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Title: NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native Fe II O 2 Reaction

The Rieske dioxygenases are a major subclass of mononuclear nonheme iron enzymes that play an important role in bioremediation. Recently, a high-spin Fe III-(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/O 2 reaction is evaluated. For the native Fe II/O 2 reaction, an Fe III-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 importantmore » insight into the relative reactivities of Fe III-superoxo and Fe III-hydroperoxo species in nonheme Fe biochemistry.« less
Authors:
 [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)
Publication Date:
Grant/Contract Number:
AC02-06CH11357
Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 140; Journal Issue: 16; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Research Org:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org:
National Institutes of Health (NIH); Japan Society for the Promotion of Science (JSPS). KAKENHI; USDOE Office of Science (SC)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
OSTI Identifier:
1465137

Sutherlin, Kyle D., Rivard, Brent S., Böttger, Lars H., Liu, Lei V., Rogers, Melanie S., Srnec, Martin, Park, Kiyoung, Yoda, Yoshitaka, Kitao, Shinji, Kobayashi, Yasuhiro, Saito, Makina, Seto, Makoto, Hu, Michael, Zhao, Jiyong, Lipscomb, John D., and Solomon, Edward I.. NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction. United States: N. p., Web. doi:10.1021/jacs.8b01822.
Sutherlin, Kyle D., Rivard, Brent S., Böttger, Lars H., Liu, Lei V., Rogers, Melanie S., Srnec, Martin, Park, Kiyoung, Yoda, Yoshitaka, Kitao, Shinji, Kobayashi, Yasuhiro, Saito, Makina, Seto, Makoto, Hu, Michael, Zhao, Jiyong, Lipscomb, John D., & Solomon, Edward I.. NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction. United States. doi:10.1021/jacs.8b01822.
Sutherlin, Kyle D., Rivard, Brent S., Böttger, Lars H., Liu, Lei V., Rogers, Melanie S., Srnec, Martin, Park, Kiyoung, Yoda, Yoshitaka, Kitao, Shinji, Kobayashi, Yasuhiro, Saito, Makina, Seto, Makoto, Hu, Michael, Zhao, Jiyong, Lipscomb, John D., and Solomon, Edward I.. 2018. "NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction". United States. doi:10.1021/jacs.8b01822. https://www.osti.gov/servlets/purl/1465137.
@article{osti_1465137,
title = {NRVS Studies of the Peroxide Shunt Intermediate in a Rieske Dioxygenase and Its Relation to the Native FeII O2 Reaction},
author = {Sutherlin, Kyle D. and Rivard, Brent S. and Böttger, Lars H. and Liu, Lei V. and Rogers, Melanie S. and Srnec, Martin and Park, Kiyoung and Yoda, Yoshitaka and Kitao, Shinji and Kobayashi, Yasuhiro and Saito, Makina and Seto, Makoto and Hu, Michael and Zhao, Jiyong and Lipscomb, John D. and Solomon, Edward I.},
abstractNote = {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.},
doi = {10.1021/jacs.8b01822},
journal = {Journal of the American Chemical Society},
number = 16,
volume = 140,
place = {United States},
year = {2018},
month = {4}
}