Skip to main content
SpringerLink
Log in

The role of active-site residues in naphthalene dioxygenase

  • Review Paper
  • Published:
Journal of Industrial Microbiology and Biotechnology

Abstract

The three-component naphthalene dioxygenase enzyme system catalyzes the first step in the degradation of naphthalene by Pseudomonas sp. strain NCIB 9816-4. A member of a large family of bacterial Rieske non-heme iron oxygenases, naphthalene dioxygenase is known to oxidize over 60 different aromatic compounds, and many of the products are enantiomerically pure. The crystal structure of the oxygenase component revealed the enzyme to be an α3β3 hexamer and identified the amino acids located near the active site. Site-directed mutagenesis studies have identified the residues involved in electron transfer and those responsible for controlling the regioselectivity and enantioselectivity of the enzyme. The results of these studies suggest that naphthalene dioxygenase can be engineered to catalyze a new and extended range of useful reactions.

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

Fig. 1.
Fig. 2.
Fig. 3A, B.
Fig. 4.
Fig. 5.
Fig. 6A, B.

Similar content being viewed by others

References

  1. Anastas PT, MM Kirchhoff (2002) Origins, current status, and future challenges of green chemistry. Acc Chem Res 35:686–694

    CAS  PubMed  Google Scholar 

  2. Beil S, JR Mason, KN Timmis, DH Pieper (1998) Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5-tetrachlorobenzene. J Bacteriol 180:5520–5528

    CAS  PubMed  Google Scholar 

  3. Boyd DR, ND Sharma, CCR Allen (2001) Aromatic dioxygenases: molecular biocatalysis and applications. Curr Opin Biotechnol 12:564–573

    CAS  PubMed  Google Scholar 

  4. Boyd DR, GN Sheldrake (1998) The dioxygenase-catalysed formation of vicinal cis-diols. Nat Prod Rep 15:309–324

    Google Scholar 

  5. Carredano E, A Karlsson, B Kauppi, D Choudhury, RE Parales, JV Parales, K Lee, DT Gibson, H Eklund, S Ramaswamy (2000) Substrate binding site of naphthalene 1,2-dioxygenase: functional implications of indole binding. J Mol Biol 296:701–712

    CAS  PubMed  Google Scholar 

  6. Eaton RW, PJ Chapman (1992) Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions. J Bacteriol 174:7542–7554

    CAS  PubMed  Google Scholar 

  7. Ensley BD, DT Gibson (1983) Naphthalene dioxygenase: purification and properties of a terminal oxygenase component. J Bacteriol 155:505–511

    CAS  PubMed  Google Scholar 

  8. Ensley BD, DT Gibson, AL Laborde (1982) Oxidation of naphthalene by a multicomponent enzyme system from Pseudomonas sp. strain NCIB 9816. J Bacteriol 149:948–954

    CAS  PubMed  Google Scholar 

  9. Ensley BD, BJ Ratzkin, TD Osslund, MJ Simon, LP Wackett, DT Gibson (1983) Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo. Science 222:167–169

    CAS  PubMed  Google Scholar 

  10. Erickson BD, FJ Mondello (1992) Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated biphenyl-degrading enzyme in Pseudomonas strain LB400. J Bacteriol 174:2903–2912

    PubMed  Google Scholar 

  11. Fukuda M, Y Yasukochi, Y Kikuchi, Y Nagata, K Kimbara, H Horiuchi, M Takagi, K Yano (1994) Identification of the bphA and bphB genes of Pseudomonas sp. strain KKS102 involved in degradation of biphenyl and polychlorinated biphenyls. Biochem Biophys Res Commun 202:850–856

    CAS  PubMed  Google Scholar 

  12. Gibson DT, RE Parales (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243

    CAS  PubMed  Google Scholar 

  13. Haigler BE, DT Gibson (1990) Purification and properties of ferredoxinNAP, a component of naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Bacteriol 172:465–468

