Skip to main content
Log in

An unexpected gene cluster for downstream degradation of alkylphenols in Sphingomonas sp. strain TTNP3

  • Environmental Biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

In silico analysis of nucleotide sequences flanking the recently found hydroquinone dioxygenase in Sphingomonas sp. strain TTNP3 revealed a gene cluster that encodes a hydroquinone catabolic pathway. In addition to the two open-reading frames encoding the recently characterized hydroquinone dioxygenase, the cluster consisted of six open-reading frames. We were able to express the three open-reading frames, hqdC, hqdD, and hqdE, and demonstrated that the three gene products, HqdC, HqdD, and HqdE had 4-hydroxymuconic semialdehyde dehydrogenase, maleylacetate reductase, and intradiol dioxygenase activity, respectively. Surprisingly, the gene cluster showed similarities to functionally related clusters found in members of the β- and γ-proteobacteria rather than to those found in other members of the genus Sphingomonas sensu latu.

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. 3
Fig. 4

Similar content being viewed by others

References

  • Addou S, Rentzsch R, Lee D, Orengo CA (2009) Domain-based and family-specific sequence identity thresholds increase the levels of reliable protein function transfer. J Mol Biol 387(2):416–430

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Cai M, Xun L (2002) Organization and regulation of pentachlorophenol-degrading genes in Sphingobium chlorophenolicum ATCC 39723. J Bacteriol 184(17):4672–4680. doi:10.1128/jb.184.17.4672-4680.2002

    Article  CAS  Google Scholar 

  • Cerdan P, Wasserfallen A, Rekik M, Timmis KN, Harayama S (1994) Substrate specificity of catechol 2, 3-dioxygenase encoded by TOL plasmid pWW0 of Pseudomonas putida and its relationship to cell growth. J Bacteriol 176(19):6074–6081

    CAS  Google Scholar 

  • Corvini PFX, Vinken R, Hommes G, Schmidt B, Dohmann M (2004) Degradation of the radioactive and non-labelled branched 4(3′,5′-dimethyl 3′-heptyl)-phenol nonylphenol isomer by Sphingomonas TTNP3. Biodegradation 15(1):9–18

    Article  CAS  Google Scholar 

  • Corvini PFX, Hollender J, Ji R, Schumacher S, Prell J, Hommes G, Priefer U, Vinken R, Schaffer A (2006a) The degradation of alpha-quaternary nonylphenol isomers by Sphingomonas sp. strain TTNP3 involves a type II ipso-substitution mechanism. Appl Microbiol Biotechnol 70(1):114–122. doi:10.1007/s00253-005-0080-0

    Article  CAS  Google Scholar 

  • Corvini PFX, Schaffer A, Schlosser D (2006b) Microbial degradation of nonylphenol and other alkylphenols—our evolving view. Appl Microbiol Biotechnol 72(2):223–243. doi:10.1007/s00253-006-0476-5

    Article  CAS  Google Scholar 

  • Endo R, Kamakura M, Miyauchi K, Fukuda M, Ohtsubo Y, Tsuda M, Nagata Y (2005) Identification and characterization of genes involved in the downstream degradation pathway of gamma-hexachlorocyclohexane in Sphingomonas paucimobilis UT26. J Bacteriol 187(3):847–853. doi:10.1128/jb.187.3.847-853.2005

    Article  CAS  Google Scholar 

  • Gabriel FLP, Giger W, Guenther K, Kohler H-PE (2005a) Differential degradation of nonylphenol isomers by Sphingomonas xenophaga Bayram. Appl Environ Microbiol 71(3):1123–1129. doi:10.1128/aem.71.3.1123-1129.2005

    Article  CAS  Google Scholar 

  • Gabriel FLP, Heidlberger A, Rentsch D, Giger W, Guenther K, Kohler HPE (2005b) A novel metabolic pathway for degradation of 4-nonylphenol environmental contaminants by Sphingomonas xenophaga Bayram: ipso-hydroxylation and intramolecular rearrangement. J Biol Chem 280(16):15526–15533. doi:10.1074/jbc.M413446200

