Kyle D Sutherlin1, Brent S Rivard2, Lars H Böttger1, Lei V Liu1, Melanie S Rogers2, Martin Srnec1,3, Kiyoung Park1,4, Yoshitaka Yoda5, Shinji Kitao6, Yasuhiro Kobayashi6, Makina Saito6, Makoto Seto6, Michael Hu7, Jiyong Zhao7, John D Lipscomb2, Edward I Solomon1,8. 1. Department of Chemistry , Stanford University , Stanford , California 94305 , United States. 2. Department of Biochemistry, Molecular Biology, & Biophysics , University of Minnesota , Minneapolis , Minnesota 55455 , United States. 3. J. Heyrovský Institute of Physical Chemistry , The Czech Academy of Sciences , Dolejškova 2155/3 , 182 23 Prague 8 , Czech Republic. 4. Department of Chemistry , KAIST , Daejeon 34141 , Republic of Korea. 5. Japan Synchrotron Radiation Research Institute , Hyogo 679-5198 , Japan. 6. Research Reactor Institute , Kyoto University , Osaka 590-0494 , Japan. 7. Advanced Photon Source , Argonne National Laboratory , Lemont , Illinois 60439 , United States. 8. SLAC National Accelerator Laboratory , Menlo Park , California 94025 , United States.
Abstract
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. 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 FeII/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. These results offer important insight into the relative reactivities of FeIII-superoxo and FeIII-hydroperoxo species in nonheme Fe biochemistry.
The Rieske dipan class="Chemical">oxygenases 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. 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 FeII/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. These results offer important insight into the relative reactivities of FeIII-superoxo and FeIII-hydroperoxo species in nonheme Fe biochemistry.
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