A molecular rack and pinion actuates a cell-surface adhesin and enables bacterial gliding motility

Abstract

The mechanism for bacterial gliding is not understood. The gliding bacterium Flavobacterium johnsoniae is known to have an adhesin, SprB, that moves along the cell surface on a spiral track. When cells are sheared by passage of a suspension through thin tubing, they stop gliding but can be tethered by addition of an anti-SprB antibody. Tethered cells spin about 3 Hz. We labeled the Type 9 secretion system (T9SS) with a yellow-fluorescent-protein (YFP) fusion of GldL. When labeled cells were tethered, a yellow fluorescent spot was found near the rotation axis, which shows that the motor that drives the rotation localizes with the T9SS. The spiral track was labeled by following the motion of Cy3-labeled SprB. The distance between the rotation axis and the track was determined by a measurement involving both labels, YFP and Cy3, yielding 90 nm. If a rotary motor spins a pinion of radius 90 nm 3 Hz, a spot on its periphery will move 1.5 µm/s, the speed at which cells glide. We suggest that the pinion drives a flexible tread that carries SprB along a track fixed to the cell surface. Cells glide when such an adhesin adheres to the solid substratum.

Structure and mechanism of the proton-driven motor that powers type 9 secretion and gliding motility

“…The third type of ion-driven motor is found in certain Bacteroidetes where it is used to power gliding motility across solid surfaces 6 using the proton motive force (PMF) across the inner membrane (IM) as the energy source 7 , 8 , 9 . The gliding motility motor generates a rotary motion at the cell surface 9 that results in a helical flow of surface adhesin proteins 7 , 10 , 11 , possibly by driving a mobile track to which the adhesins are attached 12 .…”

Bacterial swarm-mediated phage transportation disrupts a biofilm inherently protected from phage penetration

“…T9SS containing Bacteroidetes are abundant in the human oral and gut microbiota. A large cell-surface protein SprB acts as a focal adhesin and it facilitates T9SS driven bacterial gliding motility 35 . Besides aiding in motility, SprB also binds to non-motile bacterial species.…”

“…Motile members of the phylum Bacteroidetes exhibit gliding motility with the help of the Type 9 Secretion System 32,33 . Bacteroidetes gliding motility is driven by a rotary motor 34 that couples with a cell-surface track 35 . C. gingivalis moves over an external surface with the help of a cell surface adhesin SprB 35 .…”

The Type IX Secretion System: Advances in Structure, Function and Organisation

“…Domains D1 to D4 of GldM shared the same straight topology, whereas in PorM there was ~ 45° bend between domain D2 and D3 [ 37 ]. Based on the observation of SprB circular motion in sheared cells [ 39 ] and the localisation of YFP-labelled GldL close to the centre of that rotation, Shrivastava et al [ 40 ] recently predicted GldLM to be the motor of the T9SS and showed that it was driven by the proton motif force (PMF). This was confirmed by Hennell-James et al [ 41 ] (non-peer-reviewed), by solving the native structure of the GldLM /PorLM complexes using cryo-EM.…”