The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor.
Streptomycetes are mycelial soil bacteria that undergo a developmental programme that leads to sporulating aerial hyphae. As soil-dwelling bacteria, streptomycetes rely primarily on natural polymers such as cellulose, xylan and chitin for the colonization of their environmental niche and therefore these polysaccharides may play a critical role in monitoring the global nutritional status of the environment. In this work we analysed the role of DasA, the sugar-binding component of the chitobiose ATP-binding cassette transport system, in informing the cell of environmental conditions, and its role in the onset of development and in ensuring correct sporulation. The chromosomal interruption of dasA resulted in a carbon-source-dependent vegetative arrest phenotype, and we identified a second DasR-dependent sugar transporter, in addition to the N-acetylglucosamine phosphotransferase system (PTS(GlcNAc)), that relates primary metabolism to development. Under conditions that allowed sporulation, highly aberrant spores with many prematurely produced germ tubes were observed. While GlcNAc locks streptomycetes in the vegetative state, a high extracellular concentration of the GlcNAc polymer chitin has no effect on development. The striking distinction is due to a difference in the transporters responsible for the import of GlcNAc, which enters via the PTS, and of chitin, which enters as the hydrolytic product chitobiose (GlcNAc(2)) through the DasABC transporter. A model explaining the role of these two essentially different transport systems in the control of development is provided.
Colson
Séverine
S
Centre d'Ingénierie des Protéines, Université de Liège, Institut de Chimie B6a, B-4000 Liège, Belgium.
van Wezel
Gilles P
GP
Microbial Development, Leiden Institute of Chemistry, Leiden University, PO Box 9502, 2300 RA Leiden, The Netherlands.
Craig
Matthias
M
Centre d'Ingénierie des Protéines, Université de Liège, Institut de Chimie B6a, B-4000 Liège, Belgium.
Noens
Elke E E
EEE
Microbial Development, Leiden Institute of Chemistry, Leiden University, PO Box 9502, 2300 RA Leiden, The Netherlands.
Nothaft
Harald
H
Lehrstuhl für Mikrobiologie, Friedrich-Alexander-Universität Erlangen-Nürnberg, Staudtstrasse 5, 91058 Erlangen, Germany.
Mommaas
A Mieke
AM
Center for Electron Microscopy, Leiden University Medical Center, Leiden, The Netherlands.
Titgemeyer
Fritz
F
Lehrstuhl für Mikrobiologie, Friedrich-Alexander-Universität Erlangen-Nürnberg, Staudtstrasse 5, 91058 Erlangen, Germany.
Joris
Bernard
B
Centre d'Ingénierie des Protéines, Université de Liège, Institut de Chimie B6a, B-4000 Liège, Belgium.
Rigali
Sébastien
S
Centre d'Ingénierie des Protéines, Université de Liège, Institut de Chimie B6a, B-4000 Liège, Belgium.
D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000378:metabolism*; D002686:Chitin / Q000378:metabolism*; D004187:Disaccharides / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial; D008855:Microscopy, Electron, Scanning; D046529:Microscopy, Electron, Transmission; D008958:Models, Molecular; D009154:Mutation; D010641:Phenotype; D020133:Reverse Transcriptase Polymerase Chain Reaction; D048372:Streptomyces coelicolor / Q000166:cytology / Q000254:growth & development* / Q000648:ultrastructure
D018528:ATP-Binding Cassette Transporters; D001426:Bacterial Proteins; D004187:Disaccharides; D002686:Chitin; C032438:chitobiose