Skip to main content
SpringerLink
Log in

Rieske Non-Heme Iron Dioxygenases: Applications and Future Perspectives

  • Chapter
  • First Online:
Biocatalysis

Abstract

The stereo- and regioselective oxidative functionalization of olefins is amongst the most challenging reactions in organic syntheses. In particular, the catalytic asymmetric dihydroxylation of alkenes has attracted considerable attention due to the facile further transformation of the chiral diol products into valuable derivatives, making them important building blocks for the pharmaceutical and chemical industry. Nature’s creativity in developing solutions for C–H-bond functionalization reactions like hydroxylations at activated or non-activated C–H-bonds is remarkably shown by an impressive list of metal-dependent enzymes. These enzymes, like the Rieske non-heme iron oxygenases (ROs) are able to activate molecular oxygen in order to generate reactive oxygen species capable of hydroxylating alkyl-substrates and they also promote further oxidative transformations. For many of these reactions no ‘classical’ chemical counterpart is known. ROs represent promising biocatalysts for these reactions since they are the only enzymes known to catalyze the stereoselective formation of vicinal cis-diols in one step. They are soluble multicomponent systems that harness the reductive power of NAD(P)H for oxygen activation. Due to their versatility, ROs are considered as the non-heme analogues of cytochrome P450 monooxygenases and, in addition to their relaxed substrate specificity, these enzymes can also catalyze various oxidation reactions, resulting in an enormous potential of these enzymes for manifold synthetically useful transformations. This chapter describes the current understanding of the structural determinants and the catalytic behavior of dioxygenase-catalyzed reactions, and highlights how in several cases this knowledge has been harnessed to design tailored catalysts for the synthesis of various natural products, polyfunctionalized metabolites and pharmaceutical intermediates. Moreover, the chapter also gives insights into recently characterized ROs catalyzing unusual reactions as well as applications in chemo-enzymatic cascade reactions for natural product synthesis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adam D, Bosche L, Castaneda-Losada L, Winkler M, Apfel P, Happe T (2017) Sunlight-dependent hydrogen production by photosensitizer/hydrogenase systems. ChemSusChem 10:894–902

    CAS  PubMed  Google Scholar 

  • Ang EL, Obbard JP, Zhao HM (2009) Directed evolution of aniline dioxygenase for enhanced bioremediation of aromatic amines. Appl Microbiol Biotechnol 81:1063–1070

    CAS  PubMed  Google Scholar 

  • Armengaud J, Timmis KN (1997) Molecular characterization of Fdx1, a putidaredoxin-type [2Fe-2S] ferredoxin able to transfer electrons to the dioxin dioxygenase of Sphingomonas sp. RW1. Eur J Biochem 247:833–842

    CAS  PubMed  Google Scholar 

  • Armengaud J, Gaillard J, Timmis KN (2000) A second [2Fe-2S] ferredoxin from Sphingomonas sp strain RW1 can function as an electron donor for the dioxin dioxygenase. J Bacteriol 182:2238–2244

    CAS  PubMed  PubMed Central  Google Scholar 

  • Axcell BC, Geary PJ (1975) Purification and some properties of a soluble benzene-oxidizing system from a strain of pseudomonas. Biochem J 146:173–183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Badenhorst CPS, Bornscheuer UT (2018) Getting momentum: from biocatalysis to advanced synthetic biology. Trends Biochem Sci 43:180–198

    CAS  PubMed  Google Scholar 

  • Banwell MG, Darmos P, McLeod MD, Hockless DCR (1998) From toluene to taxol (TM): chemoenzymatic and enantiodivergent routes to the AB-ring systems of taxoids and ent-taxoids. Synlett 8:897–899

    Google Scholar 

  • Banwell MG, Hockless DCR, McLeod MD (2003) Chemoenzymatic total syntheses of the sesquiterpene (-)-patchoulenone. New J Chem 27:50–59

    CAS  Google Scholar 

  • Barry SM, Challis GL (2013) Mechanism and catalytic diversity of Rieske non-heme iron-dependent oxygenases. ACS Catal 3:2362–2370

    CAS  Google Scholar 

  • Bassan A, Blomberg MRA, Borowski T, Siegbahn PEM (2004) Oxygen activation by Rieske non-heme iron oxygenases, a theoretical insight. J Phys Chem B 108:13031–13041

    CAS  Google Scholar 

  • Bataille CJR, Donohoe TJ (2011) Osmium-free direct syn-dihydroxylation of alkenes. Chem Soc Rev 40:114–128

