F-1-ATPase uses ATP hydrolysis to drive rotation of the gamma subunit. The gamma C-terminal helix constitutes the rotor tip that is seated in an apical bearing formed by alpha(3)beta(3). It remains uncertain to what extent the gamma conformation during rotation differs from that seen in rigid crystal structures. Existing models assume that the entire gamma subunit participates in every rotation. Here we interrogated E. coli F-1-ATPase by hydrogen-deuterium exchange (HDX) mass spectrometry. Rotation of gamma caused greatly enhanced deuteration in the gamma C-terminal helix. The HDX kinetics implied that most F-1 complexes operate with an intact rotor at any given time, but that the rotor tip is prone to occasional unfolding. A molecular dynamics (MD) strategy was developed to model the off-axis forces acting on gamma. MD runs showed stalling of the rotor tip and unfolding of the gamma C-terminal helix. MD predicted H-bond opening events coincided with experimental HDX patterns. Our data suggest that in vitro operation of F(1)ATPase is associated with significant rotational resistance in the apical bearing. These conditions cause the gamma C-terminal helix to get "stuck" (and unfold) sporadically while the remainder of gamma continues to rotate. This scenario contrasts the traditional "greasy bearing" model that envisions smooth rotation of the gamma C-terminal helix. The fragility of the apical rotor tip in F-1-ATPase is attributed to the absence of a c(10) ring that stabilizes the rotation axis in intact F0F1. Overall, the MD/HDX strategy introduced here appears well suited for interrogating the inner workings of molecular motors.