The Coordinated Positive Regulation of Topoisomerase Genes Maintains Topological Homeostasis in Streptomyces coelicolor

Maintaining an optimal level of chromosomal supercoiling is critical for the progression of DNA replication and transcription. Moreover, changes in global supercoiling affect the expression of a large number of genes and play a fundamental role in adapting to stress. Topoisomerase I (TopA) and gyras...

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Published in:Journal of bacteriology 2016-11, Vol.198 (21), p.3016-3028
Main Authors: Szafran, Marcin Jan, Gongerowska, Martyna, Gutkowski, Paweł, Zakrzewska-Czerwińska, Jolanta, Jakimowicz, Dagmara
Format: Article
Language:English
Subjects:
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Bacteriology
Chromosomes
Deoxyribonucleic acid
DNA
DNA Gyrase - genetics
DNA Gyrase - metabolism
DNA Topoisomerases, Type I - genetics
DNA Topoisomerases, Type I - metabolism
DNA, Bacterial - genetics
DNA, Bacterial - metabolism
DNA, Superhelical - chemistry
DNA, Superhelical - metabolism
Gene Expression Regulation, Bacterial
Gene Expression Regulation, Enzymologic
Genes
Homeostasis
Operon
Promoter Regions, Genetic
Streptococcus infections
Streptomyces
Streptomyces coelicolor
Streptomyces coelicolor - enzymology
Streptomyces coelicolor - genetics
Transcription, Genetic
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Summary:Maintaining an optimal level of chromosomal supercoiling is critical for the progression of DNA replication and transcription. Moreover, changes in global supercoiling affect the expression of a large number of genes and play a fundamental role in adapting to stress. Topoisomerase I (TopA) and gyrase are key players in the regulation of bacterial chromosomal topology through their respective abilities to relax and compact DNA. Soil bacteria such as Streptomyces species, which grow as branched, multigenomic hyphae, are subject to environmental stresses that are associated with changes in chromosomal topology. The topological fluctuations modulate the transcriptional activity of a large number of genes and in Streptomyces are related to the production of antibiotics. To better understand the regulation of topological homeostasis in Streptomyces coelicolor, we investigated the interplay between the activities of the topoisomerase-encoding genes topA and gyrBA We show that the expression of both genes is supercoiling sensitive. Remarkably, increased chromosomal supercoiling induces the topA promoter but only slightly influences gyrBA transcription, while DNA relaxation affects the topA promoter only marginally but strongly activates the gyrBA operon. Moreover, we showed that exposure to elevated temperatures induces rapid relaxation, which results in changes in the levels of both topoisomerases. We therefore propose a unique mechanism of S. coelicolor chromosomal topology maintenance based on the supercoiling-dependent stimulation, rather than repression, of the transcription of both topoisomerase genes. These findings provide important insight into the maintenance of topological homeostasis in an industrially important antibiotic producer. We describe the unique regulation of genes encoding two topoisomerases, topoisomerase I (TopA) and gyrase, in a model Streptomyces species. Our studies demonstrate the coordination of topoisomerase gene regulation, which is crucial for maintenance of topological homeostasis. Streptomyces species are producers of a plethora of biologically active secondary metabolites, including antibiotics, antitumor agents, and immunosuppressants. The significant regulatory factor controlling the secondary metabolism is the global chromosomal topology. Thus, the investigation of chromosomal topology homeostasis in Streptomyces strains is crucial for their use in industrial applications as producers of secondary metabolites.
ISSN:0021-9193
1098-5530
DOI:10.1128/JB.00530-16