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Inefficient Secretion of Anti-sigma Factor FlgM Inhibits Bacterial Motility at High Temperature.

ABSTRACT: Temperature is one of the key cues that enable microorganisms to adjust their physiology in response to environmental changes. Here we show that motility is the major cellular function of Escherichia coli that is differentially regulated between growth at normal host temperature of 37°C and the febrile temperature of 42°C. Expression of both class II and class III flagellar genes is reduced at 42°C because of lowered level of the upstream activator FlhD. Class III genes are additionally repressed because of the destabilization and malfunction of secretion apparatus at high temperature, which prevents secretion of the anti-sigma factor FlgM. This mechanism of repression apparently accelerates loss of motility at 42°C. We hypothesize that E. coli perceives high temperature as a sign of inflammation, downregulating flagella to escape detection by the immune system of the host. Secretion-dependent coupling of gene expression to the environmental temperature is likely common among many bacteria.

SUBMITTER: Rudenko I

PROVIDER: S-EPMC6551532 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Inefficient Secretion of Anti-sigma Factor FlgM Inhibits Bacterial Motility at High Temperature.

Rudenko Iaroslav I Ni Bin B Glatter Timo T Sourjik Victor V

iScience 20190520

Temperature is one of the key cues that enable microorganisms to adjust their physiology in response to environmental changes. Here we show that motility is the major cellular function of Escherichia coli that is differentially regulated between growth at normal host temperature of 37°C and the febrile temperature of 42°C. Expression of both class II and class III flagellar genes is reduced at 42°C because of lowered level of the upstream activator FlhD. Class III genes are additionally represse ...[more]

PMID: 31170626

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Project description:Legionella oakridgensis causes Legionnaires' disease but is known to be less virulent than Legionella pneumophilaL. oakridgensis is one of the Legionella species that is nonflagellated. The genes of the flagellar regulon are absent, except those encoding the alternative sigma-28 factor (FliA) and its anti-sigma-28 factor (FlgM). Similar to L. oakridgensis, Legionella adelaidensis and Legionella londiniensis, located in the same phylogenetic clade, have no flagellar regulon, although both are positive for fliA and flgM Here, we investigated the role and function of both genes to better understand the role of FliA, the positive regulator of flagellin expression, in nonflagellated strains. We demonstrated that the FliA gene of L. oakridgensis encodes a functional sigma-28 factor that enables the transcription start from the sigma-28-dependent promoter site. The investigations have shown that FliA is necessary for full fitness of L. oakridgensis Interestingly, expression of FliA-dependent genes depends on the growth phase and temperature, as already shown for L. pneumophila strains that are flagellated. In addition, we demonstrated that FlgM is a negative regulator of FliA-dependent gene expression. FlgM seems to be degraded in a growth-phase- and temperature-dependent manner, instead of being exported into the medium as reported for most bacteria. The degradation of FlgM leads to an increase of FliA activity.IMPORTANCE A less virulent Legionella species, L. oakridgensis, causes Legionnaires' disease and is known to not have flagella, even though L. oakridgensis has the regulator of flagellin expression (FliA). This protein has been shown to be involved in the expression of virulence factors. Thus, the strain was chosen for use in this investigation to search for FliA target genes and to identify putative virulence factors of L. oakridgensis One of the five major target genes of FliA identified here encodes the anti-FliA sigma factor FlgM. Interestingly, in contrast to most homologs in other bacteria, FlgM in L. oakridgensis seems not to be transported from the cell so that FliA gets activated. In L. oakridgensis, FlgM seems to be degraded by protease activities.

Project description:FlgM, an antagonist of FliA (also known as σ28), inhibits transcription of bacterial class 3 flagellar genes. It does so primarily through binding to free σ28 to prevent it from forming a complex with core RNA polymerase. We recently identified an FliA homolog (FliATd) in the oral spirochete Treponema denticola; however, its antagonist FlgM remained uncharacterized. Herein, we provide several lines of evidence that TDE0201 functions as an antagonist of FliATd. TDE0201 is structurally similar to FlgM proteins, although its sequence is not conserved. Heterologous expression of TDE0201 in Escherichia coli inhibits its flagellin gene expression and motility. Biochemical and mutational analyses demonstrate that TDE0201 binds to FliATd and prevents it from binding to the σ28-dependent promoter. Deletions of flgM genes typically enhance bacterial class 3 flagellar gene expression; however, deletion of TDE0201 has an opposite effect (e.g., the mutant has a reduced level of flagellins). Follow-up studies revealed that deletion of TDE0201 leads to FliATd turnover, which in turn impairs the expression of flagellin genes. Swimming plate, cell tracking, and cryo-electron tomography analyses further disclosed that deletion of TDE0201 impairs spirochete motility and alters flagellar number and polarity: i.e., instead of having bipolar flagella, the mutant has flagella only at one end of cells. Collectively, these results indicate that TDE0201 is a FlgM homolog but acts differently from its counterparts in other bacteria. IMPORTANCE Spirochetes are a group of bacteria that cause several human diseases. A unique aspect of spirochetes is that they have bipolar periplasmic flagella (PFs), which bestow on the spirochetes a unique spiral shape and distinct swimming behaviors. While the structure and function of PFs have been extensively studied in spirochetes, the molecular mechanism that regulates the PFs' morphogenesis and assembly is poorly understood. In this report, FlgM, an anti-σ28 factor, is identified and functionally characterized in the oral spirochete Treponema denticola. Our results show that FlgM regulates the number and polarity of PFs via a unique mechanism. Identification of FliA and FlgM in T. denticola sets a benchmark to investigate their roles in other spirochetes.

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Inefficient Secretion of Anti-sigma Factor FlgM Inhibits Bacterial Motility at High Temperature.

Publications

Inefficient Secretion of Anti-sigma Factor FlgM Inhibits Bacterial Motility at High Temperature.

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