Role of pili and the phase-variable PilC protein in natural competence for transformation of Neisseria gonorrhoeae.

Rudel, Thomas; Facius, Dirk; Barten, Roland; Scheuerpflug, Ina; Nonnenmacher, Edgar; Meyer, Thomas F.

doi:10.1073/pnas.92.17.7986

Cited by 109 publications

(102 citation statements)

References 32 publications

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“…These results support the notion that the binding of DNA to ComE is not sequence specific. Strains with mutations of pilC, whose product is a pilus tip adhesin (35), are impaired in their ability to take up DNA and undergo transformation; competence could be partially restored in these mutants by supplying them with exogenous purified PilC (34). We tested rComE in a similar way and found that exogenously added ComE did not restore the transformation ability of comE mutant bacteria (data not shown).…”

Section: Vol 183 2001mentioning

confidence: 93%

“…Neisseria has type IV pili (TFP), and it was early observed that piliation is necessary for DNA uptake (3), but it is still not known whether pili themselves participate in the process, since DNA-binding activity has not been detected in pilus components (26). Among the genes known to be necessary for competence are those encoding components of the TFP, such as pilE (pilin) and pilC (tip adhesin) (34), and those encoding proteins involved in pilus biogenesis (pilD, pilG, pilF, and pilQ) or function, such as twitching motility (pilT) (10,14,42,44). Mutations in these genes result in the absence of pili or in nonfunctional pili.…”

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confidence: 99%

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ComE, a Competence Protein from Neisseria gonorrhoeae with DNA-Binding Activity

Chen

Gotschlich

2001

J Bacteriol

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Neisseria gonorrhoeae is naturally able to take up exogenous DNA and undergo genetic transformation. This ability correlates with the presence of functional type IV pili, and uptake of DNA is dependent on the presence of a specific 10-bp sequence. Among the known competence factors in N. gonorrhoeae, none has been shown to interact with the incoming DNA. Here we describe ComE, a DNA-binding protein involved in neisserial competence. The gene comE was identified through similarity searches in the gonococcal genome sequence, using as the query ComEA, the DNA receptor in competent Bacillus subtilis. The gene comE is present in four identical copies in the genomes of both N. gonorrhoeae and Neisseria meningitidis, located downstream of each of the rRNA operons. Single-copy deletion of comE in N. gonorrhoeae did not have a measurable effect on competence, whereas serial deletions led to gradual decrease in transformation frequencies, reaching a 4 ؋ 10 4 -fold reduction when all copies were deleted. Transformation deficiency correlated with impaired ability to take up exogenous DNA; however, the mutants presented normal piliation and twitching motility phenotype. The product of comE has 99 amino acids, with a predicted signal peptide; by immunodetection, a 8-kDa protein corresponding to processed ComE was observed in different strains of N. gonorrhoeae and N. meningitidis. Recombinant His-tagged ComE showed DNA binding activity, without any detectable sequence specificity. Thus, we identified a novel gonococcal DNA-binding competence factor which is necessary for DNA uptake and does not affect pilus biogenesis or function.

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Section: Vol 183 2001mentioning

confidence: 93%

mentioning

confidence: 99%

ComE, a Competence Protein from Neisseria gonorrhoeae with DNA-Binding Activity

Chen

Gotschlich

2001

J Bacteriol

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“…The DNA transformation systems of B. subtilis and H. influenzae, microorganisms which have never been found to exhibit type IV pilus structures, contain components similar to proteins implicated in type IV pilus biogenesis in other organisms (5,20,40). In N. gonorrhoeae, which exhibits a type IV piliation phenotype, the structural subunits of type IV pili (PilE) and the type IV pilus factor PilC are essential for DNA transformation (7,35). Furthermore it was demonstrated that gonococcal PilT mutants exhibit simultaneous defects in competence for natural transformation and twitching motility (43).…”

