Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA

Mellin, J. R.; Koutero, Mikael; Dar, Daniel; Nahori, Marie–Anne; Sorek, Rotem; Cossart, Pascale

doi:10.1126/science.1255083

Cited by 151 publications

(151 citation statements)

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“…This suggests tight links between metabolic sensing and virulence (Loh et al, 2009). Recent work in both Enterococcus faecalis (DebRoy et al, 2014) and L. monocytogenes (Mellin et al, 2014) shows that a B12-sensing riboswitch regulates the readthrough of an RNA that sequesters a 2CS response regulator, EutV, which senses ethanolamine. Lack of regulation attenuates Listeria virulence in mice.…”

Section: Srna Controlling Virulence Gene Expressionmentioning

confidence: 96%

“…We anticipated RNAs transcribed from autonomous intergenic regions (IGR) that activated or inhibited the translation of specific target mRNAs. Instead, we found an amazing complexity: sRNAs derived by processing from longer RNAs (Chao, Papenfort, Reinhardt, Sharma, & Vogel, 2012;Wadler & Vanderpool, 2007), bifunctional sRNAs that encode proteins (Gimpel, Heidrich, Mader, Krugel, & Brantl, 2010;Janzon, L€ ofdahl, & Arvidson, 1989;Novick et al, 1993;Wadler & Vanderpool, 2007), sRNAs that are decoys or act on other sRNAs (G€ opel, Papenfort, Reichenbach, Vogel, & G€ orke, 2013;Miyakoshi, Chao, & Vogel, 2015;Tree, Granneman, McAteer, Tollervey, & Gally, 2014), sRNAs that are regulatory targets of "trap" mRNAs (Figueroa-Bossi, Valentini, Malleret, Fiorini, & Bossi, 2009;Overgaard, Johansen, Moller-Jensen, & ValentinHansen, 2009), antisense-type sRNAs that moonlight as protein sequestrators (Jorgensen, Thomason, Havelund, Valentin-Hansen, & Storz, 2013), riboswitches that act as antisense-or protein-sequestrating sRNAs (DebRoy et al, 2014;Loh et al, 2009;Mellin et al, 2014), as well as protein factordependent or -independent sRNAs, antisense transcripts from many genomic locations (Lasa et al, 2011;Lybecker, Zimmermann, Bilusic, Tukhtubaeva, & Schroeder, 2014;Sharma et al, 2010), and a growing palette of mechanisms by which sRNAs affect gene expression. We will show specific examples that highlight the diversity of mechanisms, and will discuss the emerging impact of sRNAs on global regulatory circuits, where sRNAs either replace transcription factors (TFs) as regulatory nodes in network motifs, or add a second layer of posttranscriptional control with particular properties.…”

Section: What This Review Is Aboutmentioning

confidence: 98%

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Small RNAs in Bacteria and Archaea

Wagner

Romby

2015

Advances in Genetics

443

245

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Section: Srna Controlling Virulence Gene Expressionmentioning

confidence: 96%

Section: What This Review Is Aboutmentioning

confidence: 98%

Small RNAs in Bacteria and Archaea

Wagner

Romby

2015

Advances in Genetics

443

245

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“…1,2-Propanediol may be available for L. monocytogenes through the breakdown of salmon mucosal glycoconjugates, which contain fucose and rhamnose (80,81). Moreover, in L. monocytogenes, one cobalamin-binding riboswitch is located upstream of the first gene in the eut locus; this riboswitch regulates expression of eut in response to cobalamin availability (82). A second cobalamin-binding riboswitch is located upstream of the pdu locus; this riboswitch maximizes the expression of 1,2-propanediol utilization genes when both 1,2-propanediol and cobalamin are present (83).…”

Section: Figmentioning

confidence: 99%

Transcriptomic Analysis of the Adaptation of Listeria monocytogenes to Growth on Vacuum-Packed Cold Smoked Salmon

