Nuclear Resonance Vibrational Spectroscopic Definition of the Fe(IV)2Intermediate Q in Methane Monooxygenase and Its Reactivity

Ariel Benjamin Jacobs, Rahul Banerjee, Dory Ellen Deweese, Augustin Braun, Jeffrey Thomas Babicz, Leland Bruce Gee, Kyle David Sutherlin, Lars Hendrik Böttger, Yoshitaka Yoda, Makina Saito, Shinji Kitao, Yasuhiro Kobayashi, Makoto Seto, Kenji Tamasaku, John D. Lipscomb, Kiyoung Park, Edward I. Solomon

Research output: Contribution to journalArticlepeer-review

Abstract

Methanotrophic bacteria utilize the nonheme diiron enzyme soluble methane monooxygenase (sMMO) to convert methane to methanol in the first step of their metabolic cycle under copper-limiting conditions. The structure of the sMMO Fe(IV)2intermediate Q responsible for activating the inert C-H bond of methane (BDE = 104 kcal/mol) remains controversial, with recent studies suggesting both “open” and “closed” core geometries for its active site. In this study, we employ nuclear resonance vibrational spectroscopy (NRVS) to probe the geometric and electronic structure of intermediate Q at cryogenic temperatures. These data demonstrate that Q decays rapidly during the NRVS experiment. Combining data from several years of measurements, we derive the NRVS vibrational features of intermediate Q as well as its cryoreduced decay product. A library of 90 open and closed core models of intermediate Q is generated using density functional theory to analyze the NRVS data of Q and its cryoreduced product as well as prior spectroscopic data on Q. Our analysis reveals that a subset of closed core models reproduce these newly acquired NRVS data as well as prior data. The reaction coordinate with methane is also evaluated using both closed and open core models of Q. These studies show that the potent reactivity of Q toward methane resides in the “spectator oxo” of its Fe(IV)2O2core, in contrast to nonheme mononuclear Fe(IV)═O enzyme intermediates that H atoms abstract from weaker C-H bonds.

Original languageEnglish
Pages (from-to)16007-16029
Number of pages23
JournalJournal of the American Chemical Society
Volume143
Issue number39
DOIs
Publication statusPublished - 2021 Oct 6

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

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