Novelty in biology can arise from opportunistic repurposing of nascent characteristics of
existing features. Understanding how this process happens at the molecular scale, however,
suffers from a lack of case studies. The evolutionary emergence of rotary motors is a
particularly clear example of evolution of a new function. The simplest of rotary motors is the
archaellum, a molecular motor that spins a helical propeller for archaeal motility analogous to
the bacterial flagellum. Curiously, emergence of archaellar rotation may have pivoted on the
simple duplication and repurposing of a pre-existing component to produce a stator complex
that anchors to the cell superstructure to enable productive rotation of the rotor component.
This putative stator complex is composed of ArlF and ArlG, gene duplications of the filament
component ArlB, providing an opportunity to study how gene duplication and
neofunctionalization contributed to the radical innovation of rotary function. Toward
understanding how this happened, we used electron cryomicroscopy to determine the
structure of isolated ArlG filaments, the major component of the stator complex. Using a
hybrid modeling approach incorporating structure prediction and validation, we show that
ArlG filaments are open helices distinct to the closed helical filaments of ArlB. Curiously,
further analysis reveals that ArlG retains a subset of the inter-protomer interactions of
homologous ArlB, resulting in a superficially different assembly that nevertheless reflects the
common ancestry of the two structures. This relatively simple mechanism to change
quaternary structure was likely associated with the evolutionary neofunctionalization of the
archaellar stator complex, and we speculate that the relative deformable elasticity of an open
helix may facilitate elastic energy storage during the transmission of the discrete bursts of
energy released by ATP hydrolysis to continuous archaellar rotation, allowing the inherent
properties of a duplicated ArlB to be co-opted to fulfil a new role. Furthermore, agreement of
diverse experimental evidence in our work supports recent claims to the power of new
structure prediction techniques.