Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria

Abstract

Bacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium Myxococcus xanthus, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number of genes identified as important for gliding, no specific machinery has been identified so far, hampering in-depth investigations. Based on the premise that components of the gliding machinery must have co-evolved and encode both envelope-spanning proteins and a molecular motor, we re-annotated known gliding motility genes and examined their taxonomic distribution, genomic localization, and phylogeny. We successfully delineated three functionally related genetic clusters, which we proved experimentally carry genes encoding the basal gliding machinery in M. xanthus, using genetic and localization techniques. For the first time, this study identifies structural gliding motility genes in the Myxobacteria and opens new perspectives to study the motility mechanism. Furthermore, phylogenomics provide insight into how this machinery emerged from an ancestral conserved core of genes of unknown function that evolved to gliding by the recruitment of functional modules in Myxococcales. Surprisingly, this motility machinery appears to be highly related to a sporulation system, underscoring unsuspected common mechanisms in these apparently distinct morphogenic phenomena.

Flagella stator homologs function as motors for myxobacterial gliding motility by moving in helical trajectories

“…Our model unifies gliding and swimming with conserved power-generating modules. S4) or when they moved on agar surfaces (Movie S5) (6), consistent with the report that AglR and AgmU belong to the same gliding machinery (12). Although the SIM images show the AglR macrostructure to be clearly helical, we could not exclude possible artifacts introduced by the cell fixation procedure and the algorithms of image processing.…”

“…Besides the genes encoding the motor complex (aglR, aglQ, and aglS), ∼40 other genes are also required for gliding motility (19). For example, the AglRQS complex was shown to directly interact with another complex of gliding proteins including AgmU and AglZ (12). The ΔagmU and ΔaglZ mutants were unable to move by gliding, despite the existence of functional AglQRS motor complexes (5).…”

Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes

“…The scarcity of orthologs to F. johnsoniae motility proteins among these diverse gliding bacteria suggests that they employ gliding machineries that are not closely related to the F. johnsoniae gliding apparatus. Components of the M. xanthus and M. mobile gliding motility machineries have been identified (50)(51)(52)(53)(54)(55), and most of these do not have orthologs in F. johnsoniae (5), further supporting this suggestion.…”

Synthesis and Assembly of a Novel Glycan Layer in Myxococcus xanthus Spores

“…Some of the Exo proteins share homology with polysaccharide secretion machinery (5,11), and the Nfs proteins share homology with proteins (Glt) that may power the M. xanthus gliding motility machinery (12). It has been demonstrated that both the Glt and Nfs machinery appear to be involved in protonmotive force-dependent possessive transport processes, but the consequence and details of this mechanism remain undiscovered (13).…”