Type IV pilins regulate their own expression via direct intramembrane interactions with the sensor kinase PilS

Kilmury, Sara L.N.; Burrows, Lori L.

doi:10.1073/pnas.1512947113

Cited by 54 publications

(72 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Finally, PilS is localized at the poles in P. aeruginosa where it may interact with the T4P machinery, including pooled PilA (Boyd, ; Ethier and Boyd, ). In fact, it was recently demonstrated that P. aeruginosa PilA directly interacts with PilS (Kilmury and Burrows, ). In total, the results suggest that PilS monitors the concentration of PilA at the inner membrane, but does not measure assembled T4P.…”

Section: Discussionmentioning

confidence: 99%

Type IV‐pili dependent motility is co‐regulated by PilSR and PilS2R2 two‐component systems via distinct pathways in Myxococcus xanthus

Bretl

Müller

Ladd

et al. 2016

Molecular Microbiology

View full text Add to dashboard Cite

Myxococcus xanthus is an environmental bacterium with two forms of motility. One type, known as social motility, is dependent on extension and retraction of Type-IV pili (T4P) and production of extracellular polysaccharides (EPS). Several signaling systems have been linked to regulation of T4P-dependent motility. In particular, expression of the pilin subunit pilA requires the PilSR two-component signaling system (TCS). A second TCS, PilS2R2, encoded within the same locus that encodes PilSR, has also been linked to M. xanthus T4P-dependent motility. We demonstrate that PilSR and PilS2R2 regulate M. xanthus T4P-dependent motility through distinct pathways. Consistent with known roles of PilSR, our results indicate that the primary function of PilSR is to regulate expression of pilA. In contrast, PilS2 and PilR2 have little to no affect on PilA protein levels. However, deletion of pilR2 resulted in a reduction of assembled pili, significant decreases in EPS production and loss of T4P-dependent motility. Furthermore, the pilR2 mutation led to increased production of outer membrane vesicles (OMV). Collectively, we propose that PilS2R2 is required for proper assembly of T4P and regulation of OMV production, and hypothesize that production of these vesicles is related to M. xanthus motility.

show abstract

Section: Discussionmentioning

confidence: 99%

Type IV‐pili dependent motility is co‐regulated by PilSR and PilS2R2 two‐component systems via distinct pathways in Myxococcus xanthus

Bretl

Müller

Ladd

et al. 2016

Molecular Microbiology

View full text Add to dashboard Cite

show abstract

“…The N terminus is highly hydrophobic, and harbors the input domain that contains six transmembrane helices interspersed with short loops (residues 21–189) (Figure S1). Residues 313–376 are predicted to function as a transmitter domain, as it contains two motifs, histidine (H) at position 325 and motif E/DxxN/T, that are commonly found in SKs (Figures c and S1) (Huynh, Noriega, & Stewart, ; Kilmury & Burrows, ). When the input domain of a SK detects a signal, the conserved H autophosphorylates, initiating a signaling cascade that activates transcription of the target gene.…”

Section: Resultsmentioning

confidence: 99%

“…Pae PilS, the Nps homolog, also has six such transmembrane domains. Pae PilS is both a kinase and phosphatase; it senses the levels of membrane‐bound pilin (PilA) and regulates pilA expression through its phosphatase activity (Boyd et al., ; Kilmury & Burrows, ). The PilS kinase and phosphatase motifs are highly conserved across all Neisseria Nps (Figures and S1).…”

Section: Discussionmentioning

confidence: 99%

“…The PilS kinase and phosphatase motifs are highly conserved across all Neisseria Nps (Figures and S1). The amino acids arginine 24 in PilS, and glutamate 5 and proline 22 in PilA are important for PilS/PilA interactions and PilS autoregulation (Kilmury & Burrows, ). These residues are also present in all Neisseria Nps and PilE (Figures S1 and S6, respectively).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

RpoN and the Nps and Npa two‐component regulatory system control pilE transcription in commensal Neisseria

