Viscosity-dependent determinants of Campylobacter jejuni impacting the velocity of flagellar motility

Abstract

ABSTRACT Campylobacter jejuni colonizes the thick mucus layer lining the lower intestinal epithelium of hosts to promote commensalism in birds and animals or diarrheal disease in humans. C. jejuni displays higher swimming velocity as external viscosity increases, which likely benefits colonization and persistence in the intestinal mucus layer of hosts. C. jejuni produces one of the most structurally complex bacterial flagellar motors, which has been proposed to generate high torque for high swimming velocity. However, it is unknown how this flagellar motor alters output to impact swimming velocities in a viscosity-dependent manner. In this work, we identified vi scosity-dependent d eterminant A (VidA) ( Cjj81176_0996 ) and VidB ( Cjj81176_1107 ) in modulating swimming velocity primarily in low-viscosity environments. C. jejuni Δ vidA cells were non-motile or swam slowly in low-viscosity media, but swam with high velocity similar to wild-type cells in both Newtonian and non-Newtonian media with high viscosity. These data indicate that VidA is required for swimming in low-viscosity environments. Suppressor mutants suggested that the lower swimming velocity of Δ vidA in low viscosity was due to unregulated activity of VidB, which we propose has a brake- or clutch-like activity to reduce swimming velocity in low viscosity. Unlike other bacterial flagellar brakes or clutches, we found no evidence for cyclic diguanylate monophosphate influencing VidB activity. Our analyses suggest that the mechanics of the C. jejuni flagellar motor has naturally evolved for high-velocity swimming in milieus with high viscosity and requires the unique combination of VidA and VidB to modulate its activity to slow swimming velocity in low-viscosity environments. IMPORTANCE Bacteria can adapt flagellar motor output in response to the load that the extracellular milieu imparts on the flagellar filament to enable propulsion. Bacteria can adapt flagellar motor output in response to the load that the extracellular milieu imparts on the flagellar filament to enable propulsion through diverse environments. These changes may involve increasing power and torque in high-viscosity environments or reducing power and flagellar rotation upon contact with a surface. C. jejuni swimming velocity in low-viscosity environments is comparable to other bacterial flagellates and increases significantly as external viscosity increases. In this work, we provide evidence that the mechanics of the C. jejuni flagellar motor has evolved to naturally promote high swimming velocity in high-viscosity environments. We found that C. jejuni produces VidA and VidB as auxiliary proteins to specifically affect flagellar motor activity in low viscosity to reduce swimming velocity. Our findings provide some of the first insights into different mechanisms that exist in bacteria to alter the mechanics of a flagellar motor, depending on the viscosity of extracellular environments.