Segmented filamentous bacteria undergo a structural transition at their adhesive tip during unicellular to filament development

Segmented filamentous bacteria (SFB) are intestinal commensals that promote immune system development and pathogen protection through intimate attachment to the ileal epithelium. Attachment occurs via the tip of unicellular teardrop-shaped SFB, called intracellular offsprings (IOs), before outgrowth into filaments. To characterize this critical stage of the SFB life cycle, we imaged SFB using cryo-electron microscopy and tomography. IOs were surrounded by a repetitive surface (S)-layer that became replaced by disordered hair-like structures specifically at the IO tip. During outgrowth into filaments, the S-layer was exchanged for a morphologically distinct repetitive hair-like layer. The bacterial structures and morphological transition were conserved across SFB from mouse and rat origin, while growth of mouse-SFB under non-attachment conditions in a heterologous host affected the SFB tip length and relative proportion of the tip stages. Moreover, a major Th17 and B cell antigen, while being a ubiquitous cell wall-associated protein, was immunologically accessible only at the filament tip, underscoring the unique properties of the tip structure. This study identifies an IO-specific S-layer and reveals a conserved developmental transition of the SFB tip surface including the transient appearance of structures consistent in location and timing with being involved in host cell attachment.