole contained in petroleum oil by resting cells of Sphingomonas sp. CDH-7. Biosci Biotechnol Biochem 63:1563–1568

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi T, Kurane R, Kenji N, Nakamura Y, Kirimura K, Usami S (1995) Isolation of bacteria degrading carbazole under microaerobic conditions, i.e. nitrogen gas substituted conditions. Biosci Biotechnol Biochem 59:932–933

    Article  CAS  PubMed  Google Scholar 

  • Leblond JD, Schultz TW, Sayler GS (2001) Observations on the preferential biodegradation of selected components of polyaromatic hydrocarbon mixtures. Chemosphere 42:333–343

    Article  CAS  PubMed  Google Scholar 

  • Li FL, Xu P, Feng JH, Meng L, Zheng Y, Luo LL, Ma CQ (2005) Microbial Desulfurization of gasoline in immobilized-Cell system of Mycobacterium goodii X7B. Appl Environ Microbiol 71:276–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Xu P, Blankespoor D (2004) Degradation of carbazole in the presence of non-aqueous phase liquids by Pseudomonas sp. Biotechnol Lett 26:581–584

    Article  CAS  PubMed  Google Scholar 

  • Li M, Later SR, Stoddert D (1992) Liquid chromatographic separation schemes for pyrrole and pyridine nitrogen aromatic heterocycle fractions from crude oils suitable for rapid characterization of geochemical samples. Anal Chem 64:1337–1344

    Article  CAS  Google Scholar 

  • Malins DC, Krahn MM, Myers MS, Rhodes LD, Brown DW, Krone CA, McCain BB, Chan SL (1985) Toxic chemicals in sediments and biota from a creosote-polluted harbor: relationships with hepatic neoplasms and other hepatic lesions in English sole (Parophrys vetulus). Carcinogenesis 6:1463–1469

    Article  CAS  PubMed  Google Scholar 

  • Mao J, Pacheco CR, Traficante DD, Rosen W (1994) Analysis of neutral nitrogen compounds in diesel oil by direct injection of high-performance liquid chromatography-mass spectrometry-ultraviolet spectrometry methods. J Chromatogr A 684:103–111

    Article  CAS  Google Scholar 

  • Nam JW, Nojiri H, Noguchi H, Uchimura H, Yoshida T, Habe H, Yamane H, Omori T (2002) Purification and characterization of carbazole 1,9a-dioxygenase, a three-component dioxygenase system of Pseudomonas resinovorans strain CA10. Appl Environ Microbiol 68:5882–5890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nojiri H, Nam JW, Kosaka M, Morii KI, Takemura T, Furihata K, Yamane H, Omori T (1999) Diverse oxygenations catalyzed by carbazole 1,9a-dioxygenase from Pseudomonas sp. Strain CA10. J Bacteriol 181:3105–3113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nojiri H, Omori T (2002) Molecular bases of aerobic bacterial degradation of dioxins: involvement of angular dioxygenation. Biosci Biotechnol Biochem 66:2001–2016

    Article  CAS  PubMed  Google Scholar 

  • Nojiri H, Sekiguchi H, Maeda K, Urata M, Nakai SI, Yoshida T, Habe H, Omori T (2001) Genetic characterization and evolutionary implications of a car gene cluster in the carbazole degrader Pseudomonas sp. J Bacteriol 183:3663–3679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nojiri H, Taira H, Iwata K, Morii K, Nam JW, Yoshida T, Habe H, Nakamura S, Shimizu K, Yamane H, Omori T (2003) Purification and characterization of meta-cleavage compound hydrolase from a carbazole degrader Pseudomonas resinovorans strain CA10. Biosci Biotechnol Biochem 67:36–45

    Article  CAS  PubMed  Google Scholar 

  • O’Brien T, Schneider J, Warshawsky D, Mitchell K (2002) In vitro toxicity of 7H-dibenzo[c,g]carbazole in human liver cell lines. Toxicol In Vitro 16:235–243

    Article  PubMed  Google Scholar 

  • Ouchiyama N, Zhang Y, Omori T, Kodama T (1993) Biodegradation of carbazole by Pseudomonas spp. CA06 and CA10. Biosci Biotechnol Biochem 57:455–460