Section: Discussionmentioning

confidence: 99%

ComP, a Pilin-Like Protein Essential for Natural Competence in Acinetobacter sp. Strain BD413: Regulation, Modification, and Cellular Localization

et al. 2000

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We recently identified a pilin-like competence factor, ComP, which is essential for natural transformation of the gram-negative soil bacterium Acinetobacter sp. strain BD413. Here we demonstrate that transcription and synthesis of the pilin-like competence factor ComP are maximal in the late stationary growth phase, whereas competence is induced immediately after inoculation of a stationary-phase culture into fresh medium. Western blot analyses revealed three forms of ComP, one with an apparent molecular mass of 15 kDa, which correlates with the molecular mass deduced from the DNA sequence, one 20-kDa form, which was found to be glycosylated, and one 23-kDa form. The glycosylation of ComP was not required for its function in DNA binding and uptake. The 20-kDa form was present in the cytoplasmic membrane, the periplasm, and the outer membrane, whereas the 23-kDa form was located in the outer membrane and might be due to a further modification. Immunological data suggest that ComP is not a subunit of the pilus structures. Possible functions of ComP in the DNA transformation machinery of Acinetobacter sp. strain BD413 are discussed.

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“…3). Interestingly, while the presence of pili on the bacterial surface per se may not be required for DNA uptake, production of the major pilin is necessary (91,206,382,509,562). These findings suggest that some (but not all) components of T4P are involved in DNA uptake (141,142,189,509,602,644).…”

Section: Dna Uptake and Processingmentioning

confidence: 99%

“…T4P are hair-like appendages found on the bacterial surface that mediate cellular adhesion and twitching motility, which is a form of bacterial translocation due to polymerization or extension of the pilus fiber, attachment to a nearby surface, and then depolymerization or retraction of the pilus (112,404,417,543,621). T4P are composed of a major pilin (PilE), a minor pilin (PilV), a traffic NTPase (PilT), an ATPase (PilF), a transmembrane secretin (PilQ), a prepilin processing peptidase (PilD), a pilot protein (PilP), and an adhesin (PilC) (1,27,57,59,66,91,141,189,295,342,509,602,644) (Fig. 3).…”

Section: Dna Uptake and Processingmentioning

confidence: 99%

Change Is Good: Variations in Common Biological Mechanisms in the Epsilonproteobacterial GeneraCampylobacterandHelicobacter

Gilbreath

Cody

Merrell

et al. 2011

Microbiol Mol Biol Rev

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SUMMARY Microbial evolution and subsequent species diversification enable bacterial organisms to perform common biological processes by a variety of means. The epsilonproteobacteria are a diverse class of prokaryotes that thrive in diverse habitats. Many of these environmental niches are labeled as extreme, whereas other niches include various sites within human, animal, and insect hosts. Some epsilonproteobacteria, such as Campylobacter jejuni and Helicobacter pylori , are common pathogens of humans that inhabit specific regions of the gastrointestinal tract. As such, the biological processes of pathogenic Campylobacter and Helicobacter spp. are often modeled after those of common enteric pathogens such as Salmonella spp. and Escherichia coli . While many exquisite biological mechanisms involving biochemical processes, genetic regulatory pathways, and pathogenesis of disease have been elucidated from studies of Salmonella spp. and E. coli , these paradigms often do not apply to the same processes in the epsilonproteobacteria. Instead, these bacteria often display extensive variation in common biological mechanisms relative to those of other prototypical bacteria. In this review, five biological processes of commonly studied model bacterial species are compared to those of the epsilonproteobacteria C. jejuni and H. pylori . Distinct differences in the processes of flagellar biosynthesis, DNA uptake and recombination, iron homeostasis, interaction with epithelial cells, and protein glycosylation are highlighted. Collectively, these studies support a broader view of the vast repertoire of biological mechanisms employed by bacteria and suggest that future studies of the epsilonproteobacteria will continue to provide novel and interesting information regarding prokaryotic cellular biology.

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Role of pili and the phase-variable PilC protein in natural competence for transformation of Neisseria gonorrhoeae.

Cited by 109 publications

References 32 publications

ComE, a Competence Protein from Neisseria gonorrhoeae with DNA-Binding Activity

ComE, a Competence Protein from Neisseria gonorrhoeae with DNA-Binding Activity

ComP, a Pilin-Like Protein Essential for Natural Competence in Acinetobacter sp. Strain BD413: Regulation, Modification, and Cellular Localization

Change Is Good: Variations in Common Biological Mechanisms in the Epsilonproteobacterial GeneraCampylobacterandHelicobacter

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