Gamma-butyrolactone regulatory system of Streptomyces chattanoogensis links nutrient utilization, metabolism, and development

Applied and Environmental Microbiology

Volumn 77, Issue 23, 2011, Pages 8415-8426

  Du, Yi Ling ^a   Shen, Xue Ling ^a   Yu, Pin ^a   Bai, Lin Quan ^b   Li, Yong Quan ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE RESPONSE; ANTIBIOTIC PRODUCTION; ANTIFUNGAL AGENTS; CARBON UPTAKE; GROWTH DEFECTS; NUTRIENT UTILIZATION; PROMOTER REGION; PROTEOMIC ANALYSIS; QUORUM-SENSING; REGULATORY SYSTEMS; SECONDARY METABOLISM; SECONDARY METABOLITES; SIGNALING MOLECULES; SOLID MEDIUM; STREPTOMYCES SPECIES; STRESS RESPONSE; SUBMERGED CULTURES; TRANSCRIPTIONAL ANALYSIS;

BACTERIA; BIOCHEMISTRY; GENES; METABOLITES; NUTRIENTS; PHYSIOLOGY; TRANSCRIPTION;

METABOLISM;

BACTERIAL PROTEIN; GAMMA BUTYROLACTONE; PROTEOME; REPRESSOR PROTEIN;

ANTIBIOTICS; BACTERIUM; GENOMICS; METABOLISM; MOLECULAR ANALYSIS; MORPHOLOGY; PROTEOMICS; SECONDARY METABOLITE; SIGNALING;

ARTICLE; BACTERIAL GENE; DNA SEQUENCE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; PROTEIN BINDING; QUORUM SENSING; STREPTOMYCES;

4-BUTYROLACTONE; BACTERIAL PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEOME; QUORUM SENSING; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; STREPTOMYCES;

EID: 83255192300     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.05898-11     Document Type: Article

References (35)

