A four‐tiered transcriptional regulatory circuit controls flagellar biogenesis in <i>Pseudomonas aeruginosa</i>

Dasgupta, Nandini; Wolfgang, Matthew C.; Goodman, Andrew L.; Arora, Shiwani K.; Jyot, Jeevan; Lory, Stephen; Ramphal, Reuben

doi:10.1046/j.1365-2958.2003.03740.x

Cited by 400 publications

(599 citation statements)

References 39 publications

(75 reference statements)

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“…In the absence of cascade control of motility gene transcription, B. burgdorferi appears to rely exclusively on translational control of its motility genes. Finally, as found in many other species of bacteria, mutation of flgE results in inhibition of the expression of chemotaxis genes (16,34,36). These genes are generally the last genes transcribed in the cascade.…”

Section: Discussionmentioning

confidence: 78%

“…For B. burgdorferi, evidence suggests that S is directly controlled by 54 (61,66). 54 directly participates in the transcription of motility gene expression in other bacteria, such as Caulobacter crescentus, Vibrio species, Pseudomonas aeruginosa, and Helicobacter species (4,16,44,50). Although it has been speculated that 54 -like promoter sequences are upstream of some of the motility genes in B. burgdorferi (17), there is no definitive proof that transcription is initiated at these sites.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, completion of the hook-basal body structure acts as a general assembly checkpoint in the regulation of flagellum synthesis whereby flagellin and other genes are transcriptionally controlled in response to the state of hook completion (30). A similar scheme of cascade control of motility gene expression is found in many species of bacteria, and in some species, 54 (RpoN) also directly participates in the cascade control of motility gene regulation (1,4,16,44,50).…”

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confidence: 95%

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Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

et al. 2008

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Borrelia burgdorferi is a flat-wave, motile spirochete that causes Lyme disease. Motility is provided by periplasmic flagella (PFs) located between the cell cylinder and an outer membrane sheath. The structure of these PFs, which are composed of a basal body, a hook, and a filament, is similar to the structure of flagella of other bacteria. To determine if hook formation influences flagellin gene transcription in B. burgdorferi, we inactivated the hook structural gene flgE by targeted mutagenesis. In many bacteria, completion of the hook structure serves as a checkpoint for transcriptional control of flagellum synthesis and other chemotaxis and motility genes. Specifically, the hook allows secretion of the anti-sigma factor FlgM and concomitant late gene transcription promoted by 28 . However, the control of B. burgdorferi PF synthesis differs from the control of flagellum synthesis in other bacteria; the gene encoding 28 is not present in the genome of B. burgdorferi, nor are any 28 promoter recognition sequences associated with the motility genes. We found that B. burgdorferi flgE mutants lacked PFs, were rod shaped, and were nonmotile, which substantiates previous evidence that PFs are involved in both cell morphology and motility. Although most motility and chemotaxis gene products accumulated at wild-type levels in the absence of FlgE, mutant cells had markedly decreased levels of the flagellar filament proteins FlaA and FlaB. Further analyses showed that the reduction in the levels of flagellin proteins in the spirochetes lacking FlgE was mediated at the posttranscriptional level. Taken together, our results indicate that in B. burgdorferi, the completion of the hook does not serve as a checkpoint for transcriptional regulation of flagellum synthesis. In addition, we also present evidence that the hook protein in B. burgdorferi forms a high-molecular-weight complex and that formation of this complex occurs in the periplasmic space.Borrelia burgdorferi, the causative agent of Lyme disease, is a spirochete with a characteristic flat-wave morphology (24, 25; for a review, see reference 12). As a result of their unusual morphology, B. burgdorferi and other spirochete species have a highly specialized ability that allows them to traverse viscous gellike media (8). This unique swimming ability enables these bacteria to penetrate into specific host connective tissues and ecological niches (43). The importance of motility as a virulence factor has been implicated in several spirochete species, including Treponema denticola (42), Brachyspira hyodysenteriae (54), Borrelia garinii (60), and B. burgdorferi (10, 56).Motility in B. burgdorferi is provided by bundles of between 7 and 11 periplasmic flagella (PFs) that are subterminally attached near the cell ends. These PFs extend inward along the cell cylinder beneath an outer membrane sheath (6,24,28,46). B. burgdorferi PFs have a structure similar to that of flagella of other bacteria; a PF is composed of a basal body, a hook, and a filament containing a single major ...

