3en1 Citations

Structures of the multicomponent Rieske non-heme iron toluene 2,3-dioxygenase enzyme system.

OpenAccess logo Acta Crystallogr D Biol Crystallogr 65 24-33 (2009)
Related entries: 3dqy, 3ef6, 3eqq

Cited: 31 times
EuropePMC logo PMID: 19153463

Abstract

Bacterial Rieske non-heme iron oxygenases catalyze the initial hydroxylation of aromatic hydrocarbon substrates. The structures of all three components of one such system, the toluene 2,3-dioxygenase system, have now been determined. This system consists of a reductase, a ferredoxin and a terminal dioxygenase. The dioxygenase, which was cocrystallized with toluene, is a heterohexamer containing a catalytic and a structural subunit. The catalytic subunit contains a Rieske [2Fe-2S] cluster and mononuclear iron at the active site. This iron is not strongly bound and is easily removed during enzyme purification. The structures of the enzyme with and without mononuclear iron demonstrate that part of the structure is flexible in the absence of iron. The orientation of the toluene substrate in the active site is consistent with the regiospecificity of oxygen incorporation seen in the product formed. The ferredoxin is Rieske type and contains a [2Fe-2S] cluster close to the protein surface. The reductase belongs to the glutathione reductase family of flavoenzymes and consists of three domains: an FAD-binding domain, an NADH-binding domain and a C-terminal domain. A model for electron transfer from NADH via FAD in the reductase and the ferredoxin to the terminal active-site mononuclear iron of the dioxygenase is proposed.

Articles - 3en1 mentioned but not cited (8)

  1. Quaternary ammonium oxidative demethylation: X-ray crystallographic, resonance Raman, and UV-visible spectroscopic analysis of a Rieske-type demethylase. Daughtry KD, Xiao Y, Stoner-Ma D, Cho E, Orville AM, Liu P, Allen KN. J. Am. Chem. Soc. 134 2823-2834 (2012)
  2. Structures of the multicomponent Rieske non-heme iron toluene 2,3-dioxygenase enzyme system. Friemann R, Lee K, Brown EN, Gibson DT, Eklund H, Ramaswamy S. Acta Crystallogr. D Biol. Crystallogr. 65 24-33 (2009)
  3. Dearomative dihydroxylation with arenophiles. Southgate EH, Pospech J, Fu J, Holycross DR, Sarlah D. Nat Chem 8 922-928 (2016)
  4. Structural and Biochemical Analysis Reveals a Distinct Catalytic Site of Salicylate 5-Monooxygenase NagGH from Rieske Dioxygenases. Hou YJ, Guo Y, Li DF, Zhou NY. Appl Environ Microbiol 87 e01629-20 (2021)
  5. Toluene Dioxygenase-Catalyzed cis-Dihydroxylation of Quinolines: A Molecular Docking Study and Chemoenzymatic Synthesis of Quinoline Arene Oxides. Boyd DR, Sharma ND, Loke PL, Carroll JG, Stevenson PJ, Hoering P, Allen CCR. Front Bioeng Biotechnol 8 619175 (2020)
  6. Fluoro-recognition: New in vivo fluorescent assay for toluene dioxygenase probing induction by and metabolism of polyfluorinated compounds. Aukema KG, Bygd MD, Tassoulas LJ, Richman JE, Wackett LP. Environ Microbiol 24 5202-5216 (2022)
  7. Structural and biochemical characterization of the key components of an auxin degradation operon from the rhizosphere bacterium Variovorax. Ma Y, Li X, Wang F, Zhang L, Zhou S, Che X, Yu D, Liu X, Li Z, Sun H, Yu G, Zhang H. PLoS Biol 21 e3002189 (2023)
  8. The α- and β-Subunit Boundary at the Stem of the Mushroom-Like α3β3-Type Oxygenase Component of Rieske Non-Heme Iron Oxygenases Is the Rieske-Type Ferredoxin-Binding Site. Tsai PC, Chakraborty J, Suzuki-Minakuchi C, Terada T, Kotake T, Matsuzawa J, Okada K, Nojiri H. Appl Environ Microbiol 88 e0083522 (2022)


Reviews citing this publication (3)

  1. Structural and molecular genetic analyses of the bacterial carbazole degradation system. Nojiri H. Biosci. Biotechnol. Biochem. 76 1-18 (2012)
  2. Engineering Rieske oxygenase activity one piece at a time. Brimberry M, Garcia AA, Liu J, Tian J, Bridwell-Rabb J. Curr Opin Chem Biol 72 102227 (2023)
  3. Monooxygenase- and Dioxygenase-Catalyzed Oxidative Dearomatization of Thiophenes by Sulfoxidation, cis-Dihydroxylation and Epoxidation. Boyd DR, Sharma ND, Stevenson PJ, Hoering P, Allen CCR, Dansette PM. Int J Mol Sci 23 909 (2022)

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  2. Structural features in the KshA terminal oxygenase protein that determine substrate preference of 3-ketosteroid 9α-hydroxylase enzymes. Petrusma M, Dijkhuizen L, van der Geize R. J. Bacteriol. 194 115-121 (2012)
  3. Degradation of chloroaromatics by Pseudomonas putida GJ31: assembled route for chlorobenzene degradation encoded by clusters on plasmid pKW1 and the chromosome. Kunze M, Zerlin KF, Retzlaff A, Pohl JO, Schmidt E, Janssen DB, Vilchez-Vargas R, Pieper DH, Reineke W. Microbiology (Reading, Engl.) 155 4069-4083 (2009)
  4. Characterization of the anthranilate degradation pathway in Geobacillus thermodenitrificans NG80-2. Liu X, Dong Y, Li X, Ren Y, Li Y, Wang W, Wang L, Feng L. Microbiology (Reading, Engl.) 156 589-595 (2010)
  5. Suppression of electron transfer to dioxygen by charge transfer and electron transfer complexes in the FAD-dependent reductase component of toluene dioxygenase. Lin TY, Werther T, Jeoung JH, Dobbek H. J. Biol. Chem. 287 38338-38346 (2012)
  6. Active-site loop variations adjust activity and selectivity of the cumene dioxygenase. Heinemann PM, Armbruster D, Hauer B. Nat Commun 12 1095 (2021)
  7. Toluene Dioxygenase-Catalysed Oxidation of Benzyl Azide to Benzonitrile: Mechanistic Insights for an Unprecedented Enzymatic Transformation. Vila MA, Pazos M, Iglesias C, Veiga N, Seoane G, Carrera I. Chembiochem 17 291-295 (2016)
  8. Less is more: reduced catechol production permits Pseudomonas putida F1 to grow on styrene. George KW, Hay A. Microbiology (Reading, Engl.) 158 2781-2788 (2012)
  9. The iron-sulfur core in Rieske proteins is not symmetric. Ali ME, Nair NN, Retegan M, Neese F, Staemmler V, Marx D. J Biol Inorg Chem 19 1287-1293 (2014)
  10. Crystal structure of NADH:rubredoxin oxidoreductase from Clostridium acetobutylicum: a key component of the dioxygen scavenging system in obligatory anaerobes. Nishikawa K, Shomura Y, Kawasaki S, Niimura Y, Higuchi Y. Proteins 78 1066-1070 (2010)
  11. Custom tuning of Rieske oxygenase reactivity. Tian J, Liu J, Knapp M, Donnan PH, Boggs DG, Bridwell-Rabb J. Nat Commun 14 5858 (2023)
  12. Leveraging a Structural Blueprint to Rationally Engineer the Rieske Oxygenase TsaM. Tian J, Garcia AA, Donnan PH, Bridwell-Rabb J. Biochemistry 62 1807-1822 (2023)
  13. NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction. Sutherlin KD, Rivard BS, Böttger LH, Liu LV, Rogers MS, Srnec M, Park K, Yoda Y, Kitao S, Kobayashi Y, Saito M, Seto M, Hu M, Zhao J, Lipscomb JD, Solomon EI. J. Am. Chem. Soc. 140 5544-5559 (2018)
  14. The reduction rates of DEPC-modified mutant Thermus thermophilus Rieske proteins differ when there is a negative charge proximal to the cluster. Karagas NE, Jones CN, Osborn DJ, Dzierlenga AL, Oyala P, Konkle ME, Whitney EM, David Britt R, Hunsicker-Wang LM. J. Biol. Inorg. Chem. 19 1121-1135 (2014)
  15. Contrasting Mechanisms of Aromatic and Aryl-Methyl Substituent Hydroxylation by the Rieske Monooxygenase Salicylate 5-Hydroxylase. Rogers MS, Gordon AM, Rappe TM, Goodpaster JD, Lipscomb JD. Biochemistry 62 507-523 (2023)
  16. Design principles for site-selective hydroxylation by a Rieske oxygenase. Liu J, Tian J, Perry C, Lukowski AL, Doukov TI, Narayan ARH, Bridwell-Rabb J. Nat Commun 13 255 (2022)
  17. Evaluation of aromatic hydrocarbon decomposition catalyzed by the dioxygenase system and substitution of ferredoxin and ferredoxin reductase. Yang JW, Cho W, Lim Y, Park S, Lee D, Jang HA, Kim HS. Environ Sci Pollut Res Int (2018)
  18. Light-driven Oxidative Demethylation Reaction Catalyzed by a Rieske-type Non-heme Iron Enzyme Stc2. Hu WY, Li K, Weitz A, Wen A, Kim H, Murray JC, Cheng R, Chen B, Naowarojna N, Grinstaff MW, Elliott SJ, Chen JS, Liu P. ACS Catal 12 14559-14570 (2022)
  19. Structural and functional studies of ferredoxin and oxygenase components of 3-nitrotoluene dioxygenase from Diaphorobacter sp. strain DS2. Kumari A, Singh D, Ramaswamy S, Ramanathan G. PLoS ONE 12 e0176398 (2017)
  20. The NADH recycling enzymes TsaC and TsaD regenerate reducing equivalents for Rieske oxygenase chemistry. Tian J, Boggs DG, Donnan PH, Barroso GT, Garcia AA, Dowling DP, Buss JA, Bridwell-Rabb J. J Biol Chem 299 105222 (2023)


Related citations provided by authors (1)

  1. Purification, crystallization and preliminary X-ray diffraction studies of the three components of the toluene 2,3-dioxygenase enzyme system. Lee K, Friemann R, Parales JV, Gibson DT, Ramaswamy S Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61 669-672 (2005)