Discoordinate gene expression of gyrA and gyrB in response to DNA gyrase inhibition in Escherichia coli

Neumann, Susanne; Quiñones, Ariel

doi:10.1002/jobm.3620370109

Cited by 16 publications

(17 citation statements)

References 39 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Moreover, P A may be induced under specific conditions which require only the production of excess GyrA. For instance, there is at least one report of induction of GyrA alone in E. coli in response to treatment with GyrA inhibitors (18).…”

Section: Discussionmentioning

confidence: 99%

DNA Gyrase Genes in Mycobacterium tuberculosis : a Single Operon Driven by Multiple Promoters

2002

View full text Add to dashboard Cite

The two genes encoding DNA gyrase in Mycobacterium tuberculosis are present next to each other in the genome, with gyrB upstream of gyrA. We show that the primary transcript is dicistronic. However, in addition to the principal promoter, there are multiple weaker promoters that appear to fine-tune transcription. With these and other mycobacterial promoters, we propose consensus promoter sequences for two distinct sigma factors. In addition to this, the gyr genes in M. tuberculosis, as in other species, are subject to autoregulation, albeit with slower kinetics, probably reflecting the slower metabolism of the organism.Most of our understanding of prokaryotic transcription initiation is based on extensive analysis of promoter architecture in Escherichia coli. Since the regions in 70 involved in contacting the promoter show extensive conservation across the prokaryotic world (13), a similar picture for transcription initiation is expected in all bacteria. However, this does not appear always to be the case. For instance, results of earlier random promoter screens indicate that only a small fraction of mycobacterial promoters are recognized by the E. coli machinery (6, 26). Furthermore, a random promoter screen in Mycobacterium paratuberculosis detected only promoters that were highly GC-rich in both their Ϫ10 and Ϫ35 regions (2). Thus, the features that define species-specific promoters are not clear.Here we present the analysis of the transcription of the DNA gyrase genes in Mycobacterium tuberculosis. As the sole supercoiling activity in the cell, DNA gyrase faces the daunting task of opposing the relaxing activities of both topoisomerases I and IV (29). As a result, DNA gyrase is essential in all eubacterial cells that have been tested so far, and the final topology of DNA is maintained by the equilibrium achieved by these divergent forces. Since DNA gyrase needs to oppose the relaxation induced by other topoisomerases, it regulates its own synthesis by a unique mechanism. In general, transcription of most genes is induced by increased negative supercoiling. In contrast, negative supercoiling represses transcription of the gyrase genes in E. coli (15). This phenomenon, referred to as relaxation-stimulated transcription, is believed to be the cell's strategy to homeostatically maintain the topology of DNA (15). Thus, increased gyrase levels lead to an increase in supercoiling, which, in turn, repress the expression of gyrase and allow other topoisomerases to bring the topology of the DNA back to its optimum state. Relaxation-stimulated transcription appears to be conserved in all organisms tested so far (14,23,25,28); however, the underlying mechanism appears to vary (27).Therefore, there are multiple reasons to analyze the transcription of the gyr genes in M. tuberculosis, especially since the genome lacks both topoisomerases III and IV (5). In addition, since the expression of many virulence genes is dependent on the topology of DNA in many pathogenic bacteria (8), understanding the regulation of DNA gyrase in...

show abstract

Section: Discussionmentioning

confidence: 99%

DNA Gyrase Genes in Mycobacterium tuberculosis : a Single Operon Driven by Multiple Promoters

2002

View full text Add to dashboard Cite

show abstract

“…The gyrase of E. coli is actually encoded by two genes, gyrA and gyrB, physically independent on the bacterial chromosome. The gyrA expression is even more sensitive to DNA supercoiling fluctuations than gyrB (Neumann & Quiñones, ). In contrast, both gyrA and gyrB genes are organized within an operon in Streptomyces coelicolor .…”

Section: Introductionmentioning

confidence: 99%

The reverse gyrase TopR1 is responsible for the homeostatic control of DNA supercoiling in the hyperthermophilic archaeon Sulfolobus solfataricus

