Dustin Kass, Sagie Katz, Hivda Özgen, Stefan Mebs, Michael Haumann, Ricardo García-Serres, Holger Dau, Peter Hildebrandt, Thomas Lohmiller, Kallol Ray
{"title":"A Bioinspired Nonheme Fe<sup>III</sup>-(O<sub>2</sub><sup>2-</sup>)-Cu<sup>II</sup> Complex with an <i>S</i><sub>t</sub> = 1 Ground State.","authors":"Dustin Kass, Sagie Katz, Hivda Özgen, Stefan Mebs, Michael Haumann, Ricardo García-Serres, Holger Dau, Peter Hildebrandt, Thomas Lohmiller, Kallol Ray","doi":"10.1021/jacs.4c04492","DOIUrl":null,"url":null,"abstract":"<p><p>Cytochrome <i>c</i> oxidase (CcO) is a heme copper oxidase (HCO) that catalyzes the natural reduction of oxygen to water. A profound understanding of some of the elementary steps leading to the intricate 4e<sup>-</sup>/4H<sup>+</sup> reduction of O<sub>2</sub> is presently lacking. A total spin <i>S</i><sub>t</sub> = 1 Fe<sup>III</sup>-(O<sub>2</sub><sup>2-</sup>)-Cu<sup>II</sup> (<b>I<sub>P</sub></b>) intermediate is proposed to reduce the overpotentials associated with the reductive O-O bond rupture by allowing electron transfer from a tyrosine moiety without the necessity of any spin-surface crossing. Direct evidence of the involvement of <b>I</b><sub><b>P</b></sub> in the CcO catalytic cycle is, however, missing. A number of heme copper peroxido complexes have been prepared as synthetic models of <b>I</b><sub><b>P</b></sub>, but all of them possess the catalytically nonrelevant <i>S</i><sub>t</sub> = 0 ground state resulting from antiferromagnetic coupling between the <i>S</i> = 1/2 Fe<sup>III</sup> and Cu<sup>II</sup> centers. In a complete nonheme approach, we now report the spectroscopic characterization and reactivity of the Fe<sup>III</sup>-(O<sub>2</sub><sup>2-</sup>)-Cu<sup>II</sup> intermediates <b>1</b> and <b>2</b>, which differ only by a single -CH<sub>3</sub> versus -H substituent on the central amine of the tridentate ligands binding to copper. Complex <b>1</b> with an end-on peroxido core and ferromagnetically (<i>S</i><sub>t</sub> = 1) coupled Fe<sup>III</sup> and Cu<sup>II</sup> centers performs H-bonding-mediated O-O bond cleavage in the presence of phenol to generate oxoiron(IV) and exchange-coupled copper(II) and PhO<sup>•</sup> moieties. In contrast, the μ-η<sup>2</sup>:η<sup>1</sup> peroxido complex <b>2</b>, with a <i>S</i><sub>t</sub> = 0 ground state, is unreactive toward phenol. Thus, the implications for spin topology contributions to O-O bond cleavage, as proposed for the heme Fe<sup>III</sup>-(O<sub>2</sub><sup>2-</sup>)-Cu<sup>II</sup> intermediate in CcO, can be extended to nonheme chemistry.</p>","PeriodicalId":49,"journal":{"name":"Journal of the American Chemical Society","volume":null,"pages":null},"PeriodicalIF":14.4000,"publicationDate":"2024-07-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of the American Chemical Society","FirstCategoryId":"92","ListUrlMain":"https://doi.org/10.1021/jacs.4c04492","RegionNum":1,"RegionCategory":"化学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CHEMISTRY, MULTIDISCIPLINARY","Score":null,"Total":0}
引用次数: 0
Abstract
Cytochrome c oxidase (CcO) is a heme copper oxidase (HCO) that catalyzes the natural reduction of oxygen to water. A profound understanding of some of the elementary steps leading to the intricate 4e-/4H+ reduction of O2 is presently lacking. A total spin St = 1 FeIII-(O22-)-CuII (IP) intermediate is proposed to reduce the overpotentials associated with the reductive O-O bond rupture by allowing electron transfer from a tyrosine moiety without the necessity of any spin-surface crossing. Direct evidence of the involvement of IP in the CcO catalytic cycle is, however, missing. A number of heme copper peroxido complexes have been prepared as synthetic models of IP, but all of them possess the catalytically nonrelevant St = 0 ground state resulting from antiferromagnetic coupling between the S = 1/2 FeIII and CuII centers. In a complete nonheme approach, we now report the spectroscopic characterization and reactivity of the FeIII-(O22-)-CuII intermediates 1 and 2, which differ only by a single -CH3 versus -H substituent on the central amine of the tridentate ligands binding to copper. Complex 1 with an end-on peroxido core and ferromagnetically (St = 1) coupled FeIII and CuII centers performs H-bonding-mediated O-O bond cleavage in the presence of phenol to generate oxoiron(IV) and exchange-coupled copper(II) and PhO• moieties. In contrast, the μ-η2:η1 peroxido complex 2, with a St = 0 ground state, is unreactive toward phenol. Thus, the implications for spin topology contributions to O-O bond cleavage, as proposed for the heme FeIII-(O22-)-CuII intermediate in CcO, can be extended to nonheme chemistry.
期刊介绍:
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