MvaT proteins in Pseudomonas spp.: a novel class of H-NS-like proteins

Tendeng, Christian; Soutourina, Olga; Danchin, Antoine; Bertin, Philippe

doi:10.1099/mic.0.c0125-0

Cited by 72 publications

(67 citation statements)

References 20 publications

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“…Under standard laboratory growth conditions, expression of the cupA gene cluster is tightly repressed by MvaT (37), a putative transcription regulator that is thought to functionally resemble members of the H-NS family of nucleoid-associated proteins (34). MvaT from P. aeruginosa was originally identified as a global regulator of virulence gene expression (7), and recent microarray analyses have revealed that MvaT controls the expression of at least 150 or so genes in P. aeruginosa, with the cupA genes being the most tightly repressed (37).…”

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Local and Global Regulators Linking Anaerobiosis tocupAFimbrial Gene Expression inPseudomonas aeruginosa

2007

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The cupA gene cluster of Pseudomonas aeruginosa encodes components and assembly factors of a putative fimbrial structure that enable this opportunistic pathogen to form biofilms on abiotic surfaces. In P. aeruginosa the control of cupA gene expression is complex, with the H-NS-like MvaT protein functioning to repress phase-variable (on/off) expression of the operon. Here we identify four positive regulators of cupA gene expression, including three unusual regulators encoded by the cgrABC genes and Anr, a global regulator of anaerobic gene expression. We show that the cupA genes are expressed in a phase-variable manner under anaerobic conditions and that the cgr genes are essential for this expression. We show further that cgr gene expression is negatively controlled by MvaT and positively controlled by Anr and anaerobiosis. Expression of the cupA genes therefore appears to involve a regulatory cascade in which anaerobiosis, signaled through Anr, stimulates expression of the cgr genes, resulting in a concomitant increase in cupA gene expression. Our findings thus provide mechanistic insight into the regulation of cupA gene expression and identify anaerobiosis as an inducer of phase-variable cupA gene expression, raising the possibility that phase-variable expression of fimbrial genes important for biofilm formation may occur in P. aeruginosa persisting in the largely anaerobic environment of the cystic fibrosis host lung.The gram-negative bacterium Pseudomonas aeruginosa is an opportunistic pathogen of humans that is notorious for being the principal cause of morbidity and mortality in cystic fibrosis (CF) patients; chronic colonization of the CF lung by P. aeruginosa typically leads to progressive lung damage and eventually respiratory failure and death (13). In the CF lung the organism is thought to persist as a biofilm, forming clusters of cells encased in a polymeric matrix (32). In this biofilm mode of growth P. aeruginosa exhibits increased resistance to antibiotics and is better able to evade the host immune response (6). Recent evidence suggests that the microbial environment in the CF lung is largely anaerobic (43) and that cells of P. aeruginosa persist in the CF lung in anaerobic biofilms (47). Indeed, the biofilm formed by cells of P. aeruginosa under anaerobic conditions is especially robust (47).The cupA gene cluster of P. aeruginosa encodes components of a putative fimbrial structure that enables this organism to form biofilms on abiotic surfaces (36). Under standard laboratory growth conditions, expression of the cupA gene cluster is tightly repressed by MvaT (37), a putative transcription regulator that is thought to functionally resemble members of the H-NS family of nucleoid-associated proteins (34). MvaT from P. aeruginosa was originally identified as a global regulator of virulence gene expression (7), and recent microarray analyses have revealed that MvaT controls the expression of at least 150 or so genes in P. aeruginosa, with the cupA genes being the most tightly repressed (37). Several o...

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Local and Global Regulators Linking Anaerobiosis tocupAFimbrial Gene Expression inPseudomonas aeruginosa

2007

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“…MvaU is the second H-NS family member in P. aeruginosa, is less abundant than MvaT, and can interact with MvaT (58,59). Although MvaT and MvaU bear little sequence identity to their enteric counterparts, certain predicted structural similarities and known functional similarities suggest that they belong to the H-NS family (8,9,13,55,56,58,59). MvaU appears to play a less prominent role in the control of gene expression in P. aeruginosa than MvaT (58,59).…”

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Basis for the Essentiality of H-NS Family Members in Pseudomonas aeruginosa

Castang

Dove

2012

J. Bacteriol.

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ABSTRACTMembers of the histone-like nucleoid-structuring (H-NS) family of proteins have been shown to play important roles in silencing gene expression and in nucleoid compaction. InPseudomonas aeruginosa, the two H-NS family members MvaT and MvaU are thought to bind the same AT-rich regions of the chromosome and function coordinately to control a common set of genes. Here we present evidence that the loss of both MvaT and MvaU cannot be tolerated because it results in the production of Pf4 phage that superinfect and kill cells or inhibit their growth. Using a ClpXP-based protein depletion system in combination with transposon mutagenesis, we identify mutants ofP. aeruginosathat can tolerate the depletion of MvaT in an ΔmvaUmutant background. Many of these mutants contain insertions in genes encoding components, assembly factors, or regulators of type IV pili or contain insertions in genes of the prophage Pf4. We demonstrate that cells that no longer produce type IV pili or that no longer produce the replicative form of the Pf4 genome can tolerate the loss of both MvaT and MvaU. Furthermore, we show that the loss of both MvaT and MvaU results in an increase in expression of Pf4 genes and that cells that cannot produce type IV pili are resistant to infection by Pf4 phage. Our findings suggest that type IV pili are the receptors for Pf4 phage and that the essential activities of MvaT and MvaU are to repress the expression of Pf4 genes.

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“…As a consequence of the strong homology with H-NS, StpA is predicted to be very similar in its overall structure. Although MvaT bears little homology to E.coli H-NS, the C-terminal domains of these proteins have been predicted to be structurally very similar (26). In addition, the N-terminal domain of MvaT, like that of H-NS, is predicted to be ␣-helical and capable of dimerization (26).…”

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“…Nevertheless, these proteins can be identified by screening genomic libraries for reversal of the H-NS deficiency in E. coli mutant strains (17). Recently, a novel class of H-NS like proteins was found in Pseudomonas species (19,25,26). These so-called MvaT proteins do not exhibit any significant homology with any known H-NS-related protein (e.g., 18% identity with E. coli H-NS).…”

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DNA Bridging: a Property Shared among H-NS-Like Proteins

et al. 2005

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The nucleoid-associated protein H-NS is thought to play an essential role in the organization of bacterial chromatin in Escherichia coli. Homologues, often with very low sequence identity, are found in most gramnegative bacteria. Microscopic analysis reveals that, despite limited sequence identity, their structural organization results in similar DNA binding properties.The chromosomal DNA of bacteria is organized into a compact structure, the nucleoid. A number of factors contribute to maintaining this compact state: macromolecular crowding (or depletion), DNA supercoiling, and so-called nucleoid-associated proteins (28). It is unclear how much each of these factors contributes to nucleoid compactness, but nucleoid-associated proteins play an essential role.

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MvaT proteins in Pseudomonas spp.: a novel class of H-NS-like proteins

Cited by 72 publications

References 20 publications

Local and Global Regulators Linking Anaerobiosis tocupAFimbrial Gene Expression inPseudomonas aeruginosa

Local and Global Regulators Linking Anaerobiosis tocupAFimbrial Gene Expression inPseudomonas aeruginosa

Basis for the Essentiality of H-NS Family Members in Pseudomonas aeruginosa

DNA Bridging: a Property Shared among H-NS-Like Proteins

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