posted on 2021-09-27, 21:15authored byAriel
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
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)2 intermediate 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)2O2 core, in contrast to nonheme mononuclear Fe(IV)O enzyme
intermediates that H atoms abstract from weaker C–H bonds.