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Unlabelled: Bacterial locomotion driven by flagella is given directionality by the chemotaxis signal transduction network. In the classic plate assays of migration in porous motility agar, efficient motility is compromised in chemotaxis mutants of diverse bacteria. Nonchemotactic mutants become trapped within the agar matrix. Suppressor mutations that prevent this entanglement but do not restore chemotaxis, a phenomenon designated pseudotaxis, were first reported to arise for Escherichia coli. In this study, novel mechanisms of pseudotaxis have been identified for the plant-pathogenic alphaproteobacterium Agrobacterium tumefaciens. Mutants with chemotaxis mutation suppressor (cms) mutations that impart enhanced migration in motility agar compared to that of their straight-swimming, nonchemotactic parent were isolated. We find that pseudotaxis in A. tumefaciens occurs most commonly via mutations in the D1 domain of the flagellar hook protein, FlgE, but it can also be found less frequently to be due to mutations in the hook length regulator, FliK, or in the motor protein, MotA. Single-cell-tracking studies of cms mutants in bulk medium clearly reveal frequent changes in the direction of swimming, similar to the swimming of strains that are proficient for chemotaxis, but independent of a sensory mechanism. Our results suggest that the tumbling process can be tuned through mutation and evolution to optimize migration through complex, porous environments.
Importance: Chemotaxis sensory networks control direct bacterial motility by modulating flagellar rotary motion, alternating cellular movement between runs and tumbles. The straight-swimming phenotype of chemotaxis-deficient cells yields nonexpanding colonies in motility agar. Enhanced, chemotaxis-independent spreading, dubbed pseudotaxis, has been observed in Escherichia coli mutants. We have identified novel pseudotaxis mutations in Agrobacterium tumefaciens that alter the flagellar hook structure or motor, leading to randomly occurring reorientations observed in single-cell tracking studies in bulk medium. These directional changes allow the cells to migrate more efficiently than the parent strain through the agar matrix, independently of the chemotaxis process. These findings reveal that tumbling can be tuned for effective navigation in complex porous environments, analogous to the natural habitats for many bacteria, and provide evidence for the strong selective pressure exerted by the external environment on the basal pattern of motility, even in the absence of chemotaxis.
