Theoretical Study of Dioxygen Binding Process in Iron(III) Catechol Dioxygenase: “Oxygen Activation” vs “Substrate Activation”

• Published in: The journal of physical chemistry. B Vol. 113; no. 14; pp. 4826 - 4836
• Main Authors: Nakatani, Naoki, Nakao, Yoshihide, Sato, Hirofumi, Sakaki, Shigeyoshi
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 09-04-2009
• Subjects: B: Biophysical Chemistry; Binding Sites; Catechol 1,2-Dioxygenase - chemistry; Catechol 1,2-Dioxygenase - metabolism; Computer Simulation; Iron - chemistry; Iron - metabolism; Models, Chemical; Molecular Structure; Oxygen - chemistry; Oxygen - metabolism
• ISSN: 1520-6106; 1520-5207
• DOI: 10.1021/jp806507k

Dioxygen binding process of nonheme iron(III) center in intradiol catechol dioxygenase was investigated with CASSCF/CASPT2 method to incorporate multiconfigurational character participating in Fe−O2 interaction. In this process, two alternative mechanisms were proposed: one is called “oxygen activation” and the other is called “substrate activation”. Our CASSCF/CASPT2-calculated results support the oxygen activation. Potential energy curves and electronic structure evaluated with SA(state-averaged)-CASSCF/CASPT2 method indicate that the charge transfer directly occurs from the catecholate moiety to the dioxygen moiety in the O2 binding process, to produce η1-end-on type iron(III)−superoxo complex. This is the key step of the dioxygen activation. Interestingly, the iron center always keeps high spin d5 character during the O2 binding process, indicating the iron(III) center does not receive charge transfer from the catecholate moiety. However, this does not mean that the iron(III) center is not necessary to the dioxygen activation. The important role which the iron(III) center plays in catechol dioxygenase is to adjust the energy level of O2 to induce the charge transfer from the catecholate moiety to the dioxygen moiety. Besides the η1-end-on iron(III)−superoxo complex, η2-side-on type iron(III)−superoxo complex is also optimized. This species is more stable than the η1-end-on type iron(III)−superoxo complex, suggesting that this is considered as a stable isomer in the early stage of the catalytic cycle.