title: Models of the ox1 state of methylcoenzyme M reductase: where are the electrons?
abstract: The nature of the nickel center in the ox1 form of methylcoenzyme M reductase (MCR(ox1)), the enzyme that catalyzes the last step of biological methanogenesis, has long been controversial. A recent pulse electron paramagnetic resonance (EPR) study suggested a Ni(III)-thiolate, or equivalently a high-spin Ni(II) thiyl radical, description. The MCR(ox1) hyperfine parameters are best interpreted in terms of a Ni d(x(2)-y(2) ) SOMO, although a pure d(x(2)-y(2) ) SOMO does not explain the fact that about 7 % of the spin-density resides on the sulfur. The key goals of this DFT (PW91) study were to judge whether the Ni(III)-thiolate description is chemically sensible and, if so, to provide a detailed molecular orbital (MO) description of MCR(ox1). An Ni(III)-thiolate description was indeed found to be reasonable and was obtained as the ground state for symmetrized (C(s)) oxaporphyrin-, pyriporphyrin-, and isoporphyrin-based model complexes, as well as for a more realistic, biomimetic model. The model calculations yielded a number of insights, key among which are the following: 1) Although the SOMO topology may be viewed as d(x(2)-y(2) )-like, this MO also has a substantial amount of metal d(z(2) ) character, allowing it to overlap with a thiolate sigma lone pair, which would otherwise be orthogonal. 2) In one case (isoporphyrin), we were able to exploit the symmetry of the molecule to independently optimize the (d(x(2)-y(2) ))(1) and (d(z(2) ))(1) Ni(III) states, which turned out to be very close in energy. 3) The near-degeneracy of these two states provides an elegant explanation for the tendency of these two orbitals to hybridize. Admixture of substantial d(z(2) ) character into the d(x(2)-y(2) )-type SOMO of our most realistic model of MCR(ox1) results in a small but distinct spin population of about 0.04 on the sulfur, apparently nicely confirming the conclusions derived from the pulse EPR study. Other pure functionals also confirm this picture, although the hybrid functional B3LYP yields a spin-density profile that is clearly at odds with the EPR study.
authors.affiliation: Department of Chemistry and Center for Theoretical and Experimental Chemistry, University of Tromsø, 9037 Tromsø, Norway.
authors.forename: Emmanuel
authors.initials: E
authors.lastname: Gonzalez
authors.forename: Abhik
authors.initials: A
authors.lastname: Ghosh
mesh_terms: D004583:Electrons; D008954:Models, Biological; D008968:Molecular Conformation; D009532:Nickel / Q000737:chemistry; D010088:Oxidoreductases / Q000737:chemistry*; D011789:Quantum Theory
chemical_list: D009532:Nickel; D010088:Oxidoreductases; C021572:methyl coenzyme M reductase