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Section: Discussionmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 95%

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Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

et al. 2008

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“…Among the two-component regulatory genes that were significantly upregulated in all three interactions was the regulatory gene Pfl01_1534. This gene is an ortholog of fleR in P. aeruginosa, which is a regulator of genes for flagella biogenesis, chemotaxis, fimbrial biogenesis, and several genes annotated as 'hypothetical' (Dasgupta et al, 2003). Elevated expression of this regulator may suggest that motility and/or chemotaxis are important and general components of the P. fluorescens response to other bacteria.…”

Section: Discussionmentioning

confidence: 99%

Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors

et al. 2011

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The ability of soil bacteria to successfully compete with a range of other microbial species is crucial for their growth and survival in the nutrient-limited soil environment. In the present work, we studied the behavior and transcriptional responses of soil-inhabiting Pseudomonas fluorescens strain Pf0-1 on nutrient-poor agar to confrontation with strains of three phylogenetically different bacterial genera, that is, Bacillus, Brevundimonas and Pedobacter. Competition for nutrients was apparent as all three bacterial genera had a negative effect on the density of P. fluorescens Pf0-1; this effect was most strong during the interaction with Bacillus. Microarray-based analyses indicated strong differences in the transcriptional responses of Pf0-1 to the different competitors. There was higher similarity in the gene expression response of P. fluorescens Pf0-1 to the Gram-negative bacteria as compared with the Gram-positive strain. The Gram-negative strains did also trigger the production of an unknown broad-spectrum antibiotic in Pf0-1. More detailed analysis indicated that expression of specific Pf0-1 genes involved in signal transduction and secondary metabolite production was strongly affected by the competitors' identity, suggesting that Pf0-1 can distinguish among different competitors and fine-tune its competitive strategies. The results presented here demonstrate that P. fluorescens Pf0-1 shows a species-specific transcriptional and metabolic response to bacterial competitors and provide new leads in the identification of specific cues in bacteria-bacteria interactions and of novel competitive strategies, antimicrobial traits and genes.

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“…The P. aeruginosa wild type strain PAK used in this study is a common strain fully expressing virulence factors including T2SS, T3SS, pili and flagellum [26]. PAK ∆ fliC , a flagellin-deficient strain (Fla-), is derivated from the wild type strain where fliC has been deleted [63]. In a same way, PAK ∆ pscF (a T3SS deficient strain), PAK ∆xcpQ (a T2SS-deficient strain), and PAK ∆fliC∆xcpQ∆pscF (deficient for Fla, T2SS and T3SS) were generated [64].…”

Section: Methodsmentioning

confidence: 99%

Pseudomonas aeruginosa flagellum is critical for invasion, cutaneous persistence and induction of inflammatory response of skin epidermis

Garcia

Morello

Garnier³

et al. 2018

Virulence

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Pseudomonas aeruginosa, an opportunistic pathogen involved in skin and lung diseases, possesses numerous virulence factors, including type 2 and 3 secretion systems (T2SS and T3SS) and its flagellum, whose functions remain poorly known during cutaneous infection. Using isogenic mutants deleted from genes encoding each or all of these three virulence factors, we investigated their role in induction of inflammatory response and in tissue invasiveness in human primary keratinocytes and reconstructed epidermis. Our results showed that flagellum, but not T2SS and T3SS, is involved in induction of a large panel of cytokine, chemokine, and antimicrobial peptide (AMP) mRNA in the infected keratinocytes. Chemokine secretion and AMP tissular production were also dependent on the presence of the bacterial flagellum. This pro-inflammatory effect was significantly reduced in keratinocytes infected in presence of anti-toll-like receptor 5 (TLR5) neutralizing antibody. Bacterial invasion of human epidermis and persistence in a mouse model of sub-cutaneous infection were dependent on the P. aeruginosa flagellum. We demonstrated that flagellum constitutes the main virulence factor of P. aeruginosa involved not only in early induction of the epidermis inflammatory response but also in bacterial invasion and cutaneous persistence. P. aeruginosa is mainly sensed by TLR5 during the early innate immune response of human primary keratinocytes.

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A four‐tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa

Cited by 400 publications

References 39 publications

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

Borrelia burgdorferi Uniquely Regulates Its Motility Genes and Has an Intricate Flagellar Hook-Basal Body Structure

Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors

Pseudomonas aeruginosa flagellum is critical for invasion, cutaneous persistence and induction of inflammatory response of skin epidermis

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