    Article  CAS  Google Scholar 

  • Gabriel FLP, Cyris M, Giger W, Kohler HPE (2007a) ipso-Substitution: a general biochemical and biodegradation mechanism to cleave alpha-quaternary alkylphenols and bisphenol A. Chem Biodivers 4(9):2123–2137

    Article  CAS  Google Scholar 

  • Gabriel FLP, Cyris M, Jonkers N, Giger W, Guenther K, Kohler HPE (2007b) Elucidation of the ipso-substitution mechanism for side-chain cleavage of alpha-quaternary 4-nonylphenols and 4-t-butoxyphenol in Sphingobium xenophagum Bayram. Appl Environ Microbiol 73(10):3320–3326. doi:10.1128/aem.02994-06

    Article  CAS  Google Scholar 

  • Gabriel FLP, Routledge EJ, Heidlberger A, Rentsch D, Guenther K, Giger W, Sumpter JP, Kohler HPE (2008) Isomer-specific degradation and endocrine disrupting activity of nonylphenols. Environ Sci Technol 42(17):6399–6408. doi:10.1021/es800577a

    Article  CAS  Google Scholar 

  • Hugo N, Armengaud J, Gaillard J, Timmis KN, Jouanneau Y (1998) A novel [2Fe-2S] ferredoxin from Pseudomonas putida mt2 promotes the reductive reactivation of catechol 2,3-dioxygenase. J Biol Chem 273(16):9622–9629

    Article  CAS  Google Scholar 

  • Hugo N, Meyer C, Armengaud J, Gaillard J, Timmis KN, Jouanneau Y (2000) Characterization of three XylT-like [2Fe-2S] ferredoxins associated with catabolism of cresols or naphthalene: evidence for their involvement in catechol dioxygenase reactivation. J Bacteriol 182(19):5580–5585. doi:10.1128/jb.182.19.5580-5585.2000

    Article  CAS  Google Scholar 

  • Hussain S, Devers-Lamrani M, El Azhari N, Martin-Laurent F (2011) Isolation and characterization of an isoproturon mineralizing Sphingomonas sp. strain SH from a French agricultural soil. Biodegradation 22(3):637–650

    Article  CAS  Google Scholar 

  • Kang J-H, Katayama Y, Kondo F (2006) Biodegradation or metabolism of bisphenol A: from microorganisms to mammals. Toxicology 217(2–3):81–90

    Article  CAS  Google Scholar 

  • Kaschabek SR, Reineke W (1995) Maleylacetate reductase of Pseudomonas sp. strain B13: specificity of substrate conversion and halide elimination. J Bacteriol 177(2):320–325

    Google Scholar 

  • Klecka GM, Naylor CG, Staples CA, Losey B (2010) Occurrence of nonylphenol ethoxylates and their metabolites in municipal wastewater treatment plants and receiving waters. Water Environ Res 82:447–454

    Article  CAS  Google Scholar 

  • Kolvenbach B, Schlaich N, Raoui Z, Prell J, Zuhlke S, Schaffer A, Guengerich FP, Corvini PFX (2007) Degradation pathway of bisphenol A: does ipso substitution apply to phenols containing a quaternary alpha-carbon structure in the para position? Appl Environ Microbiol 73(15):4776–4784

    Article  CAS  Google Scholar 

  • Kolvenbach BA, Lenz M, Benndorf D, Rapp E, Vlcek C, Fouzek J, Gabriel FLP, Kohler H-PE, Schäffer A (2011) Purification and characterization of hydroquinone dioxygenase from Sphingonomas sp. strain TTNP3. AMB Express 1:8

    Article  CAS  Google Scholar 

  • Kweon O, Kim S-J, Baek S, Chae J-C, Adjei MA, Baek D-H, Kim Y-C, Cerniglia CE (2008) A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem 9:11. doi:10.1186/1471-2091-9-11

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685

    Article  CAS  Google Scholar 

  • Leung KT, Tresse O, Errampalli D, Lee H, Trevors JT (1997) Mineralization of p-nitrophenol by pentachlorophenol-degrading Sphingomonas spp. FEMS Microbiol Lett 155(1):107–114

