Polyfunctional Nanofibril Appendages Mediate Attachment, Filamentation, and Filament Adaptability in Leptothrix cholodnii.

Abstract

Leptothrix is a species of Fe/Mn-oxidizing bacteria known to form long filaments composed of chains of cells that eventually produce a rigid tube surrounding the filament. Prior to the formation of this brittle microtube, Leptothrix cells secrete hair-like structures from the cell surface, called nanofibrils, which develop into a soft sheath that surrounds the filament. To clarify the role of nanofibrils in filament formation in L. cholodnii SP-6, we analyze the behavior of individual cells and multicellular filaments in high-aspect ratio microfluidic chambers using time-lapse and intermittent in situ fluorescent staining of nanofibrils, complemented with atmospheric scanning electron microscopy. We show that in SP-6 nanofibrils are important for attachment and their distribution on young filaments post-attachment is correlated to the directionality of filament elongation. Elongating filaments demonstrate a surprising ability to adapt to their physical environment by changing direction when they encounter obstacles: they bend or reverse direction depending on the angle of the collision. We show that the forces involved in the collision can be used to predict the behavior of filament. Finally, we show that as filaments grow in length, the older region becomes confined by the sheath, while the newly secreted nanofibrils at the leading edge of the filament form a loose, divergent, structure from which cells periodically escape.