Coenzyme F430 from Methanogenic Bacteria: Oxidation of F430 Pentamethyl Ester to the Ni(III) Form

Abstract

~ ~~F430M, the pentamethyl ester of coenzyme F430, can be oxidized reversibly by one electron. The oxidation potential has been determined, and the electrolytically prepared oxidation product was characterized by its UVjVIS and ESR spectrum. The strongly anisotropic and nearly axial ESR spectrum is consistent with a S = ' / > species with the unpaired-electron spin density predominantly in a dZ2-type orbital of the central nickel ion. The properties of Ni(III)F430M are discussed in the context of two hypothetical mechanisms for the catalytic role of coenzyme F430 in methyl coenzyme M reductase, which catalyses the last step of methane formation in methanogenic bacteria. Introduction. -Factor F430 [l], the hydrocorphinoid nickel complex 1, is the prosthetic group of methyl coenzyme M reductase [2] which catalyses the last step of CH, formation in methanogenic bacteria according to Scheme 1 [3].While recent biophysical evidence points to a change of the redox state of coenzyme F430 during the catalytic cycle [5], the specific mechanism by which the enzyme catalyses this process is still unknown. One conceivable way of activation of the C-S bond in methyl coenzyme M is the addition of a thiyl radical to the thioether, followed by transfer of a Me group from the sulfuranyl intermediate to the Ni center of coenzyme F430.

Substrate‐analogue‐induced changes in the nickel‐EPR spectrum of active methyl‐coenzyme‐M reductase from Methanobacterium thermoautotrophicum

“…As indicated above, the hypothesis has been put forward that MCR-red1 or MCR-red2 are derived from Ni(1) to which methyl-coenzyme M or H-S-HTP are axially ligated via sulfur (Berkessel, 1991;Jaun, 1990;Lin and Jaun, 1991). If this is correct, then MCR-BrPrSO, could be derived from Ni(1) to which BrPrS03 is axially ligated via the halogen.…”

“…A catalytic mechanism for MCR has recently been proposed which implies that during catalysis H-S-HTP or methylcoenzyme M are axially coordinated via sulfur to nickel of coenzyme F430 (Berkessel, 1991;Jaun, 1990;Lin and Jaun, 1991). The nickel-EPR signals, MCR-red1 and MCR-red2, could be derived from such intermediates.…”

Biochemistry of methanogenesis: a tribute to Marjory Stephenson:1998 Marjory Stephenson Prize Lecture

“…The latter finding suggests that the MCR,, forms of methyl-coenzyme M reductase could contain F,,, in the Ni(II1) oxidation state. Interestingly, the two MCR,, forms exhibit a UV/visible spectrum more closely related to that of Ni(I1) F,,, than to Ni(1) F,,, or Ni(II1) F,,, (Jaun, 1990(Jaun, , 1993 (Ermler et al, 1997b;see also Ferry, 199713;and Cammack, 1997). The primary structure of the enzyme had previously been resolved by Bokranz et al (1988).…”

A Nickel–Alkyl Bond in an Inactivated State of the Enzyme Catalyzing Methane Formation

“…According to mechanism "B", the Ni I center initially acts as a nucleophile attacking methyl-coenzyme M at the carbon atom of the CH 3 S group, thus generating a CH 3 -Ni iii F 430 intermediate and HS-CoM. [10][11][12][13] Whereas corresponding CH 3 -Ni ii F 430 derivatives have been generated in situ and characterized spectroscopically, [14] no experimental evidence for the existence of a CH 3 [16] The active enzyme MCR red1 reacts very rapidly and irreversibly with simple alkyl halides such as chloroform, which has been routinely used to quench the Ni I state and generate Ni II species. The two inhibitors 2-bromoethane sulfonate and 3-bromopropane sulfonate both react irreversibly with MCR red1 , but the resulting states are completely different: while 2-bromoethane sulfonate generates a Ni II ion and a carbon-centered protein radical similar to a glycine radical, 3-bromopropane sulfonate reacts to give the MCR BPS species which has a nickel-based, axial X-band continuous-wave EPR (CW-EPR) spectrum.…”