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Structure of the key species in the enzymatic oxidation of methane to methanol

2015; Nature Portfolio; Volume: 518; Issue: 7539 Linguagem: Inglês

10.1038/nature14160

1476-4687

R. Banerjee, Yegor Proshlyakov, John D. Lipscomb, Denis A. Proshlyakov,

Porphyrin Metabolism and Disorders

Time-resolved resonance Raman vibrational spectroscopy was used to study the mechanism of soluble methane monooxygenase and obtain structural information on the key reaction cycle intermediate, compound Q, which contains a unique dinuclear FeIV cluster that breaks the strong C-H bond of methane and inserts an oxygen atom (from O2) to form methanol. Using time-resolved resonance Raman vibrational spectroscopy, Rahul Banerjee et al. have determined the structure of 'compound Q', a key transient intermediate from the soluble methane monooxygenase (sMMO) system found in methanotrophic bacteria. Q is the strongest known biological oxidant and catalyses cleavage of the ultimately stable C–H bond of methane with insertion of oxygen to form the liquid fuel methanol. With a better understanding of the structure and mechanism of action of Q it might be possible to synthesize small molecule enzyme mimetics that could convert naturally occurring methane to methanol, thereby converting a damaging greenhouse gas into a potentially important source of liquid fuel and chemicals. Methane monooxygenase (MMO) catalyses the O2-dependent conversion of methane to methanol in methanotrophic bacteria, thereby preventing the atmospheric egress of approximately one billion tons of this potent greenhouse gas annually. The key reaction cycle intermediate of the soluble form of MMO (sMMO) is termed compound Q (Q). Q contains a unique dinuclear FeIV cluster that reacts with methane to break an exceptionally strong 105 kcal mol−1 C-H bond and insert one oxygen atom1,2. No other biological oxidant, except that found in the particulate form of MMO, is capable of such catalysis. The structure of Q remains controversial despite numerous spectroscopic, computational and synthetic model studies2,3,4,5,6,7. A definitive structural assignment can be made from resonance Raman vibrational spectroscopy but, despite efforts over the past two decades, no vibrational spectrum of Q has yet been obtained. Here we report the core structures of Q and the following product complex, compound T, using time-resolved resonance Raman spectroscopy (TR3). TR3 permits fingerprinting of intermediates by their unique vibrational signatures through extended signal averaging for short-lived species. We report unambiguous evidence that Q possesses a bis-μ-oxo diamond core structure and show that both bridging oxygens originate from O2. This observation strongly supports a homolytic mechanism for O-O bond cleavage. We also show that T retains a single oxygen atom from O2 as a bridging ligand, while the other oxygen atom is incorporated into the product8. Capture of the extreme oxidizing potential of Q is of great contemporary interest for bioremediation and the development of synthetic approaches to methane-based alternative fuels and chemical industry feedstocks. Insight into the formation and reactivity of Q from the structure reported here is an important step towards harnessing this potential.