Type IV pili (T4P) are dynamic surface appendages that promote virulence, biofilm formation, horizontal gene transfer, and motility in diverse bacterial species. Pilus dynamic activity is best characterized in T4P that use distinct ATPase motors for pilus extension and retraction. Many T4P systems, however, lack a dedicated retraction motor and the mechanism underlying this motor-independent retraction remains a mystery. Using the Vibrio cholerae competence pilus as a model system, we identify mutations in the major pilin gene that enhance motor-independent retraction. These mutants produced less stable pili, likely due to diminished pilin-pilin interactions within the filament. One mutation adds a bulky residue to α1C, a universally conserved feature of type IV pilins. We found that inserting a bulky residue into α1C of the retraction motor-dependent Acinetobacter baylyi competence T4P is sufficient to induce motor-independent retraction. Conversely, removing bulky residues from α1C of the retraction motor-independent V. cholerae toxin-co-regulated T4P stabilizes the filament and prevents retraction. Furthermore, alignment of pilins from the broader type IV filament (T4F) family indicated that retraction motor-independent T4P, Com pili, and type II secretion systems generally encode larger residues within α1C oriented toward the pilus core compared to retraction motor-dependent T4P. Together, our data demonstrate that motor-independent retraction relies on the inherent instability of the pilus filament that may be conserved in diverse T4Fs. This provides the first evidence for a long-standing, yet untested, model in which pili retract in the absence of a motor by spontaneous depolymerization.
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