Skip to main content
SpringerLink
Log in

Dioxygen activation responsible for oxidation of aliphatic and aromatic hydrocarbon compounds: current state and variants

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The most significant aspect in microbial metabolisms, especially those of bacteria and archaea, is their marvelously wide acceptability of substrate electron donors and acceptors. This feature makes them to be attractive catalysts for environmental biotechnology in terms of degradation of harmful recalcitrant compounds, including hydrocarbons. Transformation of highly reduced and inert hydrocarbon compounds is with no doubt a challenging biochemical reaction for a single enzyme. However, several multi-component enzyme systems enable microorganisms to utilize hydrocarbons as carbon and energy (electron) sources. Initial biological attack to hydrocarbons is, in most cases, the hydroxylation that requires molecular dioxygen as a co-substrate. Dioxygen also contributes to the ring cleavage reaction of homo- and hetero-cyclic aromatic hydrocarbons. Although the molecular dioxygen is omnipresent and highly soluble in water, activation and splitting this triplet ground-state molecule to wed with difficult hydrocarbons need special devices. Non-heme iron, heme iron, or flavin nucleotide was designated as a major hidden dagger for this purpose.

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. 3
Fig. 4

Similar content being viewed by others

References

  • Alfieri A, Fersini F, Ruangchan N, Prongjit M, Chaiyen P, Mattevi A (2007) Structure of the monooxygenase component of a two-component flavoprotein monooxygenase. Proc Natl Acad Sci U S A 104:1177–1182

    Article  CAS  Google Scholar 

  • Bailey LJ, Fox BG (2009) Crystallographic and catalytic studies of the peroxide-shunt reaction in a diiron hydroxylase. Biochemistry 48:8932–8939

    Article  CAS  Google Scholar 

  • Balasubramanian R, Rosenzweig AC (2007) Structural and mechanistic insights into methane oxidation by particulate methane monooxygenase. Acc Chem Res 40:573–580

    Article  CAS  Google Scholar 

  • Ballou DP, Entsch B, Cole LJ (2005) Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases. Biochem Biophys Res Commun 338:590–598

    Article  CAS  Google Scholar 

  • Brown CK, Vetting MW, Earhart CA, Ohlendorf DH (2004) Biophysical analyses of designed and selected mutants of protocatechuate 3, 4-dioxygenase1. Annu Rev Microbiol 58:555–585

    Article  CAS  Google Scholar 

  • Bugg TD, Ramaswamy S (2008) Non-heme iron-dependent dioxygenases: unravelling catalytic mechanisms for complex enzymatic oxidations. Curr Opin Chem Biol 12:134–140

    Article  CAS  Google Scholar 

  • Bundy BM, Campbell AL, Neidle EL (1998) Similarities between the antABC-encoded anthranilate dioxygenase and the benABC-encoded benzoate dioxygenase of Acinetobacter sp. strain ADP1. J Bacteriol 180:4466–4474

    CAS  Google Scholar 

  • Decker A, Solomon EI (2005) Dioxygen activation by copper, heme and non-heme iron enzymes: comparison of electronic structures and reactivities. Curr Opin Chem Biol 9:152–163

    Article  CAS  Google Scholar 

  • Dunwell JM, Khuri S, Gane PJ (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev 64:153–179

    Article  CAS  Google Scholar 

  • Hirano S, Morikawa M, Takano K, Imanaka T, Kanaya S (2007) Gentisate 1, 2-dioxygenase from Xanthobacter polyaromaticivorans 127 W. Biosci Biotechnol Biochem 71:192–9

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Koehntop KD, Emerson JP, Que L Jr (2005) The 2-His-1-carboxylate facial triad: a versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes. J Biol Inorg Chem 10:87–93

    Article  CAS  Google Scholar 

  • Kovaleva EG, Lipscomb JD (2008) Versatility of biological non-heme Fe(II) centers in oxygen activation reactions. Nat Chem Biol 4:186–93

    Article  CAS  Google Scholar 

  • Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479

    Article  CAS  Google Scholar 

  • Li L, Liu X, Yang W, Xu F, Wang W, Feng L, Bartlam M, Wang L, Rao Z (2008) Crystal structure of long-chain alkane monooxygenase (LadA) in complex with coenzyme FMN: unveiling the long-chain alkane hydroxylase. J Mol Biol 376:453–465

    Article  CAS  Google Scholar 

  • Lipscomb JD (2008) Mechanism of extradiol aromatic ring-cleaving dioxygenases. Curr Opin Struct Biol 18:644–649

