A role for topoisomerase<scp>III</scp>in<i><scp>E</scp>scherichia coli</i>chromosome segregation

Perez-Cheeks, Brenda A.; Lee, Chong; Hayama, Ryo; Marians, Kenneth J.

doi:10.1111/mmi.12039

Cited by 43 publications

(58 citation statements)

References 46 publications

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“…However, as shown in our paper and as stated above, a significant interplay between topB and this gyrB(Ts) allele could be seen only when topA was also deleted. Therefore, while the paper by Perez-Cheeks et al (47) clearly reveals an interplay between Topo III and Topo IV in chromosomal segregation, our paper shows an interplay between Topo III and gyrase in this process.…”

Section: Discussionmentioning

confidence: 40%

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Interplay between Type 1A Topoisomerases and Gyrase in Chromosome Segregation in Escherichia coli

et al. 2013

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Escherichia coli possesses two type 1A topoisomerases, Topo I (topA) and Topo III (topB). Topo I relaxes excess negative supercoiling, and topA mutants can grow only in the presence of compensatory mechanisms, such as gyrase mutations. topB mutants grow as well as wild-type cells. In vitro, Topo III, but not Topo I, can efficiently decatenate DNA during replication. However, in vivo, a chromosome segregation defect is seen only when both type 1A topoisomerases are absent. Here we present experimental evidence for an interplay between gyrase and type 1A topoisomerases in chromosome segregation. We found that both the growth defect and the Par ؊ phenotypes of a gyrB(Ts) mutant at nonpermissive temperatures were significantly corrected by deleting topA, but only when topB was present. Overproducing Topo IV, the major cellular decatenase, could not substitute for topB. We also show that overproducing Topo III at a very high level could suppress the Par ؊ phenotype. We previously found that the growth and chromosome segregation defects of a triple topA rnhA gyrB(Ts) mutant in which gyrase supercoiling activity was strongly inhibited could be corrected by overproducing Topo III (V. Usongo, F. Nolent, P. Sanscartier, C. Tanguay, S. Broccoli, I. Baaklini, K. Drlica, and M. Drolet, Mol. Microbiol. 69:968-981, 2008). We show here that this overproduction could be bypassed by substituting the gyrB(Ts) allele for a gyrB ؉ one or by growing cells in a minimal medium, conditions that reduced both topA-and rnhA-dependent unregulated replication. Altogether, our data point to a role for Topo III in chromosome segregation when gyrase is inefficient and suggest that Topo I plays an indirect role via supercoiling regulation.

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Section: Discussionmentioning

confidence: 40%

“…While our manuscript was in preparation, a paper was published that demonstrated an interplay between Topo III and Topo IV in chromosome segregation in E. coli (47). However, no clues were provided as to when one specific topoisomerase would be required to allow chromosome segregation to occur.…”

Section: Discussionmentioning

confidence: 99%

Interplay between Type 1A Topoisomerases and Gyrase in Chromosome Segregation in Escherichia coli

et al. 2013

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“…1). A related topoisomerase, Topo III (topB), contributes weak DNA relaxing activity but acts chiefly as a decatenase (Nurse et al 2003;Perez-Cheeks et al 2012). Drugs are available that inhibit gyrase and Topo IV.…”

Section: Introductionmentioning

confidence: 99%

“…Of these, novobiocin is particularly useful because it interferes with ATP binding in a dose-dependent manner (Hardy and Cozzarelli 2003;Khodursky et al 1995;Sugino et al 1978). Experiments investigating the in vivo effects of the loss of Topo I and III have mainly relied on the use of strains with mutations in their respective genes, topA (Margolin et al 1985) and topB (Perez-Cheeks et al 2012). …”

Section: Introductionmentioning

confidence: 99%

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Dorman

2016

Biophys Rev

107

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Although it has become routine to consider DNA in terms of its role as a carrier of genetic information, it is also an important contributor to the control of gene expression. This regulatory principle arises from its structural properties. DNA is maintained in an underwound state in most bacterial cells and this has important implications both for DNA storage in the nucleoid and for the expression of genetic information. Underwinding of the DNA through reduction in its linking number potentially imparts energy to the duplex that is available to drive DNA transactions, such as transcription, replication and recombination. The topological state of DNA also influences its affinity for some DNA binding proteins, especially in DNA sequences that have a high A + T base content. The underwinding of DNA by the ATP-dependent topoisomerase DNA gyrase creates a continuum between metabolic flux, DNA topology and gene expression that underpins the global response of the genome to changes in the intracellular and external environments. These connections describe a fundamental and generalised mechanism affecting global gene expression that underlies the specific control of transcription operating through conventional transcription factors. This mechanism also provides a basal level of control for genes acquired by horizontal DNA transfer, assisting microbial evolution, including the evolution of pathogenic bacteria.

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“…The main role of these enzymes is to remove the topological tension created during replication, transcription, and recombination. Chromosome segregation requires the decatenase activity of topoisomerases (mostly topoisomerase IV) to separate the interlinked circular chromosomes (27,28). The decatenation of chromosomes may be performed in cooperation with XerCD recombinases, which are responsible for the topological mainte-nance of circular chromosomes (29).…”

Section: Mers) Varied Numbers Of Pars Sites (From 3 In Vibrio Choleraementioning

confidence: 99%

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

et al. 2013

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c Streptomyces species are bacteria that resemble filamentous fungi in their hyphal mode of growth and sporulation. In Streptomyces coelicolor, the conversion of multigenomic aerial hyphae into chains of unigenomic spores requires synchronized septation accompanied by segregation of tens of chromosomes into prespore compartments. The chromosome segregation is dependent on ParB protein, which assembles into an array of nucleoprotein complexes in the aerial hyphae. Here, we report that nucleoprotein ParB complexes are bound in vitro and in vivo by topoisomerase I, TopA, which is the only topoisomerase I homolog found in S. coelicolor. TopA cannot be eliminated, and its depletion inhibits growth and blocks sporulation. Surprisingly, sporulation in the TopA-depleted strain could be partially restored by deletion of parB. Furthermore, the formation of regularly spaced ParB complexes, which is a prerequisite for proper chromosome segregation and septation during the development of aerial hyphae, has been found to depend on TopA. We hypothesize that TopA is recruited to ParB complexes during sporulation, and its activity is required to resolve segregating chromosomes.

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A role for topoisomeraseIIIinEscherichia colichromosome segregation

Cited by 43 publications

References 46 publications

Interplay between Type 1A Topoisomerases and Gyrase in Chromosome Segregation in Escherichia coli

Interplay between Type 1A Topoisomerases and Gyrase in Chromosome Segregation in Escherichia coli

DNA supercoiling is a fundamental regulatory principle in the control of bacterial gene expression

Topoisomerase I (TopA) Is Recruited to ParB Complexes and Is Required for Proper Chromosome Organization during Streptomyces coelicolor Sporulation

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