Rendón

Lona

et al. 2018

MicrobiologyOpen

View full text Add to dashboard Cite

Over 20 genes are involved in the biogenesis and function of the Neisseria Type IV pilus (Tfp). In the pathogenic species, RpoD and the integration host factor (IHF) protein regulate expression of pilE, encoding the Tfp structural subunit. We previously reported that in commensal species, pilE transcription is regulated by RpoN, IHF, and activator Npa. Npa has many hallmarks of response regulators in two-component regulatory systems, leading us to search for its response regulator partner. We report that Npa partners with sensor kinase Nps to control pilE transcription. Among the genes involved in Tfp biogenesis and function, only pilE is controlled by RpoN and Npa/Nps. We summarize our findings in a model, and discuss the implications of the differential regulation of pilE the context of Neisseria Tfp biogenesis.

show abstract

“…FimV is required for bipolar localization of PilG and FimL and the T4aP structural proteins PilMNOPQ but not the Chp methyl-accepting chemotaxis protein (MCP) PilJ (22,30). To determine if FimV is required for the localization of other T4aP regulators, we examined its effects on the localization of PilS (37,38), the histidine sensor kinase component of the PilRS two-component system that regulates pilA transcription in response to changes in PilA levels in the inner membrane (39).…”

Section: Resultsmentioning

confidence: 99%

Cyclic AMP-Independent Control of Twitching Motility in Pseudomonas aeruginosa

et al. 2017

Self Cite

View full text Add to dashboard Cite

FimV is a Pseudomonas aeruginosa inner membrane hub protein that modulates levels of the second messenger, cyclic AMP (cAMP), through the activation of adenylate cyclase CyaB. Although type IVa pilus (T4aP)-dependent twitching motility is modulated by cAMP levels, mutants lacking FimV are twitching impaired, even when exogenous cAMP is provided. Here we further define FimV's cAMPdependent and -independent regulation of twitching. We confirmed that the response regulator of the T4aP-associated Chp chemotaxis system, PilG, requires both FimV and the CyaB regulator, FimL, to activate CyaB. However, in cAMP-replete backgrounds-lacking the cAMP phosphodiesterase CpdA or the CheY-like protein PilH or expressing constitutively active CyaB-pilG and fimV mutants failed to twitch. Both cytoplasmic and periplasmic domains of FimV were important for its cAMPdependent and -independent roles, while its septal peptidoglycan-targeting LysM motif was required only for twitching motility. Polar localization of the sensor kinase PilS, a key regulator of transcription of the major pilin, was FimV dependent. However, unlike its homologues in other species that localize flagellar system components, FimV was not required for swimming motility. These data provide further evidence to support FimV's role as a key hub protein that coordinates the polar localization and function of multiple structural and regulatory proteins involved in P. aeruginosa twitching motility.IMPORTANCE Pseudomonas aeruginosa is a serious opportunistic pathogen. Type IVa pili (T4aP) are important for its virulence, because they mediate dissemination and invasion via twitching motility and are involved in surface sensing, which modulates pathogenicity via changes in cAMP levels. Here we show that the hub protein FimV and the response regulator of the Chp system, PilG, regulate twitching independently of their roles in the modulation of cAMP synthesis. These functions do not require the putative scaffold protein FimL, proposed to link PilG with FimV. PilG may regulate asymmetric functioning of the T4aP system to allow for directional movement, while FimV appears to localize both structural and regulatory elements-including the PilSR two-component system-to cell poles for optimal function.

show abstract

Type IV pilins regulate their own expression via direct intramembrane interactions with the sensor kinase PilS

Cited by 54 publications

References 57 publications

Type IV‐pili dependent motility is co‐regulated by PilSR and PilS2R2 two‐component systems via distinct pathways in Myxococcus xanthus

Type IV‐pili dependent motility is co‐regulated by PilSR and PilS2R2 two‐component systems via distinct pathways in Myxococcus xanthus

RpoN and the Nps and Npa two‐component regulatory system control pilE transcription in commensal Neisseria

Cyclic AMP-Independent Control of Twitching Motility in Pseudomonas aeruginosa

Contact Info

Product

Resources

About