H-NS and RNA polymerase: a love–hate relationship?

Landick, Robert; Wade, Joseph T.; Grainger, David C.

doi:10.1016/j.mib.2015.01.009

Cited by 65 publications

(55 citation statements)

References 58 publications

(75 reference statements)

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“…H-NS binds DNA at high-affinity sites, and forms nucleoprotein filaments that spread on AT-rich DNA and bridge distant DNA sites (reviewed by Seshasayee, 2014;Landick et al, 2015). H-NS is known to play an important role in the silencing of horizontally acquired genes and in the suppression of non-coding transcription by inhibition of both transcription initiation and elongation (Saxena & Gowrishankar, 2011;Peters et al, 2012; Singh et al, 2014).…”

Section: Suppression Of Pervasive Transcriptionmentioning

confidence: 99%

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

et al. 2016

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Factor-dependent termination of transcription in bacteria relies on the activity of a specific RNA helicase, the termination factor Rho. Rho is nearly ubiquitous in bacteria, but the extent to which its physiological functions are conserved throughout the different phyla remains unknown. Most of our current knowledge concerning the mechanism of Rho's activity and its physiological roles comes from the model micro-organism Escherichia coli, where Rho is essential and involved in the control of several important biological processes. However, the rather comprehensive knowledge about the general mechanisms of action and activities of Rho based on the E. coli paradigm cannot be directly extrapolated to other bacteria. Recent studies performed in different species favour the view that Rho-dependent termination plays a significant role even in bacteria where Rho is not essential. Here, we summarize the current state of the ever-increasing knowledge about the various aspects of the physiological functions of Rho, such as limitation of deleterious foreign DNA expression, control of gene expression, suppression of pervasive transcription, prevention of R-loops and maintenance of chromosome integrity, focusing on similarities and differences of the activities of Rho in various bacterial species. Introduction Transcription termination is a critical step in gene regulation in all living organisms. In bacteria, transcription termination is well known to be essential for the generation of different types of functional RNAs, the definition of the boundaries of the transcriptional units, the release of RNA polymerase (RNAP) and the regulation of gene expression via the mechanism known as transcription attenuation (Peters et al., 2011;Santangelo & Artsimovitch, 2011).However, recent studies have revealed new roles of transcriptional termination, e.g. those linked to the maintenance of genome integrity or degradation of untranslated mRNAs. Particular attention is now paid to transcription termination due to its crucial role in the control of pervasive transcription. This type of genome-wide transcription, not associated with annotated genome features such as protein-coding genes, is a universal phenomenon for all the three domains of life and viruses (Georg & Hess, 2011;Wade & Grainger, 2014). In eukaryotes, pervasive transcription arises mainly from bidirectional promoters that synthesize both mRNA and diverse non-coding RNAs, but this phenomenon is also controlled by selective transcriptional termination (Kapranov et al., 2007;Schulz et al., 2013). Recently, an essential role of transcription termination in the control of pervasive transcription was demonstrated for both Gram-positive and Gram-negative model micro-organisms Bacillus subtilis and Escherichia coli (Nicolas et al., 2012;Peters et al., 2012).In bacteria, transcription termination is achieved by two mechanisms: factor-independent (intrinsic) and factordependent termination. Intrinsic termination is strongly associated with sequence-specific signals characterized by ...

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Section: Suppression Of Pervasive Transcriptionmentioning

confidence: 99%

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

et al. 2016

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“…In many bacterial species, horizontally acquired sequences are bound by the histone-like nucleoid structuring (H-NS) protein (12), which preferentially associates with AT-rich sequences through recognition of structural features of the minor groove of the DNA helix (13). H-NS can oligomerize along, or form cross-bridges between, AT-rich regions, thereby producing filamentous nucleoprotein complexes and stabilizing DNA hairpins (14).…”

Section: Observationmentioning

confidence: 99%

“…H-NS can oligomerize along, or form cross-bridges between, AT-rich regions, thereby producing filamentous nucleoprotein complexes and stabilizing DNA hairpins (14). H-NS binding is associated with transcriptional silencing, due both to reduced access of transcription machinery to H-NS-bound promoters and to Rho-dependent transcriptional termination resulting from increased transcriptional pausing in bound regions (13). H-NS-mediated repression is overcome by the activity of transcription factors and other DNA binding proteins that compete with H-NS for target sites (12).…”

Section: Observationmentioning

confidence: 99%

The Nucleoid Binding Protein H-NS Biases Genome-Wide Transposon Insertion Landscapes