Tang

Orsi

Bakker

et al. 2015

Appl Environ Microbiol

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The foodborne pathogen Listeria monocytogenes is able to survive and grow in ready-to-eat foods, in which it is likely to experience a number of environmental stresses due to refrigerated storage and the physicochemical properties of the food. Little is known about the specific molecular mechanisms underlying survival and growth of L. monocytogenes under different complex conditions on/in specific food matrices. Transcriptome sequencing (RNA-seq) was used to understand the transcriptional landscape of L. monocytogenes strain H7858 grown on cold smoked salmon (CSS; water phase salt, 4.65%; pH 6.1) relative to that in modified brain heart infusion broth (MBHIB; water phase salt, 4.65%; pH 6.1) at 7°C. Significant differential transcription of 149 genes was observed (false-discovery rate [FDR], <0.05; fold change, >2.5), and 88 and 61 genes were up-and downregulated, respectively, in H7858 grown on CSS relative to the genes in H7858 grown in MBHIB. In spite of these differences in transcriptomes under these two conditions, growth parameters for L. monocytogenes were not significantly different between CSS and MBHIB, indicating that the transcriptomic differences reflect how L. monocytogenes is able to facilitate growth under these different conditions. Differential expression analysis and Gene Ontology enrichment analysis indicated that genes encoding proteins involved in cobalamin biosynthesis as well as ethanolamine and 1,2-propanediol utilization have significantly higher transcript levels in H7858 grown on CSS than in that grown in MBHIB. Our data identify specific transcriptional profiles of L. monocytogenes growing on vacuum-packaged CSS, which may provide targets for the development of novel and improved strategies to control L. monocytogenes growth on this ready-to-eat food.L isteria monocytogenes is a psychrotolerant foodborne pathogen that causes a potentially severe disease, listeriosis. This pathogen is of particular concern to the ready-to-eat (RTE) meat and seafood industries due to its ability to grow at temperatures as low as Ϫ0.4°C and under conditions of salt content as high as 25% (at 4°C) (1-3). Cold smoked salmon (CSS), an RTE seafood, represents a typical food product that can support the growth of L. monocytogenes from low numbers to potentially hazardous levels (4-9). The heat treatment applied during processing of CSS is not sufficient to inactivate microbes present on the raw material, including L. monocytogenes (10, 11). In addition, RTE food products, including CSS, can be contaminated with L. monocytogenes from environmental sources in processing facilities (10-13). Importantly, typical product characteristics of CSS, including pH, water activity (a w ), salt, and phenolic components, do not seem to be sufficient to control the growth of L. monocytogenes if it is present (8, 9).With the aim of developing control strategies that prevent or reduce growth of this pathogen in RTE seafood products, there is a need for a better understanding of the mechanisms that L. monocytogenes uses to sur...

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“…These transcriptional responses include high RNAPII activity in noncoding regions, resulting in lncRNA transcription. On the one hand, lncRNA molecules may provide function, for example through riboswitch regulation 35,36 . On the other hand, the process of lncRNA transcription by RNAPII can affect the regulation of gene expression in the vicinity of target Our study uncovers how the interplay between two lncRNA limits the production of maximal mRNA levels of the Arabidopsis CBF1 gene by an RNAPII collision mechanism.…”

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confidence: 99%

Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation

Kindgren

Ard

Ivanov

2018

Preprint

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SummaryMost DNA in the genomes of higher organisms does not encode proteins, but is transcribed by RNA polymerase II (RNAPII) into long non-coding RNA (lncRNA). The biological significance of most lncRNA is largely unclear. Here, we identify a lncRNA (SVALKA) in a cold-sensitive region of the Arabidopsis genome. Mutations in SVALKA affect the timing of maximal CBF1 expression and freezing tolerance. RNAPII read-through transcription of SVALKA results in a cryptic lncRNA overlapping CBF1 on the antisense strand, termed asCBF1. asCBF1 transcription is anti-correlated with CBF1 expression. Our molecular dissection reveals that CBF1 is suppressed by RNAPII collision stemming from the SVALKA-asCBF1 lncRNA cascade. The SVK-asCBF1 cascade provides a mechanism to tightly control CBF1 expression and timing that could be exploited to maximize freezing tolerance with mitigated fitness costs. Inversion of the transcriptional direction of a lncRNA cascade relative to the genes in a co-regulated cluster provides an elegant inbuilt negative feedback for cluster expression. Our results provide a compelling example of local gene regulation by lncRNA transcription having a profound impact on the ability of plants to appropriately acclimate to suboptimal environmental conditions. not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/287946 doi: bioRxiv preprint first posted online Mar. 23, 2018; Main RNA Polymerase II (RNAPII) transcription in genomes results in the production of many long noncoding RNAs (lncRNAs) 1 . The functional significance of resulting lncRNA molecules is actively debated even though biological roles are identified for an increasing number of examples [2][3][4] . Expression of lncRNAs is remarkably specific to the environmental condition, tissue or cell type, arguing for roles of lncRNA in regulation [5][6][7] . In addition to functions carried out by lncRNA molecules, the process of transcribing non-coding DNA sequences can by itself be regulatory in many systems 8,9 . Non-coding DNA regions in genomes can therefore affect gene expression by different mechanisms that need to be resolved experimentally.Sessile organisms respond to changing environmental conditions with regulation of gene expression. Early events in the Arabidopsis cold response include rapid transcriptional upregulation of the intron-less C-repeat/dehydration-responsive element binding factors (CBFs) 10,11 . The CBFs are highly conserved transcription factors that promote cold tolerance in many plant species and are often arranged in a single cluster 12. CBF expression during cold exposure activates downstream COLD REGULATED (COR) genes that promote freezing tolerance by adjusting the physiological and biochemical properties of plant cell interiors [13][14][15] . Intriguingly, constitutive CBF expression increases cold-tolerance but is also associated with fitness penalties [16][17][18][19] . antisense CBF1 lncRNA (...

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Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA

Cited by 151 publications

References 17 publications

Small RNAs in Bacteria and Archaea

Small RNAs in Bacteria and Archaea

Transcriptomic Analysis of the Adaptation of Listeria monocytogenes to Growth on Vacuum-Packed Cold Smoked Salmon

Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation

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