(470d) Exploring the Role of Flagella in Bacterial Swarming

Proteus mirabilis is an opportunistic pathogen that causes urinary
tract infections and the biofouling of urinary catheters.
A fundamental unanswered question has centered on the mechanism by which this
bacterium invades and colonizes the urinary epithelium. Swarming may provide a
clue to these infections.

During swarming on
nutrient agar in the lab, P. mirabilis
becomes morphologically differentiated and is characterized by long (20-100 um
long), multinucleate cells that have a remarkably high dense coating of
flagella. Back-of-the-envelope calculations of the energy balance in these
cells suggests that the assembly and actuation of flagella may account for as
much as ~50% of the total energy of the cell. This phenotype is clearly
important or it would have been lost long ago.

We explored the
physiological and behavior importance of the density of flagella on swarming P. mirabilis cells. By investigating the
swimming velocity of different P.
mirabilis cell morphologies—each with a different combination of cell
length and flagellar density—we discovered that swarmer cells have a
larger swimming velocity in solutions with a microviscosity
ranging from 10-1000 cP, compared to the other morphologies
that we tested. Swarmer cells were motile in fluids with a viscosity that
approached ~9000 cP; the motility of all other cells
types we studied was inhibited at this viscosity. Overexpression of FlhD₄C₂—the
transcription factor controlling the flagellar gene cascade—increased the
swimming velocity of vegetative cells in all of the viscous fluids we tested.
Furthermore, FlhD₄C₂ overexpression rescued vegetative
cell motility at ~9000 cP. Both immunofluorescence
microscopy and quantitative Western blots demonstrate a correlation between the
density of flagella and cell velocity and suggests a threshold density for
increasing the velocity of cells in high viscosity fluids. From these data and
the reported values for the number of flagella associated with other swarming
species, we speculate that an increase in flagellar density may be a universal
requirement for swarming motility. Our hypothesis is that the high density of flagella
on P. mirabilis may be responsible
for cell motility in high viscosity environments, including the mucus secreted
by the urinary epithelium, thereby providing a route to infection.