Genome-wide analysis of in vivo binding of the master regulator DasR in Streptomyces coelicolor identifies novel non-canonical targets

Streptomycetes produce a wealth of natural products, including over half of all known antibiotics. It was previously demonstrated that N-acetylglucosamine and secondary metabolism are closely entwined in streptomycetes. Here we show that DNA recognition by the N-acetylglucosamine-responsive regulato...

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Bibliographic Details
Published in:PloS one 2015-04, Vol.10 (4), p.e0122479-e0122479
Main Authors: Świątek-Połatyńska, Magdalena A, Bucca, Giselda, Laing, Emma, Gubbens, Jacob, Titgemeyer, Fritz, Smith, Colin P, Rigali, Sébastien, van Wezel, Gilles P
Format: Article
Language:English
Subjects:
Acetylglucosamine - metabolism
Anti-Bacterial Agents - metabolism
Antibiotics
Bacteria
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Binding
Bioinformatics
Biology
Biosynthesis
Biotechnology
Carbon
Cloning
Deoxyribonucleic acid
DNA
E coli
Escherichia coli
Gene expression
Gene Expression Profiling
Gene Expression Regulation, Bacterial
Genes
Genome, Bacterial - genetics
Genomes
Genomics
Glucose
Kinases
Laboratories
Life sciences
Metabolism
Metabolites
Microbiologie
Microbiology
N-Acetylglucosamine
Natural products
Nitrogen
Oligonucleotide Array Sequence Analysis
Physiological aspects
Promoter Regions, Genetic - genetics
Protein Binding
Regulators
Regulon - genetics
Response Elements - genetics
Sciences du vivant
Streptomyces
Streptomyces coelicolor
Streptomyces coelicolor - genetics
Streptomyces coelicolor - metabolism
Streptomycetes
Target recognition
Transcription Factors - genetics
Transcription Factors - metabolism
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Summary:Streptomycetes produce a wealth of natural products, including over half of all known antibiotics. It was previously demonstrated that N-acetylglucosamine and secondary metabolism are closely entwined in streptomycetes. Here we show that DNA recognition by the N-acetylglucosamine-responsive regulator DasR is growth-phase dependent, and that DasR can bind to sites in the S. coelicolor genome that have no obvious resemblance to previously identified DasR-responsive elements. Thus, the regulon of DasR extends well beyond what was previously predicted and includes a large number of genes with functions far removed from N-acetylglucosamine metabolism, such as genes for small RNAs and DNA transposases. Conversely, the DasR regulon during vegetative growth largely correlates to the presence of canonical DasR-responsive elements. The changes in DasR binding in vivo following N-acetylglucosamine induction were studied in detail and a possible molecular mechanism by which the influence of DasR is extended is discussed. Discussion of DasR binding was further informed by a parallel transcriptome analysis of the respective cultures. Evidence is provided that DasR binds directly to the promoters of all genes encoding pathway-specific regulators of antibiotic production in S. coelicolor, thereby providing an exquisitely simple link between nutritional control and secondary metabolism.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0122479