Kimura

Hubbard

Davis

et al. 2016

mBio

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Transposon insertion sequencing (TIS; also known as TnSeq) is a potent approach commonly used to comprehensively define the genetic loci that contribute to bacterial fitness in diverse environments. A key presumption underlying analyses of TIS datasets is that loci with a low frequency of transposon insertions contribute to fitness. However, it is not known whether factors such as nucleoid binding proteins can alter the frequency of transposon insertion and thus whether TIS output may systematically reflect factors that are independent of the role of the loci in fitness. Here, we investigated whether the histone-like nucleoid structuring (H-NS) protein, which preferentially associates with AT-rich sequences, modulates the frequency of Mariner transposon insertion in the Vibrio cholerae genome, using comparative analysis of TIS results from wild-type (wt) and Δhns V. cholerae strains. These analyses were overlaid on gene classification based on GC content as well as on extant genome-wide identification of H-NS binding loci. Our analyses revealed a significant dearth of insertions within AT-rich loci in wt V. cholerae that was not apparent in the Δhns insertion library. Additionally, we observed a striking correlation between genetic loci that are overrepresented in the Δhns insertion library relative to their insertion frequency in wt V. cholerae and loci previously found to physically interact with H-NS. Collectively, our findings reveal that factors other than genetic fitness can systematically modulate the frequency of transposon insertions in TIS studies and add a cautionary note to interpretation of TIS data, particularly for AT-rich sequences.

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“…The binding of H-NS to DNA has been exclusively studied (39,76), and the results indicate that H-NS silences extensive regions of the bacterial genome by binding first to nucleating high-affinity sites and then spreading along AT-rich DNA (6). In this study, the H-NS binding sites in the lateral flagellar genes (motY and lafB) were identified by DNase I footprinting assay (Fig.…”

Section: Discussionmentioning

confidence: 73%

The Histone-Like Nucleoid Structuring Protein (H-NS) Is a Negative Regulator of the Lateral Flagellar System in the Deep-Sea Bacterium Shewanella piezotolerans WP3

Jian

Gai

et al. 2016

Appl Environ Microbiol

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cAlthough the histone-like nucleoid structuring protein (H-NS) is well known for its involvement in the adaptation of mesophilic bacteria, such as Escherichia coli, to cold environments and high-pressure stress, an understanding of the role of H-NS in the cold-adapted benthic microorganisms that live in the deep-sea ecosystem, which covers approximately 60% of the earth's surface, is still lacking. In this study, we characterized the function of H-NS in Shewanella piezotolerans WP3, which was isolated from West Pacific sediment at a depth of 1,914 m. An hns gene deletion mutant (WP3⌬hns) was constructed, and comparative whole-genome microarray analysis was performed. H-NS had a significant influence (fold change, >2) on the expression of a variety of WP3 genes (274 and 280 genes were upregulated and downregulated, respectively), particularly genes related to energy production and conversion. Notably, WP3⌬hns exhibited higher expression levels of lateral flagellar genes than WP3 and showed enhanced swarming motility and lateral flagellar production compared to those of WP3. The DNA gel mobility shift experiment showed that H-NS bound specifically to the promoter of lateral flagellar genes. Moreover, the high-affinity binding sequences of H-NS were identified by DNase I protection footprinting, and the results support the "binding and spreading" model for H-NS functioning. To our knowledge, this is the first attempt to characterize the function of the universal regulator H-NS in a deep-sea bacterium. Our data revealed that H-NS has a novel function as a repressor of the expression of genes related to the energy-consuming secondary flagellar system and to swarming motility.T he histone-like nucleoid structuring protein (H-NS), which was originally identified as a small, heat-stable protein factor that stimulates bacteriophage DNA transcription (1), is widely distributed in Gram-negative bacteria (2). By recognizing and selectively silencing the expression of xenogeneic DNA sequences (3-6), H-NS differentially regulates horizontally acquired and core-genome genes (7). As a multifunctional bacterial modulator, the phenotypes that result from hns mutations are highly pleiotropic and involve diverse functions, such as conjugative transfer (8), outer membrane protein expression (9), fimbrial gene transcription (10), lipopolysaccharide production (11), motility and osmolarity (12), biofilm formation and exopolysaccharide biosynthesis (13), and the superinfection of bacteriophages and induction of the clustered regularly interspaced short palindromic repeat (CRISPR)-cas system (14-16), especially in the environmental adaptation of some pathogenic bacteria (17-21). Given the importance of maintaining fitness when laterally acquired genes are uncontrollably expressed, mutations in hns are lethal in Salmonella enterica serovar Typhimurium (22) and Yersinia enterocolitica (23).In an Escherichia coli hns mutant, the expression of approximately 5% of genes is altered, and one-third of these genes encode proteins that are usuall...

show abstract

H-NS and RNA polymerase: a love–hate relationship?

Cited by 65 publications

References 58 publications

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

Transcription termination factor Rho: a hub linking diverse physiological processes in bacteria

The Nucleoid Binding Protein H-NS Biases Genome-Wide Transposon Insertion Landscapes

The Histone-Like Nucleoid Structuring Protein (H-NS) Is a Negative Regulator of the Lateral Flagellar System in the Deep-Sea Bacterium Shewanella piezotolerans WP3

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