    Article  CAS  Google Scholar 

  • Leung KT, Campbell S, Gan Y, White DC, Lee HT, Trevors J (1999) The role of the Sphingomonas species UG30 pentachlorophenol-4-monooxygenase in p-nitrophenol degradation. FEMS Microbiol Lett 173(1):247–253

    Article  CAS  Google Scholar 

  • Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26(4):1107–1115

    Article  CAS  Google Scholar 

  • Manickam N, Reddy MK, Saini HS, Shanker R (2008) Isolation of hexachlorocyclohexane-degrading Sphingomonas sp. by dehalogenase assay and characterization of genes involved in γ-HCH degradation. J Appl Microbiol 104(4):952–960

    Article  CAS  Google Scholar 

  • Miyauchi K, Adachi Y, Nagata Y, Takagi M (1999) Cloning and sequencing of a novel meta-cleavage dioxygenase gene whose product is involved in degradation of gamma-hexachlorocyclohexane in Sphingomonas paucimobilis. J Bacteriol 181(21):6712–6719

    CAS  Google Scholar 

  • Moonen MJH, Kamerbeek NM, Westphal AH, Boeren SA, Janssen DB, Fraaije MW, van Berkel WJH (2008) Elucidation of the 4-hydroxyacetophenone catabolic pathway in Pseudomonas fluorescens ACB. J Bacteriol 190(15):5190–5198. doi:10.1128/jb.01944-07

    Article  CAS  Google Scholar 

  • Nagata Y, Kamakura M, Endo R, Miyazaki R, Ohtsubo Y, Tsuda M (2006) Distribution of γ-hexachlorocyclohexane-degrading genes on three replicons in Sphingobium japonicum UT26. FEMS Microbiol Lett 256(1):112–118. doi:10.1111/j.1574-6968.2005.00096.x

    Article  CAS  Google Scholar 

  • Nagata Y, Endo R, Ito M, Ohtsubo Y, Tsuda M (2007) Aerobic degradation of lindane (γ-hexachlorocyclohexane) in bacteria and its biochemical and molecular basis. Appl Microbiol Biotechnol 76(4):741–752

    Article  CAS  Google Scholar 

  • Ohtsubo Y, Miyauchi K, Kanda K, Hatta T, Kiyohara H, Senda T, Nagata Y, Mitsui Y, Takagi M (1999) PcpA, which is involved in the degradation of pentachlorophenol in Sphingomonas chlorophenolica ATCC39723, is a novel type of ring-cleavage dioxygenase. FEBS Lett 459(3):395–398

    Article  CAS  Google Scholar 

  • Polissi A, Harayama S (1993) In vivo reactivation of catechol 2,3-dioxygenase mediated by a chloroplast-type ferredoxin: a bacterial strategy to expand the substrate specificity of aromatic degradative pathways. EMBO J 12(8):3339–3347

    CAS  Google Scholar 

  • Raecker T, Thiele B, Boehme RM, Guenther K (2011) Endocrine disrupting nonyl- and octylphenol in infant food in Germany: considerable daily intake of nonylphenol for babies. Chemosphere 82(11):1533–1540

    Article  CAS  Google Scholar 

  • Rieble S, Joshi DK, Gold MH (1994) Purification and characterization of a 1, 2, 4-trihydroxybenzene 1, 2-dioxygenase from the basidiomycete Phanerochaete chrysosporium. J Bacteriol 176(16):4838–4844

    CAS  Google Scholar 

  • Sakai K, Yamanaka H, Moriyoshi K, Ohmoto T, Ohe T (2007) Biodegradation of bisphenol A and related compounds by Sphingomonas sp. strain BP-7 isolated from seawater. Biosci Biotechnol Biochem 71(1):51–57. doi:10.1271/bbb.60351

    Article  CAS  Google Scholar 

  • Sasaki M, Maki J, Oshiman K, Matsumura Y, Tsuchido T (2005) Biodegradation of bisphenol A by cells and cell lysate from Sphingomonas sp. strain AO1. Biodegradation 16(5):449–459. doi:10.1007/s10532-004-5023-4