    CAS  PubMed  Google Scholar 

  • Behrens GA, Hummel A, Padhi SK, Schatzle S, Bornscheuer UT (2011) Discovery and protein engineering of biocatalysts for organic synthesis. Adv Synth Catal 353:2191–2215

    CAS  Google Scholar 

  • Bernath-Levin K, Shainsky J, Sigawi L, Fishman A (2014) Directed evolution of nitrobenzene dioxygenase for the synthesis of the antioxidant hydroxytyrosol. Appl Microbiol Biotechnol 98:4975–4985

    CAS  PubMed  Google Scholar 

  • Bernhardt R, Urlacher VB (2014) Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations. Appl Microbiol Biotechnol 98:6185–6203

    CAS  PubMed  Google Scholar 

  • Bornscheuer UT (2016) Biocatalysis: successfully crossing boundaries. Angew Chem Int Ed 55:4372–4373

    CAS  Google Scholar 

  • Bornscheuer UT, Huisman GW, Kazlauskas RJ, Lutz S, Moore JC, Robins K (2012) Engineering the third wave of biocatalysis. Nature 485:185–194

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Boyd DR, Sharma ND, Harrison JS, Kennedy MA, Allen CCR, Gibson DT (2001b) Regio- and stereo-selective dioxygenase-catalysed cis-dihydroxylation of fjord-region polycyclic arenes. J Chem Soc Perkin Trans 1:1264–1269

    Google Scholar 

  • Capyk JK, Eltis LD (2012) Phylogenetic analysis reveals the surprising diversity of an oxygenase class. J Biol Inorg Chem 17:425–436

    CAS  PubMed  Google Scholar 

  • Capyk JK, D’Angelo I, Strynadka NC, Eltis LD (2009) Characterization of 3-ketosteroid 9 alpha-hydroxylase, a Rieske oxygenase in the cholesterol degradation pathway of Mycobacterium tuberculosis. J Biol Chem 284:9937–9946

    CAS  PubMed  PubMed Central  Google Scholar 

  • Catterall FA, Williams PA (1971) Some properties of the naphthalene oxygenase from pseudomonas sp. NCIB 9816. Microbiology 67:117–124

    CAS  Google Scholar 

  • Cerdeno AM, Bibb MJ, Challis GL (2001) Analysis of the prodiginine biosynthesis gene cluster of Streptomyces coelicolor A3(2): new mechanisms for chain initiation and termination in modular multienzymes. Chem Biol 8:817–829

    CAS  PubMed  Google Scholar 

  • Chakrabarty S, Austin RN, Deng DY, Groves JT, Lipscomb JD (2007) Radical intermediates in monooxygenase reactions of Rieske dioxygenases. J Am Chem Soc 129:3514–3515

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty J, Ghosal D, Dutta A, Dutta TK (2012) An insight into the origin and functional evolution of bacterial aromatic ring-hydroxylating oxygenases. J Biomol Struct Dyn 30:419–436

    CAS  PubMed  Google Scholar 

  • Chang DL, Zhang J, Witholt B, Li Z (2004) Chemical and enzymatic synthetic methods for asymmetric oxidation of the C-C double bond. Biocatal Biotransformation 22:113–130

    CAS  Google Scholar 

  • Chang EL, Bolte B, Lan P, Willis AC, Banwell MG (2016) Chemoenzymatic total syntheses of the enantiomers of the protoilludanes 8-deoxydihydrotsugicoline and radudiol. J Org Chem 81:2078–2086

    CAS  PubMed  Google Scholar 

  • Chen MM, Coelho PS, Arnold FH (2012) Utilizing terminal oxidants to achieve P450-catalyzed oxidation of methane. Adv Synth Catal 354:964–968

    CAS  Google Scholar 

  • Chica RA, Doucet N, Pelletier JN (2005) Semi-rational approaches to engineering enzyme activity: combining the benefits of directed evolution and rational design. Curr Opin Biotechnol 16:378–384

    CAS  PubMed  Google Scholar 

  • Choi YS, Zhang HJ, Brunzelle JS, Nair SK, Zhao HM (2008) In vitro reconstitution and crystal structure of p-aminobenzoate N-oxygenase (AurF) involved in aureothin biosynthesis. Proc Natl Acad Sci U S A 105:6858–6863

    CAS  PubMed  PubMed Central  Google Scholar 

  • D’Ordine RL, Rydel TJ, Storek MJ, Sturman EJ, Moshiri F, Bartlett RK, Brown GR, Eilers RJ, Dart C, Qi Y, Flasinski S, Franklin SJ (2009) Dicamba monooxygenase: structural insights into a dynamic Rieske oxygenase that catalyzes an exocyclic monooxygenation. J Mol Biol 392:481–497

