CglB adhesins secreted at bacterial focal adhesions mediate gliding motility

Abstract

The predatory deltaproteobacterium Myxococcus xanthus uses a helically-trafficked motor at bacterial focal adhesion (bFA) sites to power gliding motility. Using TIRF and force microscopy, we herein identify the integrin αI-domain-like outer-membrane (OM) lipoprotein CglB as an essential substratum-coupling protein of the gliding motility complex. Similar to most known OM lipoproteins, CglB is anchored on the periplasmic side of the OM and thus a mechanism must exist to secrete it to the cell surface in order for it to interact with the underlying substratum. We reveal this process to be mediated by a predicted OM β-barrel structure of the gliding complex. This OM platform was found to regulate the conformational activation and secretion of CglB across the OM. These data suggest that the gliding complex promotes surface exposure of CglB at bFAs, thus explaining the manner by which forces exerted by inner-membrane motors are transduced across the cell envelope to the substratum; they also uncover a novel protein secretion mechanism, highlighting the ubiquitous connection between secretion and bacterial motility.

Bacterial glycocalyx integrity drives multicellular swarm biofilm dynamism

“…Two motility systems are required to carry out these complex physiological outcomes, with each being differentially active depending on the nature of the substratum. On hard surfaces, gliding (i.e., "adventurous" [A]) motility predominates, mediated by substratum coupling and directed transport of the trans-envelope Agl-Glt machinery at bacterial focal adhesion (bFA) sites (Faure et al, 2016;Islam & Mignot, 2015;Islam, My, et al, 2020). On soft substrata, cell groups move via type IV pilus (T4P)-dependent (i.e., "social" [S]) motility (Chang et al, 2016;Wu & Kaiser, 1995).…”

“…Cells within each layer are motile, densely packed, and aligned along their long axes, displaying the properties of an active nematic liquid-crystal state of matter (Copenhagen et al, 2020). This stratification on hard surfaces may require a functional gliding motility apparatus capable of coupling to an external contacting surface (e.g., the substratum and/ or adjacent cells) as layer formation is severely compromised when the substratum-coupling adhesin of the Agl-Glt apparatus (CglB) is absent (Islam, My, et al, 2020;Kaiser & Warrick, 2014). Prolonged incubation in such biofilms can lead to cells becoming connected via a network of outer-membrane vesicle (OMV) chains and OM tube (OMT) projections (Remis et al, 2013).…”

The differential expression of PilY1 proteins by the HsfBA phosphorelay allows twitching motility in the absence of exopolysaccharides

“…In order to find the EpsW interacting partners for the activation of the EPS biosynthetic pathway, we performed a genetic screen using a ΔepsW ΩcglB strain lacking EpsW and CglB [ 24 ], a long-known gliding motility protein [ 25 ]. As previously [ 26 ], we took advantage of the fact that this strain lacks both twitching (because of the absence of EPS, ΔepsW ) and gliding motility ( ΩcglB ) ( Fig 1A ).…”

A Multi-Rail Structure in the Cell Envelope for the Bacteroidetes Gliding Machinery

“…In M. xanthus, cytoplasmic and cytoplasmic membrane proteins migrate along a helical track in the cytoplasm, resulting in cell movement 44,47 . The cytoplasmic membrane motor proteins form a complex with periplasmic and outer membrane proteins that exert force on cell-surface adhesins that are attached to the substratum 46,[48][49][50] , which is similar to the F. johnsoniae motility model.…”