Proton mediated spin state transition of cobalt heme analogs

• Published in: Nature communications 2019-05, Vol.10 (1), p.2303-2303, Article 2303
• Main Authors: Zhao, Jianping, Peng, Qian, Wang, Zijian, Xu, Wei, Xiao, Hongyan, Wu, Qi, Sun, Hao-Ling, Ma, Fang, Zhao, Jiyong, Sun, Cheng-Jun, Zhao, Jianzhang, Li, Jianfeng
• Format: Article
• Language: English
• Subjects: 639/638/263/406/910; 639/638/263/49/1141; Analogs; Biocatalysis; Catalysis; Cobalt; Cobalt - chemistry; Cobalt - metabolism; Crystallography, X-Ray; Cytochrome; Cytochrome c; Cytochrome P-450 Enzyme System - metabolism; Cytochrome P450; Cytochromes P450; Derivatives; Distributed processing; Electron Spin Resonance Spectroscopy; Heme; Heme - analogs & derivatives; Heme - chemistry; Heme - metabolism; Histidine; Histidine - chemistry; Humanities and Social Sciences; Hydrogen bonding; Hydrogen-Ion Concentration; Imidazole; Imidazoles - metabolism; INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Iron - chemistry; Ligands; Logic programming; Metals; multidisciplinary; Oxidation-Reduction; Protons; Science; Science (multidisciplinary); Substrates
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-10357-z

The spin state transition from low spin to high spin upon substrate addition is one of the key steps in cytochrome P450 catalysis. External perturbations such as pH and hydrogen bonding can also trigger the spin state transition of hemes through deprotonated histidine (e.g. Cytochrome c ). In this work, we report the isolated 2-methylimidazole Cobalt(II) [Co(TPP)(2-MeHIm)] and [Co(TTP)(2-MeHIm)], and the corresponding 2-methylimidazolate derivatives where the N−H proton of axial 2-MeHIm is removed. Interestingly, various spectroscopies including EPR and XAFS determine a high-spin state ( S  = 3/2) for the imidazolate derivatives, in contrast to the low-spin state ( S  = 1/2) of all known imidazole analogs. DFT assisted stereoelectronic investigations are applied to understand the metal-ligand interactions, which suggest that the dramatically displaced metal center allowing a promotion e g (d π ) →  b 1g ( d x 2 - y 2 ) is crucial for the occurrence of the spin state transition. Studying the electronic structures and spin transitions of synthetic heme analogs is crucial to advancing our understanding of heme enzyme mechanisms. Here the authors show that a Co(II) porphyrin complex undergoes an unexpected spin state transition upon deprotonation of its axial imidazole ligand.