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Title: Nuclear Resonance Vibrational Spectroscopy Definition of O2 Intermediates in an Extradiol Dioxygenase: Correlation to Crystallography and Reactivity

Journal Article · · Journal of the American Chemical Society
DOI:https://doi.org/10.1021/jacs.8b06517· OSTI ID:1490963
 [1];  [2];  [3];  [3];  [1];  [1];  [1];  [1];  [1];  [1];  [4];  [5];  [5];  [5];  [5]; ORCiD logo [6];  [6];  [6]; ORCiD logo [3]; ORCiD logo [7]
  1. Stanford Univ., Stanford, CA (United States)
  2. Nagoya Institute of Technology, Nagoya (Japan)
  3. Univ. of Minnesota, Minneapolis, MN (United States)
  4. Japan Synchrotron Radiation Research Institute, Hyogo (Japan)
  5. Kyoto Univ., Osaka (Japan)
  6. Argonne National Lab. (ANL), Lemont, IL (United States)
  7. Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
+ Show Author Affiliations

The extradiol dioxygenases are a large subclass of mononuclear nonheme Fe enzymes that catalyze the oxidative cleavage of catechols distal to their OH groups. These enzymes are important in bioremediation, and there has been significant interest in understanding how they activate O2. The extradiol dioxygenase homoprotocatechuate 2,3-dioxygenase (HPCD) provides an opportunity to study this process, as two O2 intermediates have been trapped and crystallographically defined using the slow substrate 4-nitrocatechol (4NC): a side-on Fe–O2–4NC species and a Fe–O2–4NC peroxy bridged species. Also with 4NC, two solution intermediates have been trapped in the H200N variant, where H200 provides a second-sphere hydrogen bond in the wild-type enzyme. While the electronic structure of these solution intermediates has been defined previously as FeIII-superoxo-catecholate and FeIII-peroxy-semiquinone, their geometric structures are unknown. Nuclear resonance vibrational spectroscopy (NRVS) is an important tool for structural definition of nonheme Fe–O2 intermediates, as all normal modes with Fe displacement have intensity in the NRVS spectrum. In this study, NRVS is used to define the geometric structure of the H200N-4NC solution intermediates in HPCD as an end-on FeIIIsuperoxo-catecholate and an end-on FeIII-hydroperoxo-semiquinone. Parallel calculations are performed to define the electronic structures and protonation states of the crystallographically defined wild-type HPCD-4NC intermediates, where the side-on intermediate is found to be a FeIII-hydroperoxo-semiquinone. The assignment of this crystallographic intermediate is validated by correlation to the NRVS data through computational removal of H200. Even though the side-on hydroperoxo semiquinone intermediate is computationally found to be nonreactive in peroxide bridge formation, it is isoenergetic with a superoxo catecholate species that is competent in performing this reaction. This study gives insight into the relative reactivities of FeIII-superoxo and FeIII-hydroperoxo intermediates in nonheme Fe enzymes and into the role H200 plays in facilitating extradiol catalysis.

Research Organization:
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH); Japan Society for the Promotion of Science (JSPS)
Grant/Contract Number:
AC02-76SF00515; 24221005; R2304; R2606; GM 118030; GM 40392; AC02-06CH11357
OSTI ID:
1490963
Alternate ID(s):
OSTI ID: 1502992
Journal Information:
Journal of the American Chemical Society, Vol. 140, Issue 48; ISSN 0002-7863
Publisher:
American Chemical Society (ACS)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 11 works
Citation information provided by
Web of Science

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[FeII(L•)2][TCNQF4•−]2: A Redox-Active Double Radical Salt journal January 2019
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