A Bioinspired Nonheme Fe^III-(O₂^2-)-Cu^II Complex with an S_t = 1 Ground State

Area of Science:

• Bioinorganic Chemistry
• Biophysical Chemistry
• Enzyme Catalysis

Background:

• Cytochrome c oxidase (CcO) catalyzes the reduction of oxygen to water, a critical step in cellular respiration.
• The precise mechanism of O-O bond cleavage in CcO, particularly the role of key intermediates, remains incompletely understood.
• Previous synthetic models of CcO intermediates often exhibit catalytically unfavorable spin states.

Purpose of the Study:

• To investigate the role of spin state in the O-O bond cleavage mechanism of CcO.
• To synthesize and characterize nonheme iron-copper peroxido complexes as models for CcO intermediates.
• To explore the reactivity of these model complexes in O-O bond cleavage reactions.

Main Methods:

• Synthesis and spectroscopic characterization of two nonheme Fe(III)-(O2(2-))-Cu(II) complexes (1 and 2) with varying ligand substituents.
• Investigation of the ground spin state (S_t=1 or S_t=0) of the Fe-peroxido-Cu core in the synthesized complexes.
• Reactivity studies of the complexes with phenol to assess O-O bond cleavage efficiency.

Main Results:

• Complex 1, featuring an end-on peroxido core and a ferromagnetic (S_t=1) coupled Fe(III)-Cu(II) system, successfully cleaved the O-O bond in the presence of phenol via H-bonding.
• Complex 2, a μ-η2:η1 peroxido complex with an antiferromagnetic (S_t=0) ground state, was unreactive toward phenol.
• The results highlight the critical role of the S_t=1 spin state for efficient O-O bond cleavage.

Conclusions:

• The study provides direct evidence that a high-spin (S_t=1) Fe(III)-(O2(2-))-Cu(II) intermediate is essential for facilitating O-O bond cleavage.
• These findings extend the understanding of spin topology's importance in O-O bond cleavage from heme-based CcO to nonheme systems.
• The developed nonheme models offer valuable insights into the fundamental steps of oxygen reduction in biological and chemical systems.