Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator

Hollands, Kerry; Sevostiyanova, Anastasia; Groisman, Eduardo A.

doi:10.1073/pnas.1319193111

Cited by 56 publications

(60 citation statements)

References 63 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The explanation may lie with pleiotropic effects. RNAP mutants have the capacity to affect the expression of every gene, but rho influences termination in a subset of 20-50% of E. coli genes (42,43). Because rpoB has the potential for more pleiotropic interactions, it likely also has a higher probability to generate fitness tradeoffs via antagonistic pleiotropy.…”

Section: Discussionmentioning

confidence: 99%

Different tradeoffs result from alternate genetic adaptations to a common environment

Rodríguez‐Verdugo

Carrillo-Cisneros

González-González

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

122

View full text Add to dashboard Cite

Fitness tradeoffs are often assumed by evolutionary theory, yet little is known about the frequency of fitness tradeoffs during stress adaptation. Even less is known about the genetic factors that confer these tradeoffs and whether alternative adaptive mutations yield contrasting tradeoff dynamics. We addressed these issues using 114 clones of Escherichia coli that were evolved independently for 2,000 generations under thermal stress (42.2°C). For each clone, we measured their fitness relative to the ancestral clone at 37°C and 20°C. Tradeoffs were common at 37°C but more prevalent at 20°C, where 56% of clones were outperformed by the ancestor. We also characterized the upper and lower thermal boundaries of each clone. All clones shifted their upper boundary to at least 45°C; roughly half increased their lower niche boundary concomitantly, representing a shift of thermal niche. The remaining clones expanded their thermal niche by increasing their upper limit without a commensurate increase of lower limit. We associated these niche dynamics with genotypes and confirmed associations by engineering single mutations in the rpoB gene, which encodes the beta subunit of RNA polymerase, and the rho gene, which encodes a termination factor. Single mutations in the rpoB gene exhibit antagonistic pleiotropy, with fitness tradeoffs at 18°C and fitness benefits at 42.2°C. In contrast, a mutation within the rho transcriptional terminator, which defines an alternative adaptive pathway from that of rpoB, had no demonstrable effect on fitness at 18°C. This study suggests that two different genetic pathways toward high-temperature adaptation have contrasting effects with respect to thermal tradeoffs.RNA polymerase | Rho factor | genotype-phenotype associations | experimental evolution D espite the centrality of adaptation to evolution, surprisingly little is known about the diversity of mutations that contribute to adaptation or about their phenotypic and fitness effects (1). There are, in fact, only a few well-known examples linking genotype, phenotype, and adaptation in nature (2-4). In nature, this connection is often complicated by factors such as varying selection pressures or underlying genetic heterogeneities. Although the task is difficult, the general inability to connect phenotype to genotype in the context of environmental adaptation has been a major failing in the field of evolution (5).Experimental evolution provides a more tractable approach to study relationships among fitness, genotype, and phenotype (5, 6). Here we explore these relationships based on our recent, large-scale evolutionary experiment (7). The experiment began with an ancestral strain of Escherichia coli B that was inoculated into ∼115 independent replicates. Each replicate was grown at high temperature (42.2°C) for 2,000 generations. At the end of the experiment, fitness was measured at 42.2°C for a single clone from each of 114 lineages; on average, fitness increased ∼40% during the yearlong experiment.We sequenced the genome of these 114 clones, ...

show abstract

Section: Discussionmentioning

confidence: 99%

Different tradeoffs result from alternate genetic adaptations to a common environment

Rodríguez‐Verdugo

Carrillo-Cisneros

González-González

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

122

View full text Add to dashboard Cite

show abstract

“…Regulation of Rho-dependent termination by riboswitches was described for the Mg 2+ -sensing mgtA riboswitch from Salmonella enterica (Hollands et al, 2012(Hollands et al, , 2014 for the flavin mononucleotide-sensing ribB riboswitch from E. coli (Hollands et al, 2012) and flavin mononucleotide riboswitch from the Gram-positive Corynebacterium glutamicum (Takemoto et al, 2015). In general, depending on the ligand concentration (e.g.…”

Section: Regulation Of Gene Expressionmentioning

confidence: 99%

“…The significance of riboswitch function lies in the transduction of ligand binding into changes in expression of the downstream gene. Recently, it was shown that some riboswitches use Rho to attenuate transcription, thus linking Rho to the process of sensing and regulating gene expression in response to environmental cues (Proshkin et al, 2014).Regulation of Rho-dependent termination by riboswitches was described for the Mg 2+ -sensing mgtA riboswitch from Salmonella enterica (Hollands et al, 2012(Hollands et al, , 2014 for the flavin mononucleotide-sensing ribB riboswitch from E. coli (Hollands et al, 2012) and flavin mononucleotide riboswitch from the Gram-positive Corynebacterium glutamicum (Takemoto et al, 2015). In general, depending on the ligand concentration (e.g.…”

mentioning

confidence: 99%

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

et al. 2016

View full text Add to dashboard Cite

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 ...

show abstract

“…When this happens, the mgtA leader mRNA adopts a conformation that advances transcription elongation into the mgtA coding region. By contrast, when cytosolic Mg 2+ remains high, the conformation of the mgtA leader mRNA promotes transcription termination within the leader by the Rho protein [80,81]. …”

Section: Introductionmentioning

confidence: 99%

When Too Much ATP Is Bad for Protein Synthesis

Pontes

Sevostyanova

Groisman

2015

Journal of Molecular Biology

Self Cite

102

View full text Add to dashboard Cite

Adenosine triphosphate (ATP) is the energy currency of living cells. Even though ATP powers virtually all energy-dependent activity, most cellular ATP is utilized in protein synthesis via tRNA aminoacylation and GTP regeneration. Magnesium (Mg2+), the most common divalent cation in living cells, plays crucial roles in protein synthesis by maintaining the structure of ribosomes, participating in the biochemistry of translation initiation and functioning as a counter-ion for ATP. A non-physiological increase in ATP levels hinders growth in cells experiencing Mg2+ limitation because ATP is the most abundant nucleotide triphosphate in the cell and Mg2+ is also required for the stabilization of the cytoplasmic membrane and as a cofactor for essential enzymes. We propose that organisms cope with Mg2+ limitation by decreasing ATP levels and ribosome production, thereby reallocating Mg2+ to indispensable cellular processes.

show abstract

Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator

Cited by 56 publications

References 63 publications

Different tradeoffs result from alternate genetic adaptations to a common environment

Different tradeoffs result from alternate genetic adaptations to a common environment

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

When Too Much ATP Is Bad for Protein Synthesis

Contact Info

Product

Resources

About