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The dynamic architecture of the metabolic switch in Streptomyces coelicolor

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Nieselt, Kay, Battke, Florian, Herbig, Alexander, Bruheim, Per, Wentzel, Alexander, Jakobsen, Øyvind M., Sletta, Håvard, Alam, Mohammad T., Merlo, Maria E., Moore, Jonathan D. et al.
. (2010) The dynamic architecture of the metabolic switch in Streptomyces coelicolor. BMC Genomics, Vol.11 (Article 10). ISSN 1471-2164

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Official URL: http://dx.doi.org/10.1186/1471-2164-11-10

Abstract

Background: During the lifetime of a fermenter culture, the soil bacterium S. coelicolor undergoes a major metabolic switch from exponential growth to antibiotic production. We have studied gene expression patterns during this switch, using a specifically designed Affymetrix genechip and a high-resolution time-series of fermenter-grown samples. Results: Surprisingly, we find that the metabolic switch actually consists of multiple finely orchestrated switching events. Strongly coherent clusters of genes show drastic changes in gene expression already many hours before the classically defined transition phase where the switch from primary to secondary metabolism was expected. The main switch in gene expression takes only 2 hours, and changes in antibiotic biosynthesis genes are delayed relative to the metabolic rearrangements. Furthermore, global variation in morphogenesis genes indicates an involvement of cell differentiation pathways in the decision phase leading up to the commitment to antibiotic biosynthesis. Conclusions: Our study provides the first detailed insights into the complex sequence of early regulatory events during and preceding the major metabolic switch in S. coelicolor, which will form the starting point for future attempts at engineering antibiotic production in a biotechnological setting.

