Adapted evolution towards flagellar loss in Pseudomonas syringae

The flagellum is a complex molecular nanomachine crucial for cell motility. Its assembly requires coordinated expression of over 50 flagellar genes, regulated by the transcription activator FleQ. Phylogenomic analyses suggest that many non-flagellated bacterial species have evolved from flagellated ancestors by losing specific flagellar components, though the evolutionary mechanisms driving this process remain unclear. In this study, we examined the evolutionary dynamics of Pseudomonas syringae DC3000 under standard laboratory conditions using quantitative proteomics. We observed a notable reduction in flagellar gene expression following prolonged serial passages. Whole-genome sequencing revealed multiple adaptive mutations in fleQ, dksA, and glnE, all of which are associated with flagellar biosynthesis. Furthermore, our findings demonstrate that nonmotile ΔfleQ cells can hitchhike onto wild-type cells, potentially facilitated by increased production of the surfactant syringafactin. Our study suggests that the high metabolic costs associated with flagella biosynthesis, coupled with advantageous hitchhiking properties, contribute to the degenerative evolution of flagella.