    PubMed  Google Scholar 

  • Davids T, Schmidt M, Bottcher D, Bornscheuer UT (2013) Strategies for the discovery and engineering of enzymes for biocatalysis. Curr Opin Chem Biol 17:215–220

    CAS  PubMed  Google Scholar 

  • De Mot R, Parret AHA (2002) A novel class of self-sufficient cytochrome P450 monooxygenases in prokaryotes. Trends Microbiol 10:502–508

    PubMed  Google Scholar 

  • Dong J, Fernandez-Fueyo E, Hollmann F, Paul C, Pasic M, Schmidt S, Wang Y, Younes S, Zhang W (2018) Biocatalytic oxidation reactions – a chemist’s perspective. Angew Chem Int Ed 57:9238–9261

    CAS  Google Scholar 

  • Dror A, Fishman A (2012) Engineering non-heme mono- and dioxygenases for biocatalysis. Comput Struct Biotechnol J J2:1–12

    Google Scholar 

  • Elssner T, Preusser A, Wagner U, Kleber HP (1999) Metabolism of L(-)-carnitine by enterobacteriaceae under aerobic conditions. FEMS Microbiol Lett 174:295–301

    CAS  PubMed  Google Scholar 

  • Endoma MA, Bui VP, Hansen J, Hudlicky T (2002) Medium-scale preparation of useful metabolites of aromatic compounds via whole-cell fermentation with recombinant organisms. Org Process Res Dev 6:525–532

    CAS  Google Scholar 

  • Erickson BD, Mondello FJ (1993) Enhanced biodegradation of polychlorinated-biphenyls after site-directed mutagenesis of a biphenyl dioxygenase gene. Appl Environ Microbiol 59:3858–3862

    CAS  PubMed  PubMed Central  Google Scholar 

  • Escalante DE, Aukema KG, Wackett LP, Aksan A (2017) Simulation of the bottleneck controlling access into a Rieske active site: predicting substrates of naphthalene 1,2-dioxygenase. J Chem Inf Model 57:550–561

    CAS  PubMed  Google Scholar 

  • Fernandez-Lafuente R, Guisan JM, Ali S, Cowan D (2000) Immobilization of functionally unstable catechol-2,3-dioxygenase greatly improves operational stability. Enzym Microb Technol 26:568–573

    CAS  Google Scholar 

  • Ferraro DJ, Gakhar L, Ramaswamy S (2005) Rieske business: structure-function of Rieske non-heme oxygenases. Biochem Biophys Res Commun 338:175–190

    CAS  PubMed  Google Scholar 

  • Ferraro DJ, Brown EN, Yu CL, Parales RE, Gibson DT, Ramaswamy S (2007) Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae BI. BMC Struct Biol 7:10

    PubMed  PubMed Central  Google Scholar 

  • Ferraro DJ, Okerlund A, Brown E, Ramaswamy S (2017) One enzyme, many reactions: structural basis for the various reactions catalyzed by naphthalene 1,2-dioxygenase. IUCrJ 4:648–656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gally C, Nestl BM, Hauer B (2015) Engineering Rieske non-heme iron oxygenases for the asymmetric dihydroxylation of alkenes. Angew Chem Int Ed 54:12952–12956

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gibson DT, Koch JR, Kallio RE (1968) Oxidative degradation of aromatic hydrocarbons by microorganisms. I. Enzymatic formation of catechol from benzene. Biochemistry 7:2653–2662

    CAS  PubMed  Google Scholar 

  • Guzik U, Hupert-Kocurek K, Krysiak M, Wojcieszynska D (2014a) Degradation potential of protocatechuate 3,4-dioxygenase from crude extract of Stenotrophomonas maltophilia strain KB2 immobilized in calcium alginate hydrogels and on glyoxyl agarose. Biomed Res Int 2014:1–8

    Google Scholar 

  • Guzik U, Hupert-Kocurek K, Marchlewicz A, Wojcieszynska D (2014b) Enhancement of biodegradation potential of catechol 1,2-dioxygenase through its immobilization in calcium alginate gel. Electron J Biotechnol 17:83–88

    Google Scholar 

  • Halder JM, Nestl BM, Hauer B (2018) Semirational engineering of the naphthalene dioxygenase from Pseudomonas sp NCIB 9816-4 towards selective asymmetric dihydroxylation. ChemCatChem 10:178–182

    CAS  Google Scholar 

  • Hall DO, Cammack R, Rao KK (1971) Role for ferredoxins in the origin of life and biological evolution. Nature 233:136