Item Type: Journal Article
Subjects: Q Science > QR Microbiology
Divisions: Faculty of Science > Life Sciences (2010- ) > Biological Sciences ( -2010)
Faculty of Science > Chemistry
Faculty of Science > Centre for Systems Biology
Library of Congress Subject Headings (LCSH): Streptomyces coelicolor, Soil microbiology -- Research, Microbial metabolism -- Regulation, Antibiotics -- Synthesis, Bacteria -- Morphogenesis
Journal or Publication Title: BMC Genomics
Publisher: BioMed Central Ltd.
ISSN: 1471-2164
Date: 6 January 2010
Volume: Vol.11
Number: Article 10
Identification Number: 10.1186/1471-2164-11-10
Status: Peer Reviewed
Access rights to Published version: Open Access
Funder: European Commission (EC), Norges forskningsråd [Norwegian Research Council]
Grant number: GEN2006- 27745-E/SYS: P-UK-01-11-3i (SySMO), 181840/I30 (NF)
References: 1. Kolter R, Siegele DA, Tormo A: The stationary phase of the bacterial life cycle. Annu Rev Microbiol 1993, 47:855-874. 2. Hesketh A, Bucca G, Laing E, Flett F, Hotchkiss G, Smith CP, Chater KF: New pleiotropic effects of eliminating a rare tRNA from Streptomyces coelicolor, revealed by combined proteomic and transcriptomic analysis of liquid cultures. BMC Genomics 2007, 8:261. 3. Hesketh A, Chen WJ, Ryding J, Chang S, Bibb M: The global role of ppGpp synthesis in morphological differentiation and antibiotic production in Streptomyces coelicolor A3(2). Genome Biol 2007, 8(8):R161. 4. Huang J, Lih CJ, Pan KH, Cohen SN: Global analysis of growth phase responsive gene expression and regulation of antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays. Genes Dev 2001, 15(23):3183-3192. 5. Lian W, Jayapal KP, Charaniya S, Mehra S, Glod F, Kyung YS, Sherman DH, Hu WS: Genome-wide transcriptome analysis reveals that a pleiotropic antibiotic regulator, AfsS, modulates nutritional stress response in Streptomyces coelicolor A3(2). BMC Genomics 2008, 9:56. 6. Strauch E, Takano E, Baylis HA, Bibb MJ: The stringent response in Streptomyces coelicolor A3(2). Mol Microbiol 1991, 5(2):289-298. 7. DeRisi JL, Iyer VR, Brown PO: Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 1997, 278(5338):680-686. 8. Reuther J, Wohlleben W: Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 2007, 12(1-2):139-146. 9. Fink D, Weissschuh N, Reuther J, Wohlleben W, Engels A: Two transcriptional regulators GlnR and GlnRII are involved in regulation of nitrogen metabolism in Streptomyces coelicolor A3(2). Mol Microbiol 2002, 46(2):331-347. 10. Tiffert Y, Supra P, Wurm R, Wohlleben W, Wagner R, Reuther J: The Streptomyces coelicolor GlnR regulon: identification of new GlnR targets and evidence for a central role of GlnR in nitrogen metabolism in actinomycetes. Mol Microbiol 2008, 67(4):861-880. 11. Pawlik K, Kotowska M, Chater KF, Kuczek K, Takano E: A cryptic type I polyketide synthase (cpk) gene cluster in Streptomyces coelicolor A3(2). Arch Microbiol 2007, 187(2):87-99. 12. Takano E, Chakraburtty R, Nihira T, Yamada Y, Bibb MJ: A complex role for the gamma-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 2001, 41(5):1015-1028. 13. Takano E, Kinoshita H, Mersinias V, Bucca G, Hotchkiss G, Nihira T, Smith CP, Bibb M, Wohlleben W, Chater K: A bacterial hormone (the SCB1) directly controls the expression of a pathway-specific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol 2005, 56(2):465-479. 14. Kotowska M, Pawlik K, Smulczyk-Krawczyszyn A, Bartosz-Bechowski H, Kuczek K: Type II thioesterase ScoT, associated with Streptomyces coelicolor A3(2) modular polyketide synthase Cpk, hydrolyzes acyl residues and has a preference for propionate. Appl Environ Microbiol 2009, 75(4):887-896. 15. Claessen D, Rink R, de Jong W, Siebring J, de Vreugd P, Boersma FG, Dijkhuizen L, Wosten HA: A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 2003, 17(14):1714-1726. 16. Bibb MJ, Molle V, Buttner MJ: sigma(BldN), an extracytoplasmic function RNA polymerase sigma factor required for aerial mycelium formation in Streptomyces coelicolor A3(2). J Bacteriol 2000, 182(16):4606-4616. 17. Ryding NJ, Kelemen GH, Whatling CA, Flardh K, Buttner MJ, Chater KF: A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol Microbiol 1998, 29(1):343-357. 18. Ohnishi Y, Seo JW, Horinouchi S: Deprogrammed sporulation in Streptomyces. FEMS Microbiol Lett 2002, 216(1):1-7. 19. Sola-Landa A, Moura RS, Martín JF: The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA 2003, 100(10):6133-6138. 20. Sola-Landa A, Rodríguez-García A, Franco-Domínguez E, Martín JF: Binding of PhoP to promoters of phosphate-regulated genes in Streptomyces coelicolor: identification of PHO boxes. Mol Microbiol 2005, 56(5):1373- 1385. 21. Rodríguez-García A, Barreiro C, Santos-Beneit F, Sola-Landa A, Martín JF: Genome-wide transcriptomic and proteomic analysis of the primary response to phosphate limitation in Streptomyces coelicolor M145 and in a ΔphoP mutant. Proteomics 2007, 7(14):2410-2429. 22. Sola-Landa A, Rodríguez-García A, Apel AK, Martín JF: Target genes and structure of the direct repeats in the DNA-binding sequences of the response regulator PhoP in Streptomyces coelicolor. Nucleic Acids Res 2008, 36(4):1358-1368. 23. Feitelson JS, Malpartida F, Hopwood DA: Genetic and biochemical characterization of the red gene cluster of Streptomyces coelicolor A3 (2). J Gen Microbiol 1985, 131(9):2431-2441. 24. Hallam SE, Malpartida F, Hopwood DA: Nucleotide sequence, transcription and deduced function of a gene involved in polyketide antibiotic synthesis in Streptomyces coelicolor. Gene 1988, 74(2):305-320. 25. Takano E, Gramajo HC, Strauch E, Andres N, White J, Bibb MJ: Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase-dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2). Mol Microbiol 1992, 6(19):2797-2804. 26. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA: Practical Streptomyces Genetics. Norwich: John Innes Foundation 2000. 27. Bystrykh LV, Fernandez-Moreno MA, Herrema JK, Malpartida F, Hopwood DA, Dijkhuizen L: Production of actinorhodin-related "blue pigments" by Streptomyces coelicolor A3(2). J Bacteriol 1996, 178(8):2238-2244. 28. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP: Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003, 31(4): e15. 29. Ihaka R, Gentleman R: R: A Language for Data Analysis and Graphics. Journal of Computational and Graphical Statistics 2005, 5:299-314. 30. Dietzsch J, Gehlenborg N, Nieselt K: Mayday–a microarray data analysis workbench. Bioinformatics 2006, 22(8):1010-1012.
URI: http://wrap.warwick.ac.uk/id/eprint/2915

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