The mysterious nature of bacterial surface (gliding) motility: A focal adhesion-based mechanism in Myxococcus xanthus

• Bacterial gliding motility is mediated by a novel trans-envelope Glt complex.
• Glt is transported along the cell, powered by the H+-driven Agl motor.
• Glt–substratum engagement via slime stalls Glt, transports track (and cell) forward.
• Glt and sporulation machineries carry out related cell-envelope processes.
• Models for macromolecular machine evolution can be proposed.

Motility of bacterial cells promotes a range of important physiological phenomena such as nutrient detection, harm avoidance, biofilm formation, and pathogenesis. While much research has been devoted to the mechanism of bacterial swimming in liquid via rotation of flagellar filaments, the mechanisms of bacterial translocation across solid surfaces are poorly understood, particularly when cells lack external appendages such as rotary flagella and/or retractile type IV pili. Under such limitations, diverse bacteria at the single-cell level are still able to “glide” across solid surfaces, exhibiting smooth translocation of the cell along its long axis. Though multiple gliding mechanisms have evolved in different bacterial classes, most remain poorly characterized. One exception is the gliding motility mechanism used by the Gram-negative social predatory bacterium Myxococcus xanthus. The available body of research suggests that M. xanthus gliding motility is mediated by trafficked multi-protein (Glt) cell envelope complexes, powered by proton-driven flagellar stator homologues (Agl). Through coupling to the substratum via polysaccharide slime, Agl–Glt assemblies can become fixed relative to the substratum, forming a focal adhesion site. Continued directional transport of slime-associated substratum-fixed Agl–Glt complexes would result in smooth forward movement of the cell. In this review, we have provided a comprehensive synthesis of the latest mechanistic and structural data for focal adhesion-mediated gliding motility in M. xanthus, with emphasis on the role of each Agl and Glt protein. Finally, we have also highlighted the possible connection between the motility complex and a new type of spore coat assembly system, suggesting that gliding and cell envelope synthetic complexes are evolutionarily linked.

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