    CAS  PubMed  Google Scholar 

  14. Haigler BE, DT Gibson (1990) Purification and properties of NADH-ferredoxinNAP reductase, a component of naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Bacteriol 172:457–464

    CAS  PubMed  Google Scholar 

  15. Harayama S, M Rekik, KN Timmis (1986) Genetic analysis of a relaxed substrate specificity aromatic ring dioxygenase, toluate 1,2-dioxygenase, encoded by TOL plasmid pWWO of Pseudomonas putida. Mol Gen Genet 202:226–234

    CAS  PubMed  Google Scholar 

  16. Hegg EL, LJ Que (1997) The 2-His-1-carboxylate facial triad: An emerging structural motif in mononuclear non-heme iron(II) enzymes. Eur J Biochem 250:625–629

    CAS  PubMed  Google Scholar 

  17. Hirose J, A Suyama, S Hayashida, K Furukawa (1994) Construction of hybrid biphenyl (bph) and toluene (tod) genes for functional analysis of aromatic ring dioxygenases. Gene 138:27–33

    CAS  PubMed  Google Scholar 

  18. Hudlicky T, D Gonzalez, DT Gibson (1999) Enzymatic dihydroxylation of aromatics in enantioselective synthesis: Expanding asymmetric methodology. Aldrichimica Acta 32:35–62

    CAS  Google Scholar 

  19. Hurtubise Y, D Barriault, M Sylvestre (1998) Involvement of the terminal oxygenase β subunit in the biphenyl dioxygenase reactivity pattern toward chlorobiphenyls. J Bacteriol 180:5828–5835

    CAS  PubMed  Google Scholar 

  20. Jeffrey AM, HJC Yeh, DM Jerina, TR Patel, JF Davey, DT Gibson (1975) Initial reactions in the oxidation of naphthalene by Pseudomonas putida. Biochemistry 14:575–583

    CAS  PubMed  Google Scholar 

  21. Jerina DM, JW Daly, AM Jeffrey, DT Gibson (1971) cis-1,2-Dihydroxy-1,2-dihydronaphthalene: a bacterial metabolite from naphthalene. Arch Biochem Biophys 142:394–396

    CAS  PubMed  Google Scholar 

  22. Jiang H, RE Parales, DT Gibson (1999) The α subunit of toluene dioxygenase from Pseudomonas putida F1 can accept electrons from reduced ferredoxinTOL but is catalytically inactive in the absence of the β subunit. Appl Environ Microbiol 65:315–318

    CAS  PubMed  Google Scholar 

  23. Jiang H, RE Parales, NA Lynch, DT Gibson (1996) Site-directed mutagenesis of conserved amino acids in the alpha subunit of toluene dioxygenase: potential mononuclear non-heme iron coordination sites. J Bacteriol 178:3133–3139

    CAS  PubMed  Google Scholar 

  24. Karlsson A, JV Parales, RE Parales, DT Gibson, H Eklund, S Ramaswamy (2003) Crystal structure of naphthalene dioxygenase: side-on binding of dioxygen to iron. Science 299:1039–1042

    Google Scholar 

  25. Kauppi B, K Lee, E Carredano, RE Parales, DT Gibson, H Eklund, S Ramaswamy (1998) Structure of an aromatic ring-hydroxylating dioxygenase- naphthalene 1,2-dioxygenase. Structure 6:571–586

    CAS  PubMed  Google Scholar 

  26. Lee K (1999) Benzene-induced uncoupling of naphthalene dioxygenase activity and enzyme inactivation by production of hydrogen peroxide. J Bacteriol 181:2719–2725

    PubMed  Google Scholar 

  27. Parales JV, A Kumar, RE Parales, DT Gibson (1996) Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42. Gene 181:57–61

    Article  CAS  PubMed  Google Scholar 

  28. Parales JV, RE Parales, SM Resnick, DT Gibson (1998) Enzyme specificity of 2-nitrotoluene 2,3-dioxygenase from Pseudomonas sp. strain JS42 is determined by the C-terminal region of the α subunit of the oxygenase component. J Bacteriol 180:1194–1199