Couturier

Gadelle

Forterre

et al. 2019

Molecular Microbiology

View full text Add to dashboard Cite

Maintaining an appropriate DNA topology with DNA‐based processes (DNA replication, transcription and recombination) is crucial for all three domains of life. In bacteria, the homeostatic regulation for controlling DNA supercoiling relies on antagonistic activities of two DNA topoisomerases, TopoI and gyrase. In hyperthermophilic crenarchaea, the presence of such a regulatory system is suggested as two DNA topoisomerases, TopoVI and reverse gyrase, catalyze antagonistic activities. To test this hypothesis, we estimated and compared the number of the TopoVI with that of the two reverse gyrases, TopR1 and TopR2, in Sulfolobus solfataricus cells maintained either at 80 or at 88°C, or reciprocally shifted from one temperature to the other. From the three DNA topoisomerases, TopR1 is the only one exhibiting significant quantitative variations in response to the up‐ and down‐shifts. In addition, the corresponding intrinsic activities of these three DNA topoisomerases were tested in vitro at both temperatures. Although temperature modulates the three DNA topoisomerases activities, TopR1 is the sole topoisomerase able to function at high temperature. Altogether, results presented in this study demonstrate, for the first time, that the DNA topological state of a crenarchaeon is regulated via a homeostatic control, which is mainly mediated by the fine‐tuning of TopR1.

show abstract

“…The predominant response to nalidixic acid treatment is induction of the LexA-controlled SOS response (49). In addition to the SOS response, upregulation of the 32 -controlled heat shock response (18,40,45), increased activity of promoters responsive to DNA supercoiling (25,37), increased expression of emr genes (20), and other responses (13,36) are induced by nalidixic acid treatment. Accordingly, upregulation of gene fusions in two classes, fusions to genes of the LexA regulon and fusions to genes that are not part of the SOS response, was expected and was found.…”

mentioning

confidence: 99%

LuxArray, a High-Density, Genomewide Transcription Analysis of Escherichia coli Using Bioluminescent Reporter Strains

2001

View full text Add to dashboard Cite

A sequenced collection of plasmid-borne random fusions of Escherichia coli DNA to a Photorhabdus luminescens luxCDABE reporter was used as a starting point to select a set of 689 nonredundant functional gene fusions. This group, called LuxArray 1.0, represented 27% of the predicted transcriptional units in E. coli. High-density printing of the LuxArray 1.0 reporter strains to membranes on agar plates was used for simultaneous reporter gene assays of gene expression. The cellular response to nalidixic acid perturbation was analyzed using this format. As expected, fusions to promoters of LexA-controlled SOS-responsive genes dinG, dinB, uvrA, and ydjM were found to be upregulated in the presence of nalidixic acid. In addition, six fusions to genes not previously known to be induced by nalidixic acid were also reproducibly upregulated. The responses of two of these, fusions to oraA and yigN, were induced in a LexA-dependent manner by both nalidixic acid and mitomycin C, identifying these as members of the LexA regulon. The responses of the other four were neither induced by mitomycin C nor dependent on lexA function. Thus, the promoters of ycgH, intG, rihC, and a putative operon consisting of lpxA, lpxB, rnhB, and dnaE were not generally DNA damage responsive and represent a more specific response to nalidixic acid. These results demonstrate that cellular arrays of reporter gene fusions are an important alternative to DNA arrays for genomewide transcriptional analyses.

show abstract

Discoordinate gene expression of gyrA and gyrB in response to DNA gyrase inhibition in Escherichia coli

Cited by 16 publications

References 39 publications

DNA Gyrase Genes in Mycobacterium tuberculosis : a Single Operon Driven by Multiple Promoters

DNA Gyrase Genes in Mycobacterium tuberculosis : a Single Operon Driven by Multiple Promoters

The reverse gyrase TopR1 is responsible for the homeostatic control of DNA supercoiling in the hyperthermophilic archaeon Sulfolobus solfataricus

LuxArray, a High-Density, Genomewide Transcription Analysis of Escherichia coli Using Bioluminescent Reporter Strains

Contact Info

Product

Resources

About