Comparative Analysis of Regulatory Elements between Escherichia coli and Klebsiella pneumoniae by Genome-Wide Transcription Start Site Profiling

Kim, Donghyuk; Hong, Jay Sung-Joong; Qiu, Yu; Nagarajan, Harish; Seo, Joo‐Hyun; Cho, Byung-Kwan; Tsai, Shih‐Feng; Palsson, Bernhard Ø.

doi:10.1371/journal.pgen.1002867

Cited by 132 publications

(135 citation statements)

References 80 publications

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“…S1) and that the location of the copper responsive CpxR-dependent transcription start site (TSS) at the yqjA promoter in E. coli (Yamamoto and Ishihama, 2006) matches well with one of two TSSs determined at the corresponding promoter on the S. enterica genome (Fig. S1) (Kim et al, 2012;Ramachandran et al, 2012). The growth rate of the quadratic mutant ugd pmrR degP yqjA was similar to that of the quadratic mutant in the presence of all the concentrations of Fe 3+ ugd pmrR degP cpxR (Fig.…”

Section: Fig 2 Growth Of Isogenic Pmrrsupporting

confidence: 58%

Fe3+-dependent epistasis between the CpxR-activated loci and the PmrA-activated LPS modification loci in Salmonella enterica

Kato

Higashino

Utsumi

2016

J. Gen. Appl. Microbiol.

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Bacteria utilize varying combinations of twocomponent regulatory systems, many of which respond and adapt closely to stress conditions, thus expanding their niche steadily. While mechanisms of recognition and avoidance of the specific Fe 3+ signal by the PmrA/PmrB system is well understood, those of the CpxR/CpxA system are more complex because they can be induced by various stress conditions, which, in turn, expresses a variety of phenotypes. Here, we highlight another aspect of the CpxR/CpxA system; mutations in degP and yqjA genes, which are under the control of the system, exhibit an iron sensitive phenotype in the mutant background defective in the PmrA-dependent gene products that alter the pyrophosphate status of the lipid A moiety of lipopolysaccharide in Salmonella enterica. Therefore, after the PmrA/ PmrB-mediated Fe 3+ -dependent control of the pyrophosphate status on the cell surface, the CpxR/ CpxA system is one of the second layers of envelope stress response that allows adaptation to high Fe 3+ conditions in this bacterium.

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Section: Fig 2 Growth Of Isogenic Pmrrsupporting

confidence: 58%

Fe3+-dependent epistasis between the CpxR-activated loci and the PmrA-activated LPS modification loci in Salmonella enterica

Kato

Higashino

Utsumi

2016

J. Gen. Appl. Microbiol.

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“…The enrichment for two T residues comprising a potential 70 Ϫ35 element was significantly less than what was observed for the Ϫ10 element; however, both pTSS and iTSS logos showed some enrichment for a G at position Ϫ14, characteristic of an extended Ϫ10 sequence associated with 70 promoters with weak Ϫ35 elements. A window of Ϫ50 to ϩ5 relative to the TSS revealed that a subset of pTSS, iTSS, and asTSS show enrichment for a purine at ϩ1 and a pyrimidine at Ϫ1, features of E. coli 70 promoters reported previously (10). Overall, despite differences in the dRNA-seq signal, most of the pTSS, iTSS, and asTSS are likely transcribed by the 70 holoenzyme.…”

Section: Drna-seq Reveals the Primary Transcriptome Of E Coli Mg1655mentioning

confidence: 51%

“…Even for the transcriptome analyses of the well-studied model organism Escherichia coli (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22), the numbers of asRNAs reported range from hundreds to thousands. This significant variation is due, in part, to differences in cDNA library preparation, sequencing technology, and coverage as well as the criteria for what is considered an asRNA.…”

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confidence: 99%

Global Transcriptional Start Site Mapping Using Differential RNA Sequencing Reveals Novel Antisense RNAs in Escherichia coli

et al. 2015

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cWhile the model organism Escherichia coli has been the subject of intense study for decades, the full complement of its RNAs is only now being examined. Here we describe a survey of the E. coli transcriptome carried out using a differential RNA sequencing (dRNA-seq) approach, which can distinguish between primary and processed transcripts, and an automated prediction algorithm for transcriptional start sites (TSS). With the criterion of expression under at least one of three growth conditions examined, we predicted 14,868 TSS candidates, including 5,574 internal to annotated genes (iTSS) and 5,495 TSS corresponding to potential antisense RNAs (asRNAs). We examined expression of 14 candidate asRNAs by Northern analysis using RNA from wild-type E. coli and from strains defective for RNases III and E, two RNases reported to be involved in asRNA processing. Interestingly, nine asRNAs detected as distinct bands by Northern analysis were differentially affected by the rnc and rne mutations. We also compared our asRNA candidates with previously published asRNA annotations from RNA-seq data and discuss the challenges associated with these cross-comparisons. Our global transcriptional start site map represents a valuable resource for identification of transcription start sites, promoters, and novel transcripts in E. coli and is easily accessible, together with the cDNA coverage plots, in an online genome browser.A fter many years of study, we are only now beginning to understand and appreciate the complexity of bacterial transcriptomes. With the recent advances in deep-sequencing technology, transcriptome sequencing (RNA-seq) now allows for the detection of transcripts that are present at low levels or were previously missed by other methods of detection, the generation of global transcript maps, and improved genome annotation (reviewed in references 1 and 2). While these studies provide vast amounts of information about bacterial transcriptomes and regulatory elements, they also raise challenges regarding comparisons between studies and functions of the newly identified transcripts.One group of underappreciated transcripts being uncovered by these genome-wide analyses are RNAs that map opposite annotated coding regions, termed antisense RNAs (asRNAs). The abundance of pervasive antisense transcription start sites (asTSS) was first highlighted in an RNA-seq survey of the human pathogen Helicobacter pylori, where asTSS were identified opposite ϳ46% of the genes (3). Subsequent RNA-seq studies in cyanobacteria (4) and Gram-negative (5, 6) and Gram-positive (7-9) bacteria identified asRNAs expressed opposite 2 to 30% of annotated genes. This wide range in numbers of asRNAs reported may reflect differences in bacterial lifestyle or differences in the experimental setup or analyses of the RNA-seq data sets.Even for the transcriptome analyses of the well-studied model organism Escherichia coli (10-22), the numbers of asRNAs reported range from hundreds to thousands. This significant variation is due, in part, to differences i...

