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

Abstract

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 ...

sRNA-Mediated Control of Transcription Termination in E. coli

“…Rho is a multi-functional termination factor that together with its cofactor NusG is globally involved in transcription regulation (Nudler and Gottesman, 2002; Boudvillain et al, 2013; Grylak-Mielnicka et al, 2016). It is essential for generation of mRNA 3′ ends (Roberts, 1969), silencing horizontally transferred DNA elements (Cardinale et al, 2008), protecting genomic DNA from double-stranded breaks caused by transcription-replication collisions (Dutta et al, 2011), suppressing ubiquitous antisense transcription (Peters et al, 2012), and maintaining phage lysogeny (Menouni et al, 2013).…”

SraL sRNA interaction regulates the terminator by preventing premature transcription termination of rho mRNA

“…Rho is a helicase protein with RNA-dependent ATPase activity that catalyzes the disassociation of nascent mRNA from genomic DNA and RNA polymerase, promoting transcription termination. This protein is essential in many bacterial organisms, namely Escherichia coli, Salmonella enterica, Shigella flexneri, and Pseudomonas aeruginosa (3)(4)(5)(6). In fact, Rho is responsible for termination of about half of the transcription events in E. coli (7).…”

“…In fact, Rho is responsible for termination of about half of the transcription events in E. coli (7). Rho-dependent termination plays a significant role even in organisms in which it is not essential (4). For instance, Rho inactivation in Bacillus subtilis affects gene expression of important pathways related to cell motility, biofilm formation, and sporulation (8).…”

Learning from the Leaders: Gene Regulation by the Transcription Termination Factor Rho

“…Indeed, Rho has been found to execute several functions on a genome wide scale that maintain genome integrity and fidelity of gene expression. We briefly summarize these functions and refer readers to excellent reviews on this topic [6, 44, 45]. …”