    CAS  PubMed  Google Scholar 

  • Haynes SW, Sydor PK, Stanley AE, Song LJ, Challis GL (2008) Role and substrate specificity of the Streptomyces coelicolor RedH enzyme in undecylprodiginine biosynthesis. Chem Commun 16:1865–1867

    Google Scholar 

  • Haynes SW, Sydor PK, Corre C, Song LJ, Challis GL (2011) Stereochemical elucidation of Streptorubin B. J Am Chem Soc 133:1793–1798

    CAS  PubMed  Google Scholar 

  • Hibbert EG, Baganz F, Hailes HC, Ward JM, Lye GJ, Woodley JM, Dalby PA (2005) Directed evolution of biocatalytic processes. Biomol Eng 22:11–19

    CAS  PubMed  Google Scholar 

  • Hu DX, Clift MD, Lazarski KE, Thomson RJ (2011) Enantioselective total synthesis and confirmation of the absolute and relative stereochemistry of streptorubin B. J Am Chem Soc 133:1799–1804

    CAS  PubMed  Google Scholar 

  • Hudlicky T, Olivo HF (1992) A short synthesis of (+)-lycoricidine. J Am Chem Soc 114:9694–9696

    CAS  Google Scholar 

  • Hudlicky T, Reed JW (2009) Applications of biotransformations and biocatalysis to complexity generation in organic synthesis. Chem Soc Rev 38:3117–3132

    CAS  PubMed  Google Scholar 

  • Hudlicky T, Fan R, Luna H, Olivo H, Price J (1992) Enzymatic hydroxylation of arene and symmetry considerations in efficient synthetic design of oxygenated natural-products. Pure Appl Chem 64:1109–1113

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen K, Jensen PE, Moller BL (2011) Light-driven cytochrome P450 hydroxylations. ACS Chem Biol 6:533–539

    CAS  PubMed  Google Scholar 

  • Joern JM, Sakamoto T, Arisawa A, Arnold FH (2001) A versatile high throughput screen for dioxygenase activity using solid-phase digital imaging. J Biomol Screen 6:219–223

    CAS  PubMed  Google Scholar 

  • Kalnins G, Sevostjanovs E, Hartmane D, Grinberga S, Tars K (2018) CntA oxygenase substrate profile comparison and oxygen dependency of TMA production in Providencia rettgeri. J Basic Microbiol 58:52–59

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Keenan BG, Leungsakul T, Smets BF, Mori M, Henderson DE, Wood TK (2005) Protein engineering of the archetypal nitroarene dioxygenase of Ralstonia sp strain U2 for activity on aminonitrotoluenes and dinitrotoluenes through alpha-subunit residues leucine 225, phenylalanine 350, and glycine 407. J Bacteriol 187:3302–3310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D, Yoo M, Choi KY, Kang BS, Kim E (2013) Characterization and engineering of an o-xylene dioxygenase for biocatalytic applications. Bioresour Technol 145:123–127

    CAS  PubMed  Google Scholar 

  • Kim JH, Nam DH, Park CB (2014) Nanobiocatalytic assemblies for artificial photosynthesis. Curr Opin Biotechnol 28:1–9

    PubMed  Google Scholar 

  • Kimura N, Nishi A, Goto M, Furukawa K (1997) Functional analyses of a variety of chimeric dioxygenases constructed from two biphenyl dioxygenases that are similar structurally but different functionally. J Bacteriol 179:3936–3943

    CAS  PubMed  PubMed Central  Google Scholar 

  • King-Smith E, Zwick CR 3rd, Renata H (2018) Applications of oxygenases in the chemoenzymatic total synthesis of complex natural products. Biochemistry 57:403–412

    CAS  PubMed  Google Scholar 

  • Kumamaru T, Suenaga H, Mitsuoka M, Watanabe T, Furukawa K (1998) Enhanced degradation of polychlorinated biphenyls by directed evolution of biphenyl dioxygenase. Nat Biotechnol 16:663–666

    CAS  PubMed  Google Scholar 

  • Kumar P, Mohammadi M, Viger JF, Barriault D, Gomez-Gil L, Eltis LD, Bolin JT, Sylvestre M (2011) Structural insight into the expanded PCB-degrading abilities of a biphenyl dioxygenase obtained by directed evolution. J Mol Biol 405:531–547

    CAS  PubMed  Google Scholar 

  • Kumari A, Singh D, Ramaswamy S, Ramanathan G (2017) Structural and functional studies of ferredoxin and oxygenase components of 3-nitrotoluene dioxygenase from Diaphorobacter sp strain DS2. PLoS One 12:1–16

