Inter-subunit rotation and elastic power transmission in F0F1-ATPase

ATP synthase (F-ATPase) produces ATP at the expense of ion-motive force or vice versa. It is composed from two motor/generators, the ATPase (F-1) and the ion translocator (F-0), which both are rotary steppers. They are mechan ically coupled by 360 degrees rotary motion of subunits against each other. The rotor, subunits gamma epsilonc(10-14), moves against the stator, (alph a beta)(3)delta ab(2.) The enzyme copes with symmetry mismatch (C-3 versus C10-14) between its two motors, and it operates robustly in chimeric constr ucts or with drastically modified subunits. We scrutinized whether an elast ic power transmission accounts for these properties. We used the curvature of fluorescent actin filaments, attached to the rotating c ring, as a sprin g balance (flexural rigidity of 8.10(-26) N m(2)) to gauge the angular prof ile of the output torque at F0 during ATP hydrolysis by F-1. The large aver age output torque (56 pN nm) proved the absence of any slip. Angular variat ions of the torque were small, so that the output free energy of the loaded enzyme decayed almost linearly over the angular reaction coordinate. Consi dering the three-fold stepping and high activation barrier ( > 40 kJ/mol) o f the driving motor (Fl) itself, the rather constant output torque seen by F0 implied a soft elastic power transmission between F-1 and F-0. It is con sidered as essential, not only for the robust operation of this ubiquitous enzyme under symmetry mismatch, but also for a high turnover rate under loa d of the two counteracting and stepping motors/generators. (C) 2001 Federat ion of European Biochemical Societies. Published by Elsevier Science B.V. A ll rights reserved.