    CAS  PubMed  Google Scholar 

  29. Parales RE, MD Emig, NA Lynch, DT Gibson (1998) Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. J Bacteriol 180:2337–2344

    CAS  PubMed  Google Scholar 

  30. Parales RE, K Lee, SM Resnick, H Jiang, DJ Lessner, DT Gibson (2000) Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J Bacteriol 182:1641-1649

    CAS  PubMed  Google Scholar 

  31. Parales RE, JV Parales, DT Gibson (1999) Aspartate 205 in the catalytic domain of naphthalene dioxygenase is essential for activity. J Bacteriol 181:1831–1837

    CAS  PubMed  Google Scholar 

  32. Parales RE, SM Resnick, CL Yu, DR Boyd, ND Sharma, DT Gibson (2000) Regioselectivity and enantioselectivity of naphthalene dioxygenase during arene cis-dihydroxylation: control by phenylalanine 352 in the α subunit. J Bacteriol 182:5495–5504

    CAS  PubMed  Google Scholar 

  33. Que LJ (2000) One motif- many different reactions. Nat Struct Biol 7:182–184

    CAS  PubMed  Google Scholar 

  34. Resnick SM, K Lee, DT Gibson (1996) Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Ind Microbiol 17:438–457

    CAS  Google Scholar 

  35. Serdar CM, DT Gibson (1989) Isolation and characterization of altered plasmids in mutant strains of Pseudomonas putida NCIB 9816. Biochem Biophys Res Commun 164:764–771

    CAS  PubMed  Google Scholar 

  36. Simon MJ, TD Osslund, R Saunders, BD Ensley, S Suggs, A Harcourt, W-C Suen, DL Cruden, DT Gibson, GJ Zylstra (1993) Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816–4. Gene 127:31–37

    CAS  PubMed  Google Scholar 

  37. Stinson SC (1994) Chiral drugs. Chem Eng News 72:38–72

    Google Scholar 

  38. Stinson SC (1995) Chiral drugs. Chem Eng News 73:44–74

    Google Scholar 

  39. Suen W-C, BE Haigler, JC Spain (1996) 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: Similarity to naphthalene dioxygenase. J Bacteriol 178:4926–4934

    CAS  PubMed  Google Scholar 

  40. Taira K, J Hirose, S Hayashida, K Furukawa (1992) Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707. J Biol Chem 267:4844–4853

    CAS  Google Scholar 

  41. Tan H-M, C-M Cheong (1994) Substitution of the ISPα subunit of biphenyl dioxygenase from Pseudomonas results in a modification of the enzyme activity. Biochem Biophys Res Commun 204:912–917

    PubMed  Google Scholar 

  42. Werlen C, H-P Kohler, JR van der Meer (1996) The broad substrate chlorobenzene dioxygenase and cis-chlorobenzene dihydrodiol dehydrogenase of Pseudomonas sp. strain P51 are linked evolutionarily to the enzymes for benzene and toluene degradation. J Biol Chem 271:4009–4016

    CAS  Google Scholar 

  43. Yu C-L, RE Parales, DT Gibson (2001) Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enatioselectivity. J Ind Microbiol Biotechnol 27:94–103

    Article  CAS  PubMed  Google Scholar 

  44. Zylstra GJ, DT Gibson (1989) Toluene degradation by Pseudomonas putida F1: nucleotide sequence of the todC1C2BADE genes and their expression in E. coli. J Biol Chem 264:14940–14946

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

I thank Juan Parales for providing figures and David Gibson for support and encouragement.

Author information

Authors and Affiliations

  1. Section of Microbiology, 226 Briggs Hall, University of California, Davis, CA 95616, USA

    Rebecca E. Parales

Authors
  1. Rebecca E. Parales
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rebecca E. Parales.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Parales, R.E. The role of active-site residues in naphthalene dioxygenase. J IND MICROBIOL BIOTECHNOL 30, 271–278 (2003). https://doi.org/10.1007/s10295-003-0043-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-003-0043-3

Keywords

Search

Navigation