    Google Scholar 

  • Kweon O, Kim SJ, Baek S, Chae JC, Adjei MD, Baek DH, Kim YC, Cerniglia CE (2008) A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem 9:11

    PubMed  PubMed Central  Google Scholar 

  • Landman O, Borovok I, Aharonowitz Y, Cohen G (1997) The glutamine ligand in the ferrous iron active site of isopenicillin N synthase of Streptomyces jumonjinensis is not essential for catalysis. FEBS Lett 405:172–174

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Zhao HM (2006) Mechanistic studies on the conversion of arylamines into arylnitro compounds by aminopyrrolnitrin oxygenase: identification of intermediates and kinetic studies. Angew Chem Int Ed 45:622–625

    CAS  Google Scholar 

  • Lee JK, Simurdiak M, Zhao HM (2005) Reconstitution and characterization of aminopyrrolnitrin oxygenase, a Rieske N-oxygenase that catalyzes unusual arylamine oxidation. J Biol Chem 280:36719–36728

    CAS  PubMed  Google Scholar 

  • Lee JK, Ang EL, Zhao HM (2006) Probing the substrate specificity of aminopyrrolnitrin oxygenase (PrnD) by mutational analysis. J Bacteriol 188:6179–6183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SH, Nam DH, Kim JH, Baeg JO, Park CB (2009) Eosin Y-sensitized artificial photosynthesis by highly efficient visible-light-driven regeneration of nicotinamide cofactor. ChemBioChem 10:1621–1624

    CAS  PubMed  Google Scholar 

  • Lee SH, Kwon YC, Kim DM, Park CB (2013) Cytochrome P450-catalyzed O-dealkylation coupled with photochemical NADPH regeneration. Biotechnol Bioeng 110:383–390

    CAS  PubMed  Google Scholar 

  • Leger C, Lederer F, Guigliarelli B, Bertrand P (2006) Electron flow in multicenter enzymes: theory, applications, and consequences on the natural design of redox chains. J Am Chem Soc 128:180–187

    CAS  PubMed  Google Scholar 

  • Lewis JC, Coelho PS, Arnold FH (2011) Enzymatic functionalization of carbon-hydrogen bonds. Chem Soc Rev 40:2003–2021

    CAS  PubMed  Google Scholar 

  • Leys D, Scrutton NS (2004) Electrical circuitry in biology: emerging principles from protein structure. Curr Opin Struct Biol J 14:642–647

    CAS  Google Scholar 

  • Li C, Zhang L, Zhang C, Hirao H, Wu W, Shaik S (2007) Which oxidant is really responsible for sulfur oxidation by cytochrome p450? Angew Chem Int Ed 46:8168–8170

    CAS  Google Scholar 

  • Liu HH, Xu LQ, Yao K, Xiong LB, Tao XY, Liu M, Wang FQ, Wei DZ (2018) Engineered 3-ketosteroid 9 alpha-hydroxylases in Mycobacterium neoaurum: an efficient platform for production of steroid drugs. Appl Environ Microbiol 84(14):e02777–e02717

    PubMed  PubMed Central  Google Scholar 

  • Mahan KM, Penrod JT, Ju KS, Al Kass N, Tan WA, Truong R, Parales JV, Parales RE (2015) Selection for growth on 3-nitrotoluene by 2-nitrotoluene-utilizing acidovorax sp strain JS42 identifies nitroarene dioxygenases with altered specificities. Appl Environ Microbiol 81:309–319

    PubMed  Google Scholar 

  • Mahenthiralingam E, Song LJ, Sass A, White J, Wilmot C, Marchbank A, Boaisha O, Paine J, Knight D, Challis GL (2011) Enacyloxins are products of an unusual hybrid modular polyketide synthase encoded by a cryptic Burkholderia ambifaria genomic island. Chem Biol 18:665–677

    CAS  PubMed  Google Scholar 

  • Mason JR, Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305

    CAS  PubMed  Google Scholar 

  • Mathews FS, White S (1993) Electron-transfer proteins enzymes. Curr Opin Struct Biol J 3:902–911

    CAS  Google Scholar 

  • Matsui T, Dekishima Y, Ueda M (2014) Biotechnological production of chiral organic sulfoxides: current state and perspectives. Appl Microbiol Biotechnol 98:7699–7706

    CAS  PubMed  Google Scholar 

  • Mohammadi M, Viger JF, Kumar P, Barriault D, Bolin JT, Sylvestre M (2011) Retuning Rieske-type oxygenases to expand substrate range. J Biol Chem 286:27612–27621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morley KL, Kazlauskas RJ (2005) Improving enzyme properties: when are closer mutations better? Trends Biotechnol 23:231–237

