Decision-making processes in biological electron transfer: Conformational selection vs. electronic ground state selection by NMR

A. J. VILA; A.ABRIATA; M.E. ZABALLA; MORGADA, MARCOS

Grosetto

Workshop; 13th Chianti/INSTRUCT Workshop Magnetic Resonance for Cellular Structural Biology; 2014

CONFERENCIA INVITADA Cytochrome c oxidases are designed to exert a fine control of intra- and intermolecular electron transfer along defined metal cofactors which finally allow cellular respiration. CuA is a binuclear copper site which acts as the electron entry port in terminal cytochrome oxidases. The high efficiency of this metal site in long range intra- and intermolecular electron transfer has been attributed to its unusual coordination features, which ensure a rigid site and an electronic structure poised to meet the physiological requirements. The rigidity of this metal site is not compatible with the physiological requirement of interaction with selective metallochaperones. Hovewer, the non-metallated form exists in a conformational equilibrium between several substates that allow recognition with these partners. The electronic structure of the oxidized CuA center can be described by a fast equilibrium between two electronic ground states, which can be described by a σu* and a πu ground state wavefunctions, respectively. These levels are invisible to most spectroscopic techniques, except for the case of NMR which reveals that both levels are populated at room temperature, with the σu* being largely dominant. Thermal fluctuations may populate two alternative ground-state electronic wave functions optimized for electron entry and exit, respectively, through two different and nearly perpendicular pathways. These findings suggest a unique role for alternative or ?invisible? electronic ground states in directional electron transfer. Moreover, we show that this energy gap and, therefore, the equilibrium between ground states can be fine-tuned by minor perturbations, suggesting alternative ways through which protein?protein interactions and membrane potential may optimize and regulate electron?proton energy transduction.