1. Akanuma, G., H. Hara, Y. Ohnishi, and S. Horinouchi. 2009. Dynamic changes in the extracellular proteome caused by absence of a pleiotropic regulator AdpA in Streptomyces griseus. Mol. Microbiol. 73:898-912.
2. Aparicio, J. F., R. Fouces, M. V. Mendes, N. Olivera, and J. F. Martin. 2000. A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis. Chem. Biol. 7:895-905.
3. Borodina, I., et al. 2008. Antibiotic overproduction in Streptomyces coelicolor A3(2) mediated by phosphofructokinase deletion. J. Biol. Chem. 283:25186-25199.
4. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
5. Chugani, S., and E. P. Greenberg. 2010. LuxR homolog-independent gene regulation by acyl-homoserine lactones in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 107:10673-10678.
6. Corre, C., L. Song, S. O'Rourke, K. F. Chater, and G. L. Challis. 2008. 2-Alkyl-4-hydroxymethylfuran-3-carboxylic acids, antibiotic production inducers discovered by Streptomyces coelicolor genome mining. Proc. Natl. Acad. Sci. U. S. A. 105:17510-17515.
7. den Hengst, C. D., et al. 2010. Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol. Microbiol. 78:361-379.
8. Du, Y. L., et al. 2009. Identification of a novel Streptomyces chattanoogensis L10 and enhancing its natamycin production by overexpressing positive regulator ScnRII. J. Microbiol. 47:506-513.
9. Du, Y. L., et al. 2011. The pleiotropic regulator AdpAch is required for natamycin biosynthesis and morphological differentiation in Streptomyces chattanoogensis. Microbiology 157:1300-1311.
10. Folcher, M., et al. 2001. Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J. Biol. Chem. 276:44297-44306.
11. Gust, B., G. L. Challis, K. Fowler, T. Kieser, and K. F. Chater. 2003. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc. Natl. Acad. Sci. U. S. A. 100:1541-1546.
12. Horinouchi, S. 2002. A microbial hormone, A-factor, as a master switch for morphological differentiation and secondary metabolism in Streptomyces griseus. Front. Biosci. 7:d2045-2057.
13. Hsiao, N. H., et al. 2007. ScbA from Streptomyces coelicolor A3(2) has homology to fatty acid synthases and is able to synthesize gamma-butyrolactones. Microbiology 153:1394-1404.
14. Kato, J. Y., N. Funa, H. Watanabe, Y. Ohnishi, and S. Horinouchi. 2007. Biosynthesis of gamma-butyrolactone autoregulators that switch on secondary metabolism and morphological development in Streptomyces. Proc. Natl. Acad. Sci. U. S. A. 104:2378-2383.
15. Kawachi, R., et al. 2000. Identification of an AfsA homologue (BarX) from Streptomyces virginiae as a pleiotropic regulator controlling autoregulator biosynthesis, virginiamycin biosynthesis and virginiamycin M1 resistance. Mol. Microbiol. 36:302-313.
16. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, United Kingdom.
17. Kitani, S., M. Doi, T. Shimizu, A. Maeda, and T. Nihira. 2010. Control of secondary metabolism by farX, which is involved in the gamma-butyrolactone biosynthesis of Streptomyces lavendulae FRI-5. Arch. Microbiol. 192:211-220.
18. Kitani, S., H. Kinoshita, T. Nihira, and Y. Yamada. 1999. In vitro analysis of the butyrolactone autoregulator receptor protein (FarA) of Streptomyces lavendulae FRI-5 reveals that FarA acts as a DNA-binding transcriptional regulator that controls its own synthesis. J. Bacteriol. 181:5081-5084.
19. Lee, Y. J., S. Kitani, and T. Nihira. 2010. Null mutation analysis of an afsA-family gene, barX, that is involved in biosynthesis of the γ-butyrolactone autoregulator in Streptomyces virginiae. Microbiology 156:206-210.
20. Leesong, M., B. S. Henderson, J. R. Gillig, J. M. Schwab, and J. L. Smith. 1996. Structure of a dehydratase-isomerase from the bacterial pathway for biosynthesis of unsaturated fatty acids: two catalytic activities in one active site. Structure 4:253-264.
21. Manteca, A., R. Alvarez, N. Salazar, P. Yague, and J. Sanchez. 2008. Mycelium differentiation and antibiotic production in submerged cultures of Streptomyces coelicolor. Appl. Environ. Microbiol. 74:3877-3886.
22. Manteca, A., H. R. Jung, V. Schwammle, O. N. Jensen, and J. Sanchez. 2010. Quantitative proteome analysis of Streptomyces coelicolor nonsporulating liquid cultures demonstrates a complex differentiation process comparable to that occurring in sporulating solid cultures. J. Proteome Res. 9:4801-4811.
23. Ng, W. L., and B. L. Bassler. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43:197-222.
24. Novotna, J., et al. 2003. Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stressinduced proteins and central metabolic enzymes. Mol. Microbiol. 48:1289-1303.
25. Pan, Y., G. Liu, H. Yang, Y. Tian, and H. Tan. 2009. The pleiotropic regulator AdpA-L directly controls the pathway-specific activator of nikkomycin biosynthesis in Streptomyces ansochromogenes. Mol. Microbiol. 72: 710-723.
26. Recio, E., A. Colinas, A. Rumbero, J. F. Aparicio, and J. F. Martin. 2004. PI factor, a novel type quorum-sensing inducer elicits pimaricin production in Streptomyces natalensis. J. Biol. Chem. 279:41586-41593.
27. Rigali, S., et al. 2006. The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links Nacetylglucosamine metabolism to the control of development. Mol. Microbiol. 61:1237-1251.
28. Rigali, S., et al. 2008. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep. 9:670-675.
29. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
30. Shikura, N., J. Yamamura, and T. Nihira. 2002. barS1, a gene for biosynthesis of a gamma-butyrolactone autoregulator, a microbial signaling molecule eliciting antibiotic production in Streptomyces species. J. Bacteriol. 184: 5151-5157.
31. Takano, E. 2006. Gamma-butyrolactones: Streptomyces signaling molecules regulating antibiotic production and differentiation. Curr. Opin. Microbiol. 9:287-294.
32. Takano, E., R. Chakraburtty, T. Nihira, Y. Yamada, and M. J. Bibb. 2001. A complex role for the gamma-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 41:1015-1028.
33. Takano, E., et al. 2000. Purification and structural determination of SCB1, a gamma-butyrolactone that elicits antibiotic production in Streptomyces coelicolor A3(2). J. Biol. Chem. 275:11010-11016.
34. Viollier, P. H., W. Minas, G. E. Dale, M. Folcher, and C. J. Thompson. 2001. Role of acid metabolism in Streptomyces coelicolor morphological differentiation and antibiotic biosynthesis. J. Bacteriol. 183:3184-3192.
35. Vohradsky, J., et al. 2000. Developmental control of stress stimulons in Streptomyces coelicolor revealed by statistical analyses of global gene expression patterns. J. Bacteriol. 182:4979-4986.