    CAS  PubMed  Google Scholar 

  • Munro AW, Leys DG, McLean KJ, Marshall KR, Ost TWB, Daff S, Miles CS, Chapman SK, Lysek DA, Moser CC, Page CC, Dutton PL (2002) P450 BM3: the very model of a modern flavocytochrome. Trends Biochem Sci 27:250–257

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Mykles DL (2011) Ecdysteroid metabolism in crustaceans. J Steroid Biochem 127:196–203

    CAS  Google Scholar 

  • Nazor J, Dannenmann S, Adjei RO, Fordjour YB, Ghampson IT, Blanusa M, Roccatano D, Schwaneberg U (2008) Laboratory evolution of P450 BM3 for mediated electron transfer yielding an activity-improved and reductase-independent variant. Protein Eng Des Sel 21:29–35

    CAS  PubMed  Google Scholar 

  • Ohta T, Chakrabarty S, Lipscomb JD, Solomon EI (2008) Near-IR MCD of the nonheme ferrous active site in naphthalene 1,2-dioxygenase: correlation to crystallography and structural insight into the mechanism of Rieske dioxygenases. J Am Chem Soc 130:1601–1610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Page CC, Moser CC, Dutton PL (2003) Mechanism for electron transfer within and between proteins. Curr Opin Chem Biol 7:551–556

    CAS  PubMed  Google Scholar 

  • Papireddy K, Smilkstein M, Kelly JX, Shweta, Salem SM, Alhamadsheh M, Haynes SW, Challis GL, Reynolds KA (2011) Antimalarial activity of natural and synthetic prodiginines. J Med Chem 54:5296–5306

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Parales RE, Resnick SM (2004) Aromatic hydrocarbon dioxygenases. In: Singh A, Ward OP (eds) Biodegradation and bioremediation. Springer, Heidelberg, pp 175–195

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park JH, Lee SH, Cha GS, Choi DS, Nam DH, Lee JH, Lee JK, Yun CH, Jeong KJ, Park CB (2015) Cofactor-free light-driven whole-cell cytochrome P450 catalysis. Angew Chem Int Ed 54:969–973

    CAS  Google Scholar 

  • Pfender WF, Kraus J, Loper JE (1993) A genomic region from pseudomonas-fluorescens Pf-5 required for pyrrolnitrin production and inhibition of pyrenophora-tritici-repentis in wheat-straw. Phytopathology 83:1223–1228

    CAS  Google Scholar 

  • Pollmann K, Wray V, Hecht HJ, Pieper DH (2003) Rational engineering of the regioselectivity of TecA tetrachlorobenzene dioxygenase for the transformation of chlorinated toluenes. Microbiology 149:903–913

    CAS  PubMed  Google Scholar 

  • Punniyamurthy T, Velusamy S, Iqbal J (2005) Recent advances in transition metal catalyzed oxidation of organic substrates with molecular oxygen. Chem Rev 105:2329–2363

    CAS  PubMed  Google Scholar 

  • Reetz MT (2013) The importance of additive and non-additive mutational effects in protein engineering. Angew Chem Int Ed 52:2658–2666

    CAS  Google Scholar 

  • Reetz MT, Kahakeaw D, Lohmer R (2008) Addressing the numbers problem in directed evolution. ChemBioChem 9:1797–1804

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Rinner U, Hudlicky T (2012) Synthesis of morphine alkaloids and derivatives. Top Curr Chem 309:33–66

    CAS  PubMed  Google Scholar 

  • Rivard BS, Rogers MS, Marell DJ, Neibergall MB, Chakrabarty S, Cramer CJ, Lipscomb JD (2015) Rate-determining attack on substrate precedes rieske cluster oxidation during cis-dihydroxylation by benzoate dioxygenase. Biochemistry 54:4652–4664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roach PL, Clifton IJ, Hensgens CMH, Shibata N, Schofield CJ, Hajdu J, Baldwin JE (1997) Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation. Nature 387:827–830

    CAS  PubMed  Google Scholar 

  • Robledo-Ortiz JR, Ramirez-Arreola DE, Perez-Fonseca AA, Gomez C, Gonzalez-Reynoso O, Ramos-Quirarte J, Gonzalez-Nunez R (2011) Benzene, toluene, and o-xylene degradation by free and immobilized P. putida F1 of postconsumer agave-fiber/polymer foamed composites. Int Biodeterior Biodegrad 65:539–546

    CAS  Google Scholar 

  • Sakamoto T, Joern JM, Arisawa A, Arnold FH (2001) Laboratory evolution of toluene dioxygenase to accept 4-picoline as a substrate. Appl Environ Microbiol 67:3882–3887