    Article  CAS  Google Scholar 

  • Schuler L, Jouanneau Y, Ní Chadhain S, Meyer C, Pouli M, Zylstra G, Hols P, Agathos S (2009) Characterization of a ring-hydroxylating dioxygenase from phenanthrene-degrading Sphingomonas sp. strain LH128 able to oxidize benz[a]anthracene. Appl Microbiol Biotechnol 83(3):465–475. doi:10.1007/s00253-009-1858-2

    Article  CAS  Google Scholar 

  • Shen W, Liu W, Zhang J, Tao J, Deng H, Cao H, Cui Z (2010) Cloning and characterization of a gene cluster involved in the catabolism of p-nitrophenol from Pseudomonas putida DLL-E4. Bioresource Tech 101(19):7516–1522

    Article  CAS  Google Scholar 

  • Shimojo M, Kawakami M, Amada K (2009) Analysis of genes encoding the 2,4-dichlorophenoxyacetic acid-degrading enzyme from Sphingomonas agrestis 58–1. J Biosci Bioeng 108(1):56–59

    Article  CAS  Google Scholar 

  • Soares A, Guieysse B, Jefferson B, Cartmell E, Lester JN (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34(7):1033–1049

    Article  CAS  Google Scholar 

  • Spain JC, Gibson DT (1991) Pathway for biodegradation of p-nitrophenol in a Moraxella sp. Appl Environ Microbiol 57(3):812–819

    CAS  Google Scholar 

  • Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81(5):793–811. doi:10.1007/s00253-008-1752-3

    Article  CAS  Google Scholar 

  • Tanghe T, Dhooge V, Verstraete W (1999) Isolation of a bacterial strain able to degrade branched nonylphenol. Appl Environ Microbiol 65(2):746–751

    CAS  Google Scholar 

  • vom Saal FS, Hughes C (2005) An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 113(8):926–933. doi:10.1289/ehp.7713

    Article  Google Scholar 

  • Wei Q, Liu H, Zhang J-J, Wang S-H, Xiao Y, Zhou N-Y (2010) Characterization of a para-nitrophenol catabolic cluster in Pseudomonas sp. strain NyZ402 and construction of an engineered strain capable of simultaneously mineralizing both para- and ortho-nitrophenols. Biodegradation 21(4):575–584

    Article  CAS  Google Scholar 

  • Yang C-F, Lee C-M, Wang C-C (2006) Isolation and physiological characterization of the pentachlorophenol degrading bacterium Sphingomonas chlorophenolica. Chemosphere 62(5):709–714

    Article  CAS  Google Scholar 

  • Zhang J-J, Liu H, Xiao Y, Zhang X-E, Zhou N-Y (2009) Identification and characterization of catabolic para-nitrophenol 4-monooxygenase and para-benzoquinone reductase from Pseudomonas sp. strain WBC-3. J Bacteriol 191(8):2703–2710. doi:10.1128/jb.01566-08

    Article  CAS  Google Scholar 

  • Zhao H-P, Wang L, Ren J-R, Li Z, Li M, Gao H-W (2008) Isolation and characterization of phenanthrene-degrading strains Sphingomonas sp. ZP1 and Tistrella sp. ZP5. J Hazard Mater 152(3):1293–1300

    Article  CAS  Google Scholar 

Download references

Acknowledgments

BAK and FLPG were funded by the Swiss National Science Foundation grant SNF-200021-120547. JF and CV were funded by the EC Grant Agreement 265946. We thank Dr. Stefan Kaschabek (University Freiberg) for generously providing a sample of cis-butenolide.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Boris A. Kolvenbach.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kolvenbach, B.A., Dobrowinski, H., Fousek, J. et al. An unexpected gene cluster for downstream degradation of alkylphenols in Sphingomonas sp. strain TTNP3. Appl Microbiol Biotechnol 93, 1315–1324 (2012). https://doi.org/10.1007/s00253-011-3451-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-011-3451-8

Keywords

Navigation