Wang, Z.; Uday, A. B.; Nelea, V.; Reinhardt, D. P.; Tieleman, D. P.; Bui, K. H.; Zeytuni, N.

Bacterial fimbriae are central to adhesion, colonization, and biofilm formation, yet how related fimbriae systems are structurally and mechanically specialized within the same pathogen remains poorly understood. Porphyromonas gingivalis, a keystone periodontal pathogen, expresses two primary type V fimbriae systems, the major Fim and minor Mfa fimbriae, which support distinct adhesive and biofilm-associated functions. Here, we determine high resolution cryo-electron microscopy structures of native FimA and Mfa1 shafts purified directly from P. gingivalis and show that a shared donor-strand exchange mechanism produces markedly different filament architectures. FimA forms a more extended shaft, whereas Mfa1 forms a compact filament in which the Mfa1 donor strand is deeply buried and shielded by an ordered N-terminal region. Comparison with monomeric pilin structures reveals distinct assembly-associated remodeling, including ordering of the Mfa1 N-terminal region during polymerization. Structure-guided deletion of this region reduces heat-resistant Mfa polymer accumulation. However, the filaments that can assemble still retain their overall architecture and mechanical behavior, indicating that his region contributes to polymer maturation or helical registry rather than directly determining mature shaft mechanics. Combining atomic force microscopy indentation and steered molecular dynamics, we further show that FimA and Mfa1 occupy complementary mechanical regimes: FimA is locally stiffer under transverse deformation, whereas Mfa1 undergoes a concentrated high-force transition during axial pulling. These findings establish P. gingivalis type V fimbriae as structurally and mechanically specialized adhesive polymers and provide a framework for understanding how bacterial pathogens tune surface filaments for persistence in mechanically complex polymicrobial biofilms.