The Pseudomonas aeruginosa PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
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ABSTRACT
Motility is an important virulence trait for many bacterial pathogens, allowing them to position themselves in appropriate locations at appropriate times. The motility structures type IV pili and flagella are also involved in sensing surface contact, which modulates pathogenicity. In
Pseudomonas aeruginosa
, the PilS-PilR two-component system (TCS) regulates expression of the type IV pilus (T4P) major subunit PilA, while biosynthesis of the single polar flagellum is regulated by a hierarchical system that includes the FleSR TCS. Previous studies of
Geobacter sulfurreducens
and
Dichelobacter nodosus
implicated PilR in regulation of non-T4P-related genes, including some involved in flagellar biosynthesis. Here we used transcriptome sequencing (RNA-seq) analysis to identify genes in addition to
pilA
with changes in expression in the absence of
pilR
. Among the genes identified were 10 genes whose transcription increased in the
pilA
mutant but decreased in the
pilR
mutant, despite both mutants lacking T4P and pilus-related phenotypes. The products of these inversely dysregulated genes, many of which were hypothetical, may be important for virulence and surface-associated behaviors, as mutants had altered swarming motility, biofilm formation, type VI secretion system expression, and pathogenicity in a nematode model. Further, the PilSR TCS positively regulated transcription of
fleSR
, and thus many genes in the FleSR regulon. As a result,
pilSR
deletion mutants had defects in swimming motility that were independent of the loss of PilA. Together, these data suggest that in addition to controlling T4P expression, PilSR could have a broader role in the regulation of
P. aeruginosa
motility and surface sensing behaviors.
IMPORTANCE
Surface appendages such as type IV pili and flagella are important for establishing surface attachment and infection in a host in response to appropriate cues. The PilSR regulatory system that controls type IV pilus expression in
Pseudomonas aeruginosa
has an established role in expression of the major pilin PilA. Here we provide evidence supporting a new role for PilSR in regulating flagellum-dependent swimming motility in addition to pilus-dependent twitching motility. Further, even though both
pilA
and
pilR
mutants lack PilA and pili, we identified sets of genes downregulated in the
pilR
mutant and upregulated in a
pilA
mutant as well as genes downregulated only in a
pilR
mutant, independent of pilus expression. This finding suggests that change in the inner membrane levels of PilA is only one of the cues to which PilR responds to modulate gene expression. Identification of PilR as a regulator of multiple motility pathways may make it an interesting therapeutic target for antivirulence compounds.