    Article  CAS  Google Scholar 

  • Prince RC, Grossman MJ (2003) Substrate preferences in biodesulfurization of diesel range fuels by Rhodococcus sp. Strain ECRD-1. Appl Environ Microbiol 69:5833–5838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy MY, Randerath K (1990) A comparison of DNA adduct formation in white blood cells and internal organs of mice exposed to benzo[a]pyrene, dibenzo[c,g]carbazole, safrole and cigarette smoke condensate. Mutat Res 241:37–48

    Article  CAS  PubMed  Google Scholar 

  • Riddle RR, Gibbs PR, Willson RC, Benedik MJ (2003a) Purification and properties of 2-hydroxy-6-oxo-6-(2′-aminophenyl)hexa-2,4-dienoic acid hydrolase involved in microbial degradation of carbazole. Protein Expr Purif 28:182–189

    Article  CAS  PubMed  Google Scholar 

  • Riddle RR, Gibbs PR, Willson RC, Benedik MJ (2003b) Recombinant carbazole-degrading strains for enhanced petroleum processing. J Ind Microbiol Biotechnol 30:6–12

    Article  CAS  PubMed  Google Scholar 

  • Santos SCC, Alviano DS, Alviano CS, Pádula M, Leitão AC, Martins OB, Ribeiro CMS, Sassaki MYM, Matta CPS, Bevilaqua J, Sebastián GV, Seldin L (2006) Characterization of Gordonia sp. strain F.5.25.8 capable of dibenzothiophene desulfurization and carbazole utilization. Appl Microbiol Biotechnol 71:355–362

    Article  CAS  PubMed  Google Scholar 

  • Sato SI, Nam JW, Kasuga K, Nojiri H, Yamane H, Omori T (1997a) Identification and characterization of genes encoding carbazole 1,9a-dioxygenase in Pseudomonas sp. Strain CA10. J Bacteriol 179:4850–4858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato SI, Ouchiyama N, Kimura T, Nojiri H, Yamane H, Omori T (1997b) Cloning of genes Involved in carbazole degradation of Pseudomonas sp. Strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase. J Bacteriol 179:4841–4849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider J, Grosser RJ, Jayasimhulu K, Xue W, Kinkle B, Warshawsky D (2000) Biodegradation of carbazole by Ralstonia sp. RJGII. 123 isolated from a hydrocarbon contaminated soil. Can J Microbiol 46:269–277

    Article  CAS  PubMed  Google Scholar 

  • Shepherd JM, Lloyd-Jones G (1998) Novel Carbazole degradation genes of Sphingomonas CB3: sequence analysis, transcription and molecular ecology. Biochem Biophys Res Commun 247:129–135

    Article  CAS  PubMed  Google Scholar 

  • Sverdrup LE, Jensen J, Kelley AE, Krogh PH, Stenersen J (2002) Effect of eight polycyclic aromatic compounds on the survival and reproduction of Enchytraeus crypticus (Oligochaeta, clitellata). Environ Toxicol Chem 21:109–114

    Article  CAS  PubMed  Google Scholar 

  • Wammer KH, Peters CA (2005) Polycyclic aromatic hydrocarbon biodegradation rates: a structure-based study. Environ Sci Technol 39:2571–2578

    Article  CAS  PubMed  Google Scholar 

  • Warshawsky D (1992) Environmental source, carcinogenicity, mutagenicity, metabolism and DNA binding of nitrogen and sulfur heterocyclic aromatics. Environ Carcinog Ecotoxicol Rev C 10:1–71

    Article  Google Scholar 

Download references

Acknowledgements

The work was supported by the Chinese National Natural Science Foundation (grant nos. 20377026 and 20590368) and Chinese National Programs for High Technology Research and Development (grant no. 2004AA649160).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ping Xu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, L., Li, Q., Li, F. et al. Degradation of carbazole and its derivatives by a Pseudomonas sp.. Appl Microbiol Biotechnol 73, 941–948 (2006). https://doi.org/10.1007/s00253-006-0530-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-006-0530-3

Keywords

Navigation