The distribution of RNA polymerase in <i>Escherichia coli</i> is dynamic and sensitive to environmental cues

Cabrera, Julio E.; Jin, Ding Jun

doi:10.1046/j.1365-2958.2003.03805.x

Cited by 167 publications

(267 citation statements)

References 51 publications

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“…Because gene expression profiles reflect the distribution of RNAP at promoters across the genome (32), our data suggest that reprogramming of RNAP by binding ppGpp increases the transcription initiation frequency at many more promoters than had been recognized previously, including the CRP and RpoS regulons. Also, it was recently shown that growth arrest is accompanied by RelA-dependent, physical redistribution of RNAP (29). Thus, regardless of whether the ppGpp effect is direct or indirect, gene expression profiling of E. coli during diauxie supports the proposed switch model (Fig.…”

supporting

confidence: 58%

“…To our knowledge, all growth perturbations result in rapid accumulation of ppGpp (5, 28), which binds to RNAP and causes the down-regulation of the translation apparatus that characterizes the stringent response (5). Given that stable RNA synthesis constitutes up to Ϸ80% of transcription in rapidly growing cells (29,30), reduced transcription from these stringent promoters, which has been proposed to result from various mechanisms, including destabilization of the RNAP-promoter open complex or inactive dead-end promoter complexes (13,19,31), should greatly increase the availability of free RNAP (5,30). The indirect or so-called passive model postulates that the increased availability of RNAP caused by inhibition of rRNA transcription frees RNAP to bind to other promoters, i.e., amino acid biosynthetic genes and those shown in this study to be activated.…”

mentioning

confidence: 99%

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Guanosine 3′,5′-bispyrophosphate coordinates global gene expression during glucose-lactose diauxie in Escherichia coli

Traxler

Chang

Conway

2006

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

104

128

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Guanosine 3 ,5 -bispyrophosphate (ppGpp), also known as ''magic spot,'' has been shown to bind prokaryotic RNA polymerase to down-regulate ribosome production and increase transcription of amino acid biosynthesis genes during the stringent response to amino acid starvation. Because many environmental growth perturbations cause ppGpp to accumulate, we hypothesize ppGpp to have an overarching role in regulating the genetic program that coordinates transitions between logarithmic growth (feast) and growth arrest (famine). We used the classic glucose-lactose diauxie as an experimental system to investigate the temporal changes in transcription that accompany growth arrest and recovery in wildtype Escherichia coli and in mutants that lack RelA (ppGpp synthetase) and other global regulators, i.e., RpoS and Crp. In particular, diauxie was delayed in the relA mutant and was accompanied by a 15% decrease in the number of carbon sources used and a 3-fold overall decrease in the induction of RpoS and Crp regulon genes. Thus the data significantly expand the previously known role of ppGpp and support a model wherein the ppGpp-dependent redistribution of RNA polymerase across the genome is the driving force behind control of the stringent response, general stress response, and starvation-induced carbon scavenging. Our conceptual model of diauxie describes these global control circuits as dynamic, interconnected, and dependent upon ppGpp for the efficient temporal coordination of gene expression that programs the cell for transitions between feast and famine.catabolite repression ͉ stringent response ͉ conceptual model T he fitness of free-living organisms depends on their ability to withstand environmental insults and grow as rapidly as possible when conditions allow. Consequently, the coordination of growth control processes constitutes a fundamental level of regulation in prokaryotes. For this reason, the bacterial existence is often thought to be one of ''feast and famine'' (1). In the laboratory, nutritional conditions that cause biphasic growth provide a unique opportunity to investigate this most basic of bacterial behaviors. When cultured on a mixture of glucose and lactose, Escherichia coli grows preferentially on glucose until the glucose is exhausted, resulting in growth arrest while the cells adjust to growth on lactose, i.e., diauxie. The genetic basis for biphasic sugar catabolism, elucidated by Jacob and Monod (2), is exemplified by lac operon induction, which is a textbook paradigm for illustrating genetic control. However, transcriptome analysis revealed that diauxie involves much more than induction of the lac operon, and that diauxie is accompanied by a global response to growth arrest that apparently ensures recovery when conditions allow growth to resume (3). The purpose of this study is to dissect the regulatory networks that govern diauxie as a means for understanding how the cell integrates the response to growth arrest.We showed previously (3) that during steady-state logarithmic growth, gene expressi...

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supporting

confidence: 58%

mentioning

confidence: 99%

Guanosine 3′,5′-bispyrophosphate coordinates global gene expression during glucose-lactose diauxie in Escherichia coli

Traxler

Chang

Conway

2006

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

104

128

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“…and Jin 2003). The distances between pairs of rRNA operons were essentially the same in cells treated with rifampicin for different times and in the untreated cells (for the rrnD, rrnG pair, cf.…”

Section: (C) Oric Rrnc (Rlg11999) (D) Rrnb Oric (Rlg7440) (E) λAtmentioning

confidence: 86%

“…In previous wide-field studies using RNAP-GFP fusions, it was observed that the fluorescent RNAP foci disappeared, and RNAPs became evenly distributed when rRNA transcription was reduced or inhibited (Cabrera and Jin 2003). Similarly, inhibition of rRNA transcription in single-molecule studies resulted in more evenly distributed RNAPs (Endesfelder et al 2013).…”

Section: Other Modelsmentioning

confidence: 97%

“…Several reports in recent years have speculated that there might be nucleolus-like structures in bacteria (e.g., Lewis et al 2000;Cabrera and Jin 2003;Endesfelder et al 2013;Jin et al 2013). Fluorescence-labeled "transcription foci" were observed in fast-growing strains encoding fusions of GFP to RNAP, correlating with the high numbers of RNAP molecules expected to be engaged in transcribing rRNA under these conditions.…”

mentioning

confidence: 94%

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Colocalization of distant chromosomal loci in space in E. coli: a bacterial nucleolus

et al. 2016

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The spatial organization of DNA within the bacterial nucleoid remains unclear. To investigate chromosome organization in Escherichia coli, we examined the relative positions of the ribosomal RNA (rRNA) operons in space. The seven rRNA operons are nearly identical and separated from each other by as much as 180°on the circular genetic map, a distance of ≥2 million base pairs. By inserting binding sites for fluorescent proteins adjacent to the rRNA operons and then examining their positions pairwise in live cells by epifluorescence microscopy, we found that all but rrnC are in close proximity. Colocalization of the rRNA operons required the rrn P1 promoter region but not the rrn P2 promoter or the rRNA structural genes and occurred with and without active transcription. Non-rRNA operon pairs did not colocalize, and the magnitude of their physical separation generally correlated with that of their genetic separation. Our results show that E. coli bacterial chromosome folding in three dimensions is not dictated entirely by genetic position but rather includes functionally related, genetically distant loci that come into close proximity, with rRNA operons forming a structure reminiscent of the eukaryotic nucleolus.

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The Distribution and Spatial Organization of RNA Polymerase inEscherichia Coli: Growth Rate Regulation and Stress Responses

Jin

Cagliero²,

Izard

et al. 2016

Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria

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The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues

Cited by 167 publications

References 51 publications

Guanosine 3′,5′-bispyrophosphate coordinates global gene expression during glucose-lactose diauxie in Escherichia coli

Guanosine 3′,5′-bispyrophosphate coordinates global gene expression during glucose-lactose diauxie in Escherichia coli

Colocalization of distant chromosomal loci in space in E. coli: a bacterial nucleolus

The Distribution and Spatial Organization of RNA Polymerase inEscherichia Coli: Growth Rate Regulation and Stress Responses

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