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sami M, Brown TJN, Roach PL, Schofield CJ, Jack E (1997) Glutamine-330 is not essential for activity in isopenicillin N synthase from Aspergillus nidulans. FEBS Lett 405:191–194

    CAS  PubMed  Google Scholar 

  • Sathapondecha P, Panyim S, Udomkit A (2017) An essential role of Rieske domain oxygenase Neverland in the molting cycle of black tiger shrimp, Penaeus monodon. Comp Biochem Physiol A Mol Integr Physiol 213:11–19

    CAS  PubMed  Google Scholar 

  • Sauber K, Frohner C, Rosenberg G, Eberspacher J, Lingens F (1977) Purification and properties of pyrazon dioxygenase from pyrazon-degrading bacteria. Eur J Biochem 74:89–97

    CAS  PubMed  Google Scholar 

  • Scheps D, Malca SH, Richter SM, Marisch K, Nestl BM, Hauer B (2013) Synthesis of omega-hydroxy dodecanoic acid based on an engineered CYP153A fusion construct. Microb Biotechnol 6:694–707

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt S, Blom JF, Pernthaler J, Berg G, Baldwin A, Mahenthiralingam E, Eberl L (2009) Production of the antifungal compound pyrrolnitrin is quorum sensing-regulated in members of the Burkholderia cepacia complex. Environ Microbiol 11:1422–1437

    PubMed  Google Scholar 

  • Schmidt S, Scherkus C, Muschiol J, Menyes U, Winkler T, Hummel W, Groger H, Liese A, Herz HG, Bornscheuer UT (2015) An enzyme cascade synthesis of epsilon-caprolactone and its oligomers. Angew Chem Int Ed 54:2784–2787

    CAS  Google Scholar 

  • Seo J, Ryu JY, Han J, Ahn JH, Sadowsky MJ, Hur HG, Chong Y (2013) Amino acid substitutions in naphthalene dioxygenase from Pseudomonas sp strain NCIB 9816-4 result in regio- and stereo-specific hydroxylation of flavanone and isoflavanone. Appl Microbiol Biotechnol 97:693–704

    CAS  PubMed  Google Scholar 

  • Shainsky J, Bernath-Levin K, Isaschar-Ovdat S, Glaser F, Fishman A (2013) Protein engineering of nirobenzene dioxygenase for enantioselective synthesis of chiral sulfoxides. Protein Eng Des Sel 26:335–345

    CAS  PubMed  Google Scholar 

  • Stanley AE, Walton LJ, Zerikly MK, Corre C, Challis GL (2006) Elucidation of the Streptomyces coelicolor pathway to 4-methoxy-2, 2′-bipyrrole-5-carboxaldehyde, an intermediate in prodiginine biosynthesis. Chem Commun 15:3981–3983

    Google Scholar 

  • Steiner K, Schwab H (2012) Recent advances in rational approaches for enzyme engineering. Comput Struct Biotechnol J J2:1–12

    Google Scholar 

  • Suenaga H, Watanabe T, Sato M, Ngadiman, Furukawa K (2002) Alteration of regiospecificity in biphenyl dioxygenase by active-site engineering. J Bacteriol 184:3682–3688

    CAS  PubMed  PubMed Central  Google Scholar 

  • Summers RM, Louie TM, Yu CL, Gakhar L, Louie KC, Subramanian M (2012) Novel, highly specific N-demethylases enable bacteria to live on caffeine and related purine alkaloids. J Bacteriol 194:2041–2049

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sydor PK, Barry SM, Odulate OM, Barona-Gomez F, Haynes SW, Corre C, Song LJ, Challis GL (2011) Regio- and stereodivergent antibiotic oxidative carbocyclizations catalysed by Rieske oxygenase-like enzymes. Nat Chem 3:388–392

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan WA, Parales RE (2016) Application of aromatic hydrocarbon dioxygenases. In: Davis UC (ed) Green biocatalysis. Wiley, Hoboken, NJ

    Google Scholar 

  • Thebtaranonth C, Thebtaranonth Y, Wanauppathamkul S, Yuthavong Y (1995) Antimalarial sesquiterpenes from tubers of Cyperus-rotundus – structure of 10,12-peroxycalamenene, a sesquiterpene endoperoxide. Phytochemistry 40:125–128

    CAS  PubMed  Google Scholar 

  • Thomas H, Dirk NJ (1993) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481

    Google Scholar 

  • Torres Pazmiño DE, Winkler M, Glieder A, Fraaije MW (2010) Monooxygenases as biocatalysts: classification, mechanistic aspects and biotechnological applications. J Biotechnol 146:9–24

