Alternative ground states enable pathway switching in biological electron transfer

ABRIATA, L.A.; ALVAREZ PAGGI, D.; LEDESMA, G.N.; BLACKBURN, N.J.; VILA, A.J.; MURGIDA, D.H.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

NATL ACAD SCIENCES

Lugar: Washington DC, USA; Año: 2012 vol. 109 p. 17348 - 17353

0027-8424

Electron transfer is the simplest chemical reaction and constitutes the basis of a large variety of biological processes such as photosynthesis and cellular respiration. Nature has evolved specific proteins and cofactors for these functions. The mechanisms optimizing biological electron transfer have been matter of intense debate, such as the role of the protein milieu between donor and acceptor sites. Here we propose a novel mechanism regulating long range electron transfer in proteins. Specifically, we report a spectroscopic, electrochemical and theoretical study on WT and single-mutant CuA redox centers from T. thermophilus, which shows that thermal fluctuations may populate two alternative ground state electronic wavefunctions optimized for electron entry and exit, respectively, through two different and nearly perpendicular pathways. These findings suggest a novel role for alternative or ?invisible? electronic ground states in directional electron transfer. Moreover, it is shown that the energy gap and, therefore, the equilibrium between ground states can be fine-tuned trough minor perturbations, suggesting new ways through which protein-protein interactions and membrane potential may optimize and tune electron-proton energy transduction.