A nickel hydride complex in the active site of methyl-coenzyme m reductase: implications for the catalytic cycle.
Methanogenic archaea utilize a specific pathway in their metabolism, converting C1 substrates (i.e., CO2) or acetate to methane and thereby providing energy for the cell. Methyl-coenzyme M reductase (MCR) catalyzes the key step in the process, namely methyl-coenzyme M (CH3-S-CoM) plus coenzyme B (HS-CoB) to methane and CoM-S-S-CoB. The active site of MCR contains the nickel porphinoid F430. We report here on the coordinated ligands of the two paramagnetic MCR red2 states, induced when HS-CoM (a reversible competitive inhibitor) and the second substrate HS-CoB or its analogue CH3-S-CoB are added to the enzyme in the active MCR red1 state (Ni(I)F430). Continuous wave and pulse EPR spectroscopy are used to show that the MCR red2a state exhibits a very large proton hyperfine interaction with principal values A((1)H) = [-43,-42,-5] MHz and thus represents formally a Ni(III)F430 hydride complex formed by oxidative addition to Ni(I). In view of the known ability of nickel hydrides to activate methane, and the growing body of evidence for the involvement of MCR in "reverse" methanogenesis (anaerobic oxidation of methane), we believe that the nickel hydride complex reported here could play a key role in helping to understand both the mechanism of "reverse" and "forward" methanogenesis.
Harmer
Jeffrey
J
Centre for Advanced Electron Spin Resonance, Department of Chemistry, University of Oxford, South Parks Road, OX1 3QR, Oxford, United Kingdom. jeffrey.harmer@chem.ox.ac.uk
Finazzo
Cinzia
C
Piskorski
Rafal
R
Ebner
Sieglinde
S
Duin
Evert C
EC
Goenrich
Meike
M
Thauer
Rudolf K
RK
Reiher
Markus
M
Schweiger
Arthur
A
Hinderberger
Dariush
D
Jaun
Bernhard
B
D000085:Acetates / Q000737:chemistry; D001665:Binding Sites; D002245:Carbon Dioxide / Q000737:chemistry; D002384:Catalysis; D004578:Electron Spin Resonance Spectroscopy / Q000379:methods; D006859:Hydrogen / Q000737:chemistry*; D008665:Metalloporphyrins / Q000737:chemistry*; D008697:Methane / Q000138:chemical synthesis / Q000737:chemistry; D017013:Methanobacteriaceae / Q000201:enzymology; D008956:Models, Chemical; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000737:chemistry* / Q000302:isolation & purification
D000085:Acetates; D008665:Metalloporphyrins; D002245:Carbon Dioxide; C023540:factor F430; D006859:Hydrogen; D010088:Oxidoreductases; C021572:methyl coenzyme M reductase; D008697:Methane