    PubMed  Google Scholar 

  • Tran NH, Nguyen D, Dwaraknath S, Mahadevan S, Chavez G, Nguyen A, Dao T, Mullen S, Nguyen TA, Cheruzel LE (2013) An efficient light-driven P450 BM3 biocatalyst. J Am Chem Soc 135:14484–14487

    CAS  PubMed  PubMed Central  Google Scholar 

  • Udit AK, Hill MG, Gray HB (2006) Electrochemistry of cytochrome P450BM3 in sodium dodecyl sulfate films. Langmuir 22:10854–10857

    CAS  PubMed  PubMed Central  Google Scholar 

  • van Beilen JB, Duetz WA, Schmid A, Witholt B (2003) Practical issues in the application of oxygenases. Trends Biotechnol 21:170–177

    PubMed  Google Scholar 

  • Van der Geize R, Yam K, Heuser T, Wilbrink MH, Hara H, Anderton MC, Sim E, Dijkhuizen L, Davies JE, Mohn WW, Eltis LD (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci USA 104:1947–1952

    PubMed  Google Scholar 

  • Varghese V, Hudlicky T (2014) Short chemoenzymatic total synthesis of ent-hydromorphone: an oxidative dearomatization/intramolecular [4+2] cycloaddition/amination sequence. Angew Chem Int Ed 53:4355–4358

    CAS  Google Scholar 

  • Winkler M, Heil B, Heil B, Happe T (2002) Isolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca. Biochim Biophys Acta 1576:330–334

    CAS  PubMed  Google Scholar 

  • Winkler M, Hemschemeier A, Jacobs J, Stripp S, Happe T (2010) Multiple ferredoxin isoforms in Chlamydomonas reinhardtii – their role under stress conditions and biotechnological implications. Eur J Cell Biol 89:998–1004

    CAS  PubMed  Google Scholar 

  • Wollam J, Magomedova L, Magner DB, Shen YD, Rottiers V, Motola DL, Mangelsdorf DJ, Cummins CL, Antebi A (2011) The Rieske oxygenase DAF-36 functions as a cholesterol 7-desaturase in steroidogenic pathways governing longevity. Aging Cell 10:879–884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshiyama-Yanagawa T, Enya S, Shimada-Niwa Y, Yaguchi S, Haramoto Y, Matsuya T, Shiomi K, Sasakura Y, Takahashi S, Asashima M, Kataoka H, Niwa R (2011) The conserved Rieske oxygenase DAF-36/Neverland is a novel cholesterol-metabolizing enzyme. J Biol Chem 286:25756–25762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu CL, Parales RE, Gibson DT (2001) Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enantioselectivity. J Ind Microbiol Biotechnol 27:94–103

    CAS  PubMed  Google Scholar 

  • Zaitsev AB, Adolfsson H (2006) Recent developments in asymmetric dihydroxylations. Synthesis-Stuttgart 37:1725–1756

    Google Scholar 

  • Zhang WY, Hollmann F (2018) Nonconventional regeneration of redox enzymes – a practical approach for organic synthesis? Chem Commun 54:7281–7289

    CAS  Google Scholar 

  • Zhang W, Liu Y, Yan JY, Cao SN, Bai FL, Yang Y, Huang SH, Yao LS, Anzai Y, Kato F, Podust LM, Sherman DH, Li SY (2014) New reactions and products resulting from alternative interactions between the P450 enzyme and redox partners. J Am Chem Soc 136:3640–3646

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu YJ, Jameson E, Crosatti M, Schafer H, Rajakumar K, Bugg TDH, Chen Y (2014) Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota. Proc Natl Acad Sci U S A 111:4268–4273

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This project has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 764920.

Author information

Authors and Affiliations

  1. Institute of Molecular Biotechnology, Graz University of Technology, Graz, Austria

    Fatma Feyza Özgen & Sandy Schmidt

Authors
  1. Fatma Feyza Özgen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandy Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandy Schmidt .

Editor information

Editors and Affiliations

  1. Department of Biochemistry, Aligarh Muslim University, Aligarh, India

    Qayyum Husain

  2. Department of Medical Laboratory Technology, FAMS, University of Tabuk, Tabuk, Saudi Arabia

    Mohammad Fahad Ullah

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Özgen, F.F., Schmidt, S. (2019). Rieske Non-Heme Iron Dioxygenases: Applications and Future Perspectives. In: Husain, Q., Ullah, M. (eds) Biocatalysis. Springer, Cham. https://doi.org/10.1007/978-3-030-25023-2_4

Download citation

Publish with us

Policies and ethics

Search

Navigation