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“…These changes are particularly relevant because ATP and GTP are the strongly preferred initiating NTPs in E. coli (26,(29)(30)(31). Our comparisons of the resulting promoters suggest that the importance of start site sequence is, at least in large part, its contribution to the base-pairing strength of the RNA-DNA hybrid formed by the first 4 or 5 residues at the 5= end of the nascent transcript and the DNA template.…”

Section: Discussionmentioning

confidence: 87%

“…These two sites are the most preferred locations for transcription initiation in E. coli, with position 7 typically the better start site unless it is occupied by a poor initiating nucleotide (26,(29)(30)(31). The effect of spacing, observed with promoters FIG 6 Levels of productive carAp 1 ::lacZ transcripts initiated in vivo at wildtype and mutant carAB P1 promoters with different spacing between the Ϫ10 region and transcription start site.…”

Section: Discussionmentioning

confidence: 99%

Transcription Start Site Sequence and Spacing between the −10 Region and the Start Site Affect Reiterative Transcription-Mediated Regulation of Gene Expression in Escherichia coli

Han

Turnbough

2014

J Bacteriol

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Reiterative transcription is a reaction catalyzed by RNA polymerase, in which nucleotides are repetitively added to the 3= end of a nascent transcript due to upstream slippage of the transcript without movement of the DNA template. In Escherichia coli, the expression of several operons is regulated through mechanisms in which high intracellular levels of UTP promote reiterative transcription that adds extra U residues to the 3= end of a nascent transcript during transcription initiation. Immediately following the addition of one or more extra U residues, the nascent transcripts are released from the transcription initiation complex, thereby reducing the level of gene expression. Therefore, gene expression can be regulated by internal UTP levels, which reflect the availability of external pyrimidine sources. The magnitude of gene regulation by these mechanisms varies considerably, even when control mechanisms are analogous. These variations apparently are due to differences in promoter sequences. One of the operons regulated (in part) by UTP-sensitive reiterative transcription in E. coli is the carAB operon, which encodes the first enzyme in the pyrimidine nucleotide biosynthetic pathway. In this study, we used the carAB operon to examine the effects of nucleotide sequence at and near the transcription start site and spacing between the start site and ؊10 region of the promoter on reiterative transcription and gene regulation. Our results indicate that these variables are important determinants in establishing the extent of reiterative transcription, levels of productive transcription, and range of gene regulation. Usually during transcription, the nascent RNA transcript and the template strand of DNA move in tandem as an RNA-DNA hybrid. However, during transcription of a homopolymeric tract in the DNA template, the nascent transcript can slip (typically) one base upstream without movement of the DNA template within the active site of RNA polymerase (RNAP) (1, 2). This repositioning allows the same template base to specify an additional nucleotide in the transcript, and when transcript slippage occurs repetitively, the same template nucleotide can specify multiple extra residues. This reaction is called reiterative transcription (also known as RNAP stuttering, transcription slippage, and pseudotemplated transcription) and appears to be catalyzed by all RNAPs (2-5). Reiterative transcription can involve the repetitive addition of any of the four nucleoside triphosphate substrates and occurs during transcription initiation, elongation, and termination (2, 3, 6, 7). During initiation, when the length of the RNA-DNA hybrid can be shorter than that of the 8-to 9-bp hybrid that forms during elongation (8), a homopolymeric tract as short as three residues can enable reiterative transcription (9, 10). In contrast, longer homopolymeric tracts usually are required for reiterative transcription during elongation and termination (6, 7).The physiological significance of reiterative transcription is that it plays a central rol...

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Comparative Analysis of Regulatory Elements between Escherichia coli and Klebsiella pneumoniae by Genome-Wide Transcription Start Site Profiling

Cited by 132 publications

References 80 publications

Fe<sup>3+</sup>-dependent epistasis between the CpxR-activated loci and the PmrA-activated LPS modification loci in <i>Salmonella enterica</i>

Fe<sup>3+</sup>-dependent epistasis between the CpxR-activated loci and the PmrA-activated LPS modification loci in <i>Salmonella enterica</i>

Global Transcriptional Start Site Mapping Using Differential RNA Sequencing Reveals Novel Antisense RNAs in Escherichia coli

Transcription Start Site Sequence and Spacing between the −10 Region and the Start Site Affect Reiterative Transcription-Mediated Regulation of Gene Expression in Escherichia coli

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