    Article  CAS  Google Scholar 

  • Liu YC, Zhou TT, Zhang J, Xu L, Zhang ZH, Shen QR, Shen B (2009) Molecular characterization of the alkB gene in the thermophilic Geobacillus sp. strain MH-1. Res Microbiol 160:560–566

    Article  CAS  Google Scholar 

  • Munro AW, Girvan HM, McLean KJ (2007) Cytochrome P450-redox partner fusion enzymes. Biochim Biophys Acta 1770:345–359

    CAS  Google Scholar 

  • Neidig ML, Solomon EI (2005) Structure–function correlations in oxygen activating non-heme iron enzymes. Chem Commun 47:5843–5863

    Google Scholar 

  • Nordlund P, Eklund H (1995) Di-iron-carboxylate proteins. Curr Opin Struct Biol 5:758–766

    Article  CAS  Google Scholar 

  • Parales RE (2003) The role of active-site residues in naphthalene dioxygenase. J Ind Microbiol Biotechnol 30:271–278

    Article  CAS  Google Scholar 

  • Rieske JS, Maclennan DH, Coleman R (1964) Isolation and properties of an iron-protein from the (reduced coenzyme Q)-cytochrome C reductase complex of the respiratory chain. Biochem Biophys Res Commun 15:338–344

    Article  Google Scholar 

  • Roberts GA, Celik A, Hunter DJ, Ost TW, White JH, Chapman SK, Turner NJ, Flitsch SL (2003) A Self-sufficient Cytochrome P450 with a primary structural organization that includes a Flavin Domain and a [2Fe-2S] Redox Center. J Biol Chem 278:48914–48920

    Article  CAS  Google Scholar 

  • Rosenzweig AC (2008) The metal centres of particulate methane mono-oxygenase. Biochem Soc Trans 36:1134–1137

    Article  CAS  Google Scholar 

  • Senda M, Kishigami S, Kimura S, Fukuda M, Ishida T, Senda T (2007) Molecular mechanism of the redox-dependent interaction between NADH-dependent ferredoxin reductase and Rieske-type [2Fe-2S] ferredoxin. J Mol Biol 373:382–400

    Article  CAS  Google Scholar 

  • Steiner RA, Kalk KH, Dijkstra BW (2002) Anaerobic enzyme substrate structures provide insight into the reaction mechanism of the copper-dependent quercetin 2, 3-dioxygenase. Proc Natl Acad Sci 99:16625–16630

    Article  CAS  Google Scholar 

  • Throne-Holst M, Wentzel A, Ellingsen TE, Kotlar H-K, Zotchev SB (2007) Identification of novel genes involved in long-chain n-alkane degradation by Acinetobacter sp. strain DSM17874. Appl Environ Microbiol 73:3327–3332

    Article  CAS  Google Scholar 

  • Tropel D, Meyer C, Jouanneau Y (2002) Ferredoxin-mediated reactivation of the chlorocatechol 2, 3-dioxygenase from Pseudomonas putida GJ31. Arch Microbiol 177:345–351

    Article  CAS  Google Scholar 

  • Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41:241–67

    Article  CAS  Google Scholar 

  • van Beilen JB, Smits TH, Roos FF, Brunner T, Balada SB, Röthlisberger M, Witholt B (2005) Identification of an amino acid position that determines the substrate range of integral membrane alkane hydroxylases. J Bacteriol 187:85–91

    Article  Google Scholar 

  • van Beilen JB, Funhoff EG, van Loon A, Just A, Kaysser L, Bouza M, Holtackers R, Röthlisberger M, Li Z, Witholt B (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72:59–65

    Article  Google Scholar 

  • van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21

    Article  CAS  Google Scholar 

  • van Berkel WJ, Kamerbeek NM, Fraaije MW (2006) Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J Biotechnol 124:670–689

    Article  Google Scholar 

  • Yamaguchi M, Fujisawa H (1982) Subunit structure of oxygenase component in benzoate-1, 2-dioxygenase system from Pseudomonas arvilla C-1. J Biol Chem 257:12497–12502

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Section of Environmental Biology,Faculty of Environmental Earth Science, Hokkaido University, Sapporo, 060-0810, Japan

    Masaaki Morikawa

Authors
  1. Masaaki Morikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masaaki Morikawa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morikawa, M. Dioxygen activation responsible for oxidation of aliphatic and aromatic hydrocarbon compounds: current state and variants. Appl Microbiol Biotechnol 87, 1595–1603 (2010). https://doi.org/10.1007/s00253-010-2715-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-010-2715-z

Keywords

Search

Navigation