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Title: NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction

Journal Article · · Journal of the American Chemical Society
DOI:https://doi.org/10.1021/jacs.8b01822· OSTI ID:1465137
 [1];  [2];  [1];  [1];  [2];  [3];  [4];  [5];  [6];  [6];  [6];  [6];  [7];  [7]; ORCiD logo [2]; ORCiD logo [8]
  1. Stanford Univ., CA (United States). Dept. of Chemistry
  2. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Biochemistry, Molecular Biology, & Biophysics
  3. Stanford Univ., CA (United States). Dept. of Chemistry; Academy of Sciences of the Czech Republic (ASCR), Prague (Czech Republic). J. Heyrovsky Inst. of Physical Chemistry
  4. Stanford Univ., CA (United States). Dept. of Chemistry; Korea Advanced Inst. Science and Technology (KAIST), Daejeon (Korea, Republic of). Dept. of Chemistry
  5. Japan Synchrotron Radiation Research Inst., Hyogo (Japan)
  6. Kyoto Univ. (Japan). Research Reactor Inst.
  7. Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
  8. Stanford Univ., CA (United States). Dept. of Chemistry; SLAC National Accelerator Lab., Menlo Park, CA (United States)
+ Show Author Affiliations

The Rieske dioxygenases are a major subclass of mononuclear nonheme iron enzymes that play an important role in bioremediation. Recently, a high-spin FeIII-(hydro)-peroxy intermediate (BZDOp) has been trapped in the peroxide shunt reaction of benzoate 1,2-dioxygenase. Here, defining the structure of this intermediate is essential to understanding the reactivity of these enzymes. Nuclear resonance vibrational spectroscopy (NRVS) is a recently developed synchrotron technique that is ideal for obtaining vibrational, and thus structural, information on Fe sites, as it gives complete information on all vibrational normal modes containing Fe displacement. In this study, we present NRVS data on BZDOp and assign its structure using these data coupled to experimentally calibrated density functional theory calculations. From this NRVS structure, we define the mechanism for the peroxide shunt reaction. The relevance of the peroxide shunt to the native Fe-II/O2 reaction is evaluated. For the native FeII/O2 reaction, an FeIII-superoxo intermediate is found to react directly with substrate. This process, while uphill thermodynamically, is found to be driven by the highly favorable thermodynamics of proton-coupled electron transfer with an electron provided by the Rieske [2Fe-2S] center at a later step in the reaction. Finally, these results offer important insight into the relative reactivities of FeIII-superoxo and FeIII-hydroperoxo species in nonheme Fe biochemistry.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
National Institutes of Health (NIH); Japan Society for the Promotion of Science (JSPS). KAKENHI; USDOE Office of Science (SC)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1465137
Journal Information:
Journal of the American Chemical Society, Vol. 140, Issue 16; ISSN 0002-7863
Publisher:
American Chemical Society (ACS)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 23 works
Citation information provided by
Web of Science

References (82)

Benzoate 1,2-Dioxygenase from Pseudomonas putida :  Single Turnover Kinetics and Regulation of a Two-Component Rieske Dioxygenase † journal July 2002
Modeling nuclear resonance vibrational spectroscopic data of binuclear nonheme iron enzymes using density functional theory journal October 2014
Structure and reactivity of a mononuclear non-haem iron(III)–peroxo complex journal October 2011
On the Theory of Oxidation‐Reduction Reactions Involving Electron Transfer. I journal May 1956
Direct Spectroscopic Evidence for a High-Spin Fe(IV) Intermediate in Tyrosine Hydroxylase journal September 2007
One enzyme, many reactions: structural basis for the various reactions catalyzed by naphthalene 1,2-dioxygenase journal August 2017
Structures of the multicomponent Rieske non-heme iron toluene 2,3-dioxygenase enzyme system journal December 2008
Trapping and spectroscopic characterization of an FeIII-superoxo intermediate from a nonheme mononuclear iron-containing enzyme journal September 2010
Rieske business: Structure–function of Rieske non-heme oxygenases journal December 2005
Mechanism and Catalytic Diversity of Rieske Non-Heme Iron-Dependent Oxygenases journal September 2013
Inner-Sphere Reorganization Energy of Iron−Sulfur Clusters Studied with Theoretical Methods journal April 2001
Determining Rieske cluster reduction potentials journal August 2008
Accurate spin-dependent electron liquid correlation energies for local spin density calculations: a critical analysis journal August 1980
Radical Intermediates in Monooxygenase Reactions of Rieske Dioxygenases journal March 2007
Redox potential of the Rieske iron–sulfur protein journal March 2010
Theoretical relations among rate constants, barriers, and Broensted slopes of chemical reactions journal March 1968
Versatility of biological non-heme Fe(II) centers in oxygen activation reactions journal February 2008
Spectroscopic Evidence for the Two C–H-Cleaving Intermediates of Aspergillus nidulans Isopenicillin N Synthase journal July 2016
The catalytic pocket of the ring-hydroxylating dioxygenase from Sphingomonas CHY-1 journal January 2007
Perferryl Fe V –Oxo Nonheme Complexes: Do They Have High-Spin or Low-Spin Ground States? journal August 2011
Phonon Density of States Measured by Inelastic Nuclear Resonant Scattering journal May 1995
High-valent nonheme iron-oxo complexes: Synthesis, structure, and spectroscopy journal January 2013
Self‐consistent molecular orbital methods. XX. A basis set for correlated wave functions journal January 1980
Specific Interactions between the Ferredoxin and Terminal Oxygenase Components of a Class IIB Rieske Nonheme Iron Oxygenase, Carbazole 1,9a-Dioxygenase journal September 2009
Definition of the intermediates and mechanism of the anticancer drug bleomycin using nuclear resonance vibrational spectroscopy and related methods journal December 2010
A DFT Study of the cis -Dihydroxylation of Nitroaromatic Compounds Catalyzed by Nitrobenzene Dioxygenase journal January 2014
Mechanism of O 2 activation and substrate hydroxylation in noncoupled binuclear copper monooxygenases journal October 2016
Nuclear Resonance Vibrational Spectroscopic Definition of Peroxy Intermediates in Nonheme Iron Sites journal October 2016
A DFT and ONIOM study of C–H hydroxylation catalyzed by nitrobenzene 1,2-dioxygenase journal January 2014
Cyclizations of Alkynes: Revisiting Baldwin’s Rules for Ring Closure journal November 2011
Isolation and properties of an iron-protein from the (reduced coenzyme Q)-cytochrome C reductase complex of the respiratory chain journal April 1964
VTVH-MCD and DFT Studies of Thiolate Bonding to {FeNO} 7 /{FeO 2 } 8 Complexes of Isopenicillin N Synthase:  Substrate Determination of Oxidase versus Oxygenase Activity in Nonheme Fe Enzymes journal June 2007
Spectroscopy and Kinetics of Wild-Type and Mutant Tyrosine Hydroxylase: Mechanistic Insight into O 2 Activation journal June 2009
Phenol-Induced O–O Bond Cleavage in a Low-Spin Heme–Peroxo–Copper Complex: Implications for O 2 Reduction in Heme–Copper Oxidases journal June 2017
Diverse reactions catalyzed by naphthalene dioxygenase fromPseudomonas sp strain NCIB 9816 journal November 1996
Oxygen activation in extradiol catecholate dioxygenases – a density functional study journal January 2012
Gaussian basis sets for molecular wavefunctions containing third-row atoms journal January 1971
Crystal Structure of Naphthalene Dioxygenase: Side-on Binding of Dioxygen to Iron journal February 2003
Engineering dioxygenases for efficient degradation of environmental pollutants journal June 2000
Substrate Binding to NO−Ferro−Naphthalene 1,2-Dioxygenase Studied by High-Resolution Q-Band Pulsed 2 H-ENDOR Spectroscopy journal June 2003
Peroxide Activation for Electrophilic Reactivity by the Binuclear Non-heme Iron Enzyme AurF journal May 2017
Gaussian basis sets for molecular calculations. The representation of 3 d orbitals in transition‐metal atoms journal May 1977
Spectroscopic and Electronic Structure Studies of 2,3-Dihydroxybiphenyl 1,2-Dioxygenase:  O 2 Reactivity of the Non-Heme Ferrous Site in Extradiol Dioxygenases journal September 2003
Density‐functional thermochemistry. III. The role of exact exchange journal April 1993
Aspartate 205 in the Catalytic Domain of Naphthalene Dioxygenase Is Essential for Activity journal March 1999
Directly Relating Gas-Phase Cluster Measurements to Solution-Phase Hydrolysis, the Absolute Standard Hydrogen Electrode Potential, and the Absolute Proton Solvation Energy journal June 2009
Observation of Nuclear Resonant Scattering Accompanied by Phonon Excitation Using Synchrotron Radiation journal May 1995
Initial reactions in the oxidation of naphthalene by Pseudomonas putida journal February 1975
Geometric and Electronic Structure/Function Correlations in Non-Heme Iron Enzymes journal January 2000
Structure of isopenicillinN synthase complexed with substrate and the mechanism ofpenicillin formation journal June 1997
Hydrogen Peroxide-coupled cis-Diol Formation Catalyzed by Naphthalene 1,2-Dioxygenase journal January 2003
Structural insight into the substrate- and dioxygen-binding manner in the catalytic cycle of rieske nonheme iron oxygenase system, carbazole 1,9a-dioxygenase journal January 2012
Geometric and Electronic Structure Contributions to Function in Non-heme Iron Enzymes journal July 2013
Spectroscopic Studies of Substrate Interactions with Clavaminate Synthase 2, a Multifunctional α-KG-Dependent Non-Heme Iron Enzyme:  Correlation with Mechanisms and Reactivities journal July 2001
Comparison of High-Spin and Low-Spin Nonheme FeIII–OOH Complexes in O–O Bond Homolysis and H-Atom Abstraction Reactivities journal February 2013
Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z=11–18 journal May 1980
CONUSS and PHOENIX: Evaluation of nuclear resonant scattering data journal March 2000
Theoretical Analysis of Proton Relays in Electrochemical Proton-Coupled Electron Transfer journal June 2011
Characterization of a Paramagnetic Mononuclear Nonheme Iron-Superoxo Complex journal July 2014
Rate-Determining Attack on Substrate Precedes Rieske Cluster Oxidation during Cis-Dihydroxylation by Benzoate Dioxygenase journal July 2015
Structure of an aromatic-ring-hydroxylating dioxygenase – naphthalene 1,2-dioxygenase journal May 1998
Elucidation of the Fe(iv)=O intermediate in the catalytic cycle of the halogenase SyrB2 journal July 2013
A theoretical study of the cis-dihydroxylation mechanism in naphthalene 1,2-dioxygenase journal March 2004
Density functional calculation of pK a values and redox potentials in the bovine Rieske iron-sulfur protein journal February 2002
Kinetic studies of pigment synthesis by non-sulfur purple bacteria journal February 1957
Implicit Solvation Models:  Equilibria, Structure, Spectra, and Dynamics journal August 1999
NCBI BLAST: a better web interface journal May 2008
Normal-Mode Analysis of FeCl 4 - and Fe 2 S 2 Cl 4 2 - via Vibrational Mössbauer, Resonance Raman, and FT-IR Spectroscopies journal August 2005
Single Turnover Chemistry and Regulation of O2Activation by the Oxygenase Component of Naphthalene 1,2-Dioxygenase journal January 2001
Structural Insight into the Dioxygenation of Nitroarene Compounds: the Crystal Structure of Nitrobenzene Dioxygenase journal May 2005
Hydrogen Peroxide Dependent cis -Dihydroxylation of Benzoate by Fully Oxidized Benzoate 1,2-Dioxygenase journal June 2007
Regio- and stereodivergent antibiotic oxidative carbocyclizations catalysed by Rieske oxygenase-like enzymes journal April 2011
2-Oxoquinoline 8-Monooxygenase Oxygenase Component: Active Site Modulation by Rieske-[2Fe-2S] Center Oxidation/Reduction journal May 2005
Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields journal November 1994
Aromatic hydrocarbon dioxygenases in environmental biotechnology journal June 2000
Oxygen Activation by Rieske Non-Heme Iron Oxygenases, a Theoretical Insight journal August 2004
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 journal February 2008
O 2 Activation by Non-Heme Iron Enzymes journal November 2016
A Mononuclear Non-Heme High-Spin Iron(III)–Hydroperoxo Complex as an Active Oxidant in Sulfoxidation Reactions journal June 2013
The potential diagram for oxygen at pH 7 journal July 1988
Spectroscopic and Computational Evaluation of the Structure of the High-Spin Fe(IV)-Oxo Intermediates in Taurine: α-Ketoglutarate Dioxygenase from Escherichia coli and Its His99Ala Ligand Variant journal May 2007
Activated bleomycin. A transient complex of drug, iron, and oxygen that degrades DNA. journal November 1981

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Insights from $^{125}Te$ and $^{57}Fe$ nuclear resonance vibrational spectroscopy: a [4Fe–4Te] cluster from two points of view text January 2019
Spectroscopic Characterisation of the Naphthalene Dioxygenase from Rhodococcus sp. Strain